176.Crespi, B. (2021) Pattern Unifies Autism.Front. Psychiatry 12 Pattern Unifies Autism
autism; repetitive behavior; systemizing; social cognition; pattern; psychosis
Autism is a highly heterogeneous condition, genetically and phenotypically. This diversity of causation and presentation has impeded its definition, recognition, assessment, and treatment. Current diagnostic criteria for autism involve two domains, restricted interests and repetitive behavior (RRBs) and social deficits, whose relationship remains unclear. I suggest that the large suite of traits associated with autism can be usefully conceptualized under the single rubric of "pattern," a term that connects autism with basic brain and cognitive functions and structures its phenotypes within a single theoretical framework. Autism thus involves increases and enhancements to pattern perception, pattern recognition, pattern maintenance, pattern generation, pattern processing, and pattern seeking. RRBs result from increased and imbalanced pattern-related perception and cognition, and social alterations result in part from the usual lack of clear pattern in social interactions, combined with the interference of RRBs with social development. This framework has strong implications for assessment of social and non-social autism-related traits, personalized therapy, and priorities for research. DOI PubMed
175.Crespi, B; Alcock, J. (2021) Conflicts over calcium and the treatment of COVID-19.Evol. Med. Public Health 9: 149-156 Conflicts over calcium and the treatment of COVID-19
SARS-CoV-2; COVID-19; conflict; hypocalcemia; calcium
Several recent studies have provided evidence that use of calcium channel blockers (CCBs), especially amlodipine and nifedipine, can reduce mortality from coronavirus disease 2019 (COVID-19). Moreover, hypocalcemia (a reduced level of serum ionized calcium) has been shown to be strongly positively associated with COVID-19 severity. Both effectiveness of CCBs as antiviral therapy, and positive associations of hypocalcemia with mortality, have been demonstrated for many other viruses as well. We evaluate these findings in the contexts of virus-host evolutionary conflicts over calcium metabolism, and hypocalcemia as either pathology, viral manipulation or host defence against pathogens. Considerable evidence supports the hypothesis that hypocalcemia represents a host defence. Indeed, hypocalcemia may exert antiviral effects in a similar manner as do CCBs, through interference with calcium metabolism in virus-infected cells. Prospective clinical studies that address the efficacy of CCBs and hypocalcemia should provide novel insights into the pathogenicity and treatment of COVID-19 and other viruses. DOI PubMed
174. Dinsdale, NL; Crespi, BJ. (2021) Endometriosis and polycystic ovary syndrome are diametric disorders.Evol. Appl. 14: 1693-1715 Endometriosis and polycystic ovary syndrome are diametric disorders
anogenital distance; endometriosis; folliculogenesis; polycystic ovary syndrome; testosterone
Evolutionary and comparative approaches can yield novel insights into human adaptation and disease. Endometriosis and polycystic ovary syndrome (PCOS) each affect up to 10% of women and significantly reduce the health, fertility, and quality of life of those affected. PCOS and endometriosis have yet to be considered as related to one another, although both conditions involve alterations to prenatal testosterone levels and atypical functioning of the hypothalamic-pituitary-gonadal (HPG) axis. Here, we propose and evaluate the novel hypothesis that endometriosis and PCOS represent extreme and diametric (opposite) outcomes of variation in HPG axis development and activity, with endometriosis mediated in notable part by low prenatal and postnatal testosterone, while PCOS is mediated by high prenatal testosterone. This diametric disorder hypothesis predicts that, for characteristics shaped by the HPG axis, including hormonal profiles, reproductive physiology, life-history traits, and body morphology, women with PCOS and women with endometriosis will manifest opposite phenotypes. To evaluate these predictions, we review and synthesize existing evidence from developmental biology, endocrinology, physiology, life history, and epidemiology. The hypothesis of diametric phenotypes between endometriosis and PCOS is strongly supported across these diverse fields of research. Furthermore, the contrasts between endometriosis and PCOS in humans parallel differences among nonhuman animals in effects of low versus high prenatal testosterone on female reproductive traits. These findings suggest that PCOS and endometriosis represent maladaptive extremes of both female life-history variation and expression of sexually dimorphic female reproductive traits. The diametric disorder hypothesis for endometriosis and PCOS provides novel, unifying, proximate, and evolutionary explanations for endometriosis risk, synthesizes diverse lines of research concerning the two most common female reproductive disorders, and generates future avenues of research for improving the quality of life and health of women. DOI PubMed
173. Nahal, P; Hurd, PL; Read, S; Crespi, B. (2021) Cognitive Empathy as Imagination: Evidence From Reading the Mind in the Eyes in Autism and Schizotypy.Front. Psychiatry 12 Cognitive Empathy as Imagination: Evidence From Reading the Mind in the Eyes in Autism and Schizotypy
empathy; autism; schizotypy; RMET; imagination; sociality
How is cognitive empathy related to sociality, imagination, and other psychological constructs? How is it altered in disorders of human social cognition? We leveraged a large data set (1,168 students, 62% female) on the Reading the Mind in the Eyes test (RMET), the Autism Quotient (AQ), and the Schizotypal Personality Questionnaire (SPQ-BR) to test the hypotheses that the RMET, as a metric of cognitive empathy, reflects mainly social abilities, imagination, or both. RMET showed the expected female bias in performance, though only for eyes that expressed emotions and not for neutral expressions. RMET performance was significantly, and more strongly, associated with the AQ and SPQ subscales that reflect aspects of imagination (AQ-Imagination and SPQ-Magical Ideation) than aspects of social abilities (AQ-Social, AQ-Communication, and SPQ-Interpersonal subscales). These results were confirmed with multiple regression analysis, which also implicated increased attention (AQ-Attention Switching and, marginally non-significantly, AQ-Attention to Detail) in RMET performance. The two imagination-related correlates of RMET performance also show the strongest sex biases for the AQ and SPQ: male biased in AQ-Imagination, and female biased in SPQ-Magical Ideation, with small to medium effect sizes. Taken together, these findings suggest that cognitive empathy, as quantified by the RMET, centrally involves imagination, which is underdeveloped (with a male bias) on the autism spectrum and overdeveloped (with a female bias) on the schizotypy spectrum, with optimal emotion-recognition performance intermediate between the two. The results, in conjunction with previous studies, implicate a combination of optimal imagination and focused attention in enhanced RMET performance. DOI PubMed
171.Crespi, B. (2020) Evolutionary medical insights into the SARS-CoV-2 pandemic.Evol. Med. Public Health : 314-322 Evolutionary medical insights into the SARS-CoV-2 pandemic
COVID-19; SARS-CoV-2; inflammation; interferon; coronavirus; amlodipine
The author apply concepts and tools from evolutionary medicine to understanding the SARS-CoV-2 pandemic. The pandemic represents a mismatched conflict, with dynamics and pathology apparently driven by three main factors: (i) bat immune systems that rely on low inflammation but high efficacy of interferon-based defenses; (ii) viral tactics that differentially target the human interferon system, leading to substantial asymptomatic and pre-symptomatic transmission; and (ii) high mortality caused by hyper-inflammatory and hyper-coagulatory phenotypes, that represent dysregulated tradeoffs whereby collateral immune-induced damage becomes systemic and severe. This framework can explain the association of mortality with age (which involves immune life-history shifts towards higher inflammation and coagulation and reduced adaptive immunity), and sex (since males senesce faster than females). Genetic-risk factors for COVID-19 mortality can be shown, from a phenome-wide association analysis of the relevant SNPs, to be associated with inflammation and coagulation; the phenome-wide association study also provides evidence, consistent with several previous studies, that the calcium channel blocking drug amlodipine mediates risk of mortality. Lay Summary: SARS-CoV-2 is a bat virus that jumped into humans. The virus is adapted to bat immune systems, where it evolved to suppress the immune defenses (interferons) that mammals use to tell that they are infected. In humans, the virus can apparently spread effectively in the body with a delay in the production of symptoms and the initiation of immune responses. This delay may then promote overactive immune responses, when the virus is detected, that damage the body as a side effect. Older people are more vulnerable to the virus because they are less adapted to novel infectious agents, and invest less in immune defense, compared to younger people. Genes that increase risk of mortality from SARS-CoV-2 are functionally associated with a drug called amlodipine, which may represent a useful treatment. DOI PubMed
170.Crespi, BJ. (2020) Why and How Imprinted Genes Drive Fetal Programming.Front. Endocrinol. 10 Why and How Imprinted Genes Drive Fetal Programming
genomic imprinting; fetal programming; metabolic syndrome; type 2 diabetes; mother-offspring conflict
Imprinted genes mediate fetal and childhood growth and development, and early growth patterns drive fetal programming effects. However, predictions and evidence from the kinship theory of imprinting have yet to be directly integrated with data on fetal programming and risks of metabolic disease. I first define paternal-gene and maternal-gene optima with regard to early human growth and development. Next, I review salient evidence with regard to imprinted gene effects on birth weight, body composition, trajectories of feeding and growth, and timing of developmental stages, to evaluate why and how imprinted gene expression influences risks of metabolic disease in later life. I find that metabolic disease risks derive primarily from maternal gene biases that lead to reduced placental efficacy, low birth weight, low relative muscle mass, high relative white fat, increased abdominal adiposity, reduced pancreatic beta-cell mass that promotes insulin resistance, reduced appetite and infant sucking efficacy, catch-up fat deposition from family foods after weaning, and early puberty. Paternal gene biases, by contrast, may contribute to metabolic disease via lower rates of brown fat thermiogenesis, and through favoring more rapid postnatal catch-up growth after intrauterine growth restriction from environmental causes. These disease risks can be alleviated through dietary and pharmacological alterations that selectively target imprinted gene expression and relevant metabolic pathways. The kinship theory of imprinting, and mother-offspring conflict more generally, provide a clear predictive framework for guiding future research on fetal programming and metabolic disease. DOI PubMed
169.Crespi, BJ. (2020) Evolutionary and genetic insights for clinical psychology.Clin. Psychol. Rev. 78 Evolutionary and genetic insights for clinical psychology
Evolutionary biology; Fitness; Genomics; Adaptation; Dynamical systems
Recent advances in genetics, and new applications of evolutionary biology, are transforming psychology and psychiatry. The purpose of this article is to review and synthesize the progress in these two areas that is most salient to the practice of clinical psychology. First, I describe how the results of genome-wide studies have elucidated the genetic architectures of psychiatric disorders. These genetic results can be applied to generate polygenic risk scores, identify rare causal mutations, evaluate gene by environment interactions, and help determine the specific causes of psychiatric disorders for each individual, all of which can help to guide therapies and treatments. Second, I explain how evolutionary theory, applied to human development, the human psyche, and mental disorders, leads to novel insights relevant to therapy. Evolutionary thinking for psychiatry and psychology is consilient with contemporary schools of thought in clinical psychology, but also provides novel, non-intuitive, and clinically-useful insights. Effects of the genome in development, and functioning of the adult psyche, are both usefully conceived as dynamical, non-linear systems, regulated by feedbacks, that can become disordered in predictable yet individualistic ways. The merging of genetic, neurological, psychological, and evolutionary approaches is set to transform clinical psychology and psychiatry, but requires increased emphasis on cross-disciplinary thinking and research. DOI PubMed
168.Crespi, BJ. (2020) The blind men and the elephant: What is missing cognitively in the study of cumulative technological evolution.Behav. Brain Sci. 43 The blind men and the elephant: What is missing cognitively in the study of cumulative technological evolution
I describe and explain (1) evidence regarding a key role for autism spectrum cognition in human technology; (2) tradeoffs of autistic cognition with social skills; and (3) a model of how cumulative technological culture evolves. This model involves positive feedback whereby increased technical complexity selects for enhanced social learning of mechanistic concepts and skills, leading to further advances in technology. DOI PubMed
167. Procyshyn, TL; Watson, NV; Crespi, BJ. (2020) Experimental empathy induction promotes oxytocin increases and testosterone decreases.Horm. Behav. 117 Experimental empathy induction promotes oxytocin increases and testosterone decreases
Oxytocin; Testosterone; Empathy; Systemizing
Oxytocin and testosterone coordinate adaptive social behaviors with stimuli in the environment. Administration of oxytocin and testosterone is associated with increased and reduced indicators of empathy, respectively, but how levels of these hormones are jointly affected by naturalistic empathy-inducing stimuli remains unclear. In this study, salivary oxytocin and testosterone levels were measured in 173 healthy adults before and after watching a video involving a gravely ill child. Participants also completed questionnaires to assess psychological variables predicted to affect oxytocin reactivity (Autism-Spectrum Quotient, Interpersonal Reactivity Index, Empathy and Systemizing Quotients). On average, there was a 14% increase in oxytocin (p = 0.003) and 4% decrease in testosterone (p = 0.001) pre- to post-video. Opposite directional changes in hormone levels occurred together, as supported by a chi-square test (p < 0.001) and a circular statistics test (p < 0.05). Considered separately, psychological traits did not predict hormone levels or changes to any appreciable degree. However, oxytocin and testosterone changes were linked with empathy relative to systemizing such that: (1) 'Empathy Bias' was associated with a large oxytocin increase but little change in testosterone, while (2) 'Systemizing Bias' and 'Balance' between empathy and systemizing were associated with a decrease in testosterone but little change in oxytocin. These findings suggest that participants were divisible into 'high oxytocin responders' (relatively empathetic) and 'high testosterone responders' (balanced or systemizing-biased). These findings support a model of joint, opposite changes in oxytocin and testosterone under experimental empathy induction, with high, somewhat predictable, diversity in individual responses. DOI PubMed
166. Salminen, I; Read, S; Hurd, P; Crespi, B. (2020) Does SNORD116 mediate aspects of psychosis in Prader-Willi syndrome? Evidence from a non-clinical population.Psychiatry Res. 286 Does SNORD116 mediate aspects of psychosis in Prader-Willi syndrome? Evidence from a non-clinical population
Paranoia; Psychosis; Autism spectrum disorder; Schizophrenia; Genomic imprinting
The paternally expressed gene SNORD116 encodes a set of short nucleolar RNAs that affect the expression of hundreds of other genes via epigenetic interactions. Lack of expression for SNORD116 has been implicated in major phenotypes of Prader-Willi Syndrome (PWS). Rates of psychosis and autism spectrum disorders are greatly increased in PWS, but the genetic and epigenetic causes of these increases remain unknown. We genotyped a large population of typical individuals for five SNPs within SNORD116 and phenotyped them for variation in schizotypal and autism spectrum traits. SNORD116 SNP and haplotype variation mediated variation exclusively in the Schizotypal Personality Questionnaire - Ideas of Reference subscale, which reflects variation in aspects of paranoia. The effect was restricted to females. SNORD116 represents, in addition to UBE3A and NDN-MAGEL2, a third, independent locus in the 15q11-q13 imprinted region that preferentially or exclusively affects levels of paranoia. This convergent pattern may reflect a common neural pathway affected by multiple genes, or an effect of interactions between the imprinted loci. DOI PubMed
165.Crespi, B; Dinsdale, N; Read, S; Hurd, P. (2019) Spirituality, dimensional autism, and schizotypal traits: The search for meaning.PLoS One 14 Spirituality, dimensional autism, and schizotypal traits: The search for meaning
The relationships of spirituality with human social cognition, as exemplified in autism spectrum and schizophrenia spectrum cognitive variation, remain largely unstudied. We quantified non-clinical levels of autism spectrum and schizotypal spectrum traits (using the Autism Quotient and the Schizotypal Personality Questionnaire-Brief Revised) and dimensions of spirituality (using the Hardt Spirituality Questionnaire) in a large sample of undergraduate students. We tested in particular the hypothesis, based on the diametrical model of autism and psychosis, that autism should be negatively associated, and positive schizotypal traits should be positively associated, with spirituality. Our primary findings were threefold. First, in support of the diametric model, total Spirituality score was significantly negatively correlated with total Autism Quotient score, and significantly positively correlated with Positive Schizotypal traits (the Schizotypal Personality Cognitive-Perceptual subscale), as predicted. Second, these associations were driven mainly by opposite patterns regarding the Search for Meaning Spirituality subscale, which was the only subscale that was significantly negatively associated with autism, and significantly positively associated with Positive Schizotypal traits. Third, Belief in God was positively correlated with Positive Schizotypal traits, but was uncorrelated with autism traits. The opposite findings for Search for Meaning can be interpreted in the contexts of well-supported cognitive models for understanding autism in terms of weak central coherence, and understanding Positive Schizotypal traits in terms of enhanced salience. DOI PubMed
164.Crespi, BJ. (2019) Autism, psychosis, and genomic imprinting: recent discoveries and conundrums.Curr. Opin. Behav. Sci. 25: 1-7 Autism, psychosis, and genomic imprinting: recent discoveries and conundrums
Genomic imprinting generates a category of genes that is unique because: (1) they are subject to intragenomic conflicts, within individuals, and thus (2) their phenotypic effects on offspring-to-mother interactions are predictable from evolutionary theory. I describe recent advances in our understanding of how imprinted genes may exert conflicting effects, and how the sequelae of such conflicts may impact upon aspects of human behavior and risks for specific psychiatric conditions. The main conclusion is that imprinted genes mediate expression of many penetrant human social-brain disorders including autism and psychosis. However, discerning the targets, mechanisms, and large-scale significance of their effects requires more studies of small, SNP-based and methylation-based imprinted gene effects on phenotypes relevant to offspring-mother social interactions in typical populations. DOI
163. Salminen, I; Read, S; Hurd, P; Crespi, B. (2019) Genetic variation of UBE3A is associated with schizotypy in a population of typical individuals.Psychiatry Res. 275: 94-99 Genetic variation of UBE3A is associated with schizotypy in a population of typical individuals
Angelman syndrome; Prader-Willi syndrome; Autism spectrum disorder; Schizophrenia; 15q11-q13 duplication; Genomic imprinting
The maternally expressed imprinted gene UBE3A has been implicated in autism, schizophrenia and psychosis. The phenotype of Angelman syndrome, caused by loss of UBE3A expression, involves autism spectrum traits, while Prader-Willi syndrome, where the genotype of maternal disomy increases dosage of UBE3A, shows high penetrance for the development of psychosis. Maternal duplications of the 15q11-q13 chromosome region that overlap the imprinted region also show an association with schizophrenia, further implying a connection between increased dosage of UBE3A and the development of schizophrenia and psychosis. We phenotyped a large population of typical individuals for autism spectrum and schizotypal traits and genotyped them for a set of SNPs in UBE3A. Genetic variation of rs732739, an intronic SNP tagging a large haplotype spanning nearly the entire range of UBE3A, was significantly associated with variation in total schizotypy. Our results provide an independent line of evidence, connecting the imprinted UBE3A gene to the schizophrenia spectrum. DOI PubMed
162. Salminen, II; Crespi, BJ; Mokkonen, M. (2019) Baby food and bedtime: Evidence for opposite phenotypes from different genetic and epigenetic alterations in Prader-Willi and Angelman syndromes.SAGE Open Med. 7 Baby food and bedtime: Evidence for opposite phenotypes from different genetic and epigenetic alterations in Prader-Willi and Angelman syndromes
Angelman syndrome; Prader-Willi syndrome; evolutionary medicine; genomic imprinting; hyperphagia; sleep
Prader-Willi and Angelman syndromes are often referred to as a sister pair of neurodevelopmental disorders, resulting from different genetic and epigenetic alterations to the same chromosomal region, 15q11-q13. Some of the primary phenotypes of the two syndromes have been suggested to be opposite to one another, but this hypothesis has yet to be tested comprehensively, and it remains unclear how opposite effects could be produced by changes to different genes in one syndrome compared to the other. We evaluated the evidence for opposite effects on sleep and eating phenotypes in Prader-Willi syndrome and Angelman syndrome, and developed physiological-genetic models that represent hypothesized causes of these differences. Sleep latency shows opposite deviations from controls in Prader-Willi and Angelman syndromes, with shorter latency in Prader-Willi syndrome by meta-analysis and longer latency in Angelman syndrome from previous studies. These differences can be accounted for by the effects of variable gene dosages of UBE3A and MAGEL2, interacting with clock genes, and leading to acceleration (in Prader-Willi syndrome) or deceleration (in Angelman syndrome) of circadian rhythms. Prader-Willi and Angelman syndromes also show evidence of opposite alterations in hyperphagic food selectivity, with more paternally biased subtypes of Angelman syndrome apparently involving increased preference for complementary foods ("baby foods"); hedonic reward from eating may also be increased in Angelman syndrome and decreased in Prader-Willi syndrome. These differences can be explained in part under a model whereby hyperphagia and food selectivity are mediated by the effects of the genes SNORD-116, UBE3A and MAGEL2, with outcomes depending upon the genotypic cause of Angelman syndrome. The diametric variation observed in sleep and eating phenotypes in Prader-Willi and Angelman syndromes is consistent with predictions from the kinship theory of imprinting, reflecting extremes of higher resource demand in Angelman syndrome and lower demand in Prader-Willi syndrome, with a special emphasis on social-attentional demands and attachment associated with bedtime, and feeding demands associated with mother-provided complementary foods compared to offspring-foraged family-type foods. DOI PubMed
161.Crespi, B; Read, S; Hurd, P. (2018) The SETDB2 locus: evidence for a genetic link between handedness and atopic disease.Heredity 120: 77-82 The SETDB2 locus: evidence for a genetic link between handedness and atopic disease
The gene SETDB2, which mediates aspects of laterality in animal model systems, has recently been linked with human handedness as measured continuously on a scale from strong left to strong right. By contrast, it was marginally associated with a left-right dichotomous measure, and it showed no evidence of association with absolute handedness strength independent of direction. We genotyped the SETDB2 handedness-associated single nucleotide polymorphism, rs4942830, in a large healthy population likewise phenotyped for continuous, absolute, and dichotomous handedness variables. Our results demonstrated significant effects of rs4942830 genotype on continuous handedness, and weaker, marginal effects on dichotomous handedness, but no effects on absolute handedness. These results help to establish the locus marked by the SNP rs4942830 as a strong candidate for mediating human handedness. Intriguingly, rs4942830 is also in complete linkage disequilibrium with rs386770867, a polymorphism recently shown to affect human serum levels of IgE production and other atopic phenotypes. These findings implicate this locus in the longstanding links of handedness with asthma and other atopic diseases. DOI
160.Crespi, B; Read, S; Salminen, I; Hurd, P. (2018) A genetic locus for paranoia.Biology Letters 14 A genetic locus for paranoia
paranoia; Prader-Willi; magel2; necdin; genomic imprinting
The psychological effects of brain-expressed imprinted genes in humans are virtually unknown. Prader-Willi syndrome (PWS) is a neurogenetic condition mediated by genomic imprinting, which involves high rates of psychosis characterized by hallucinations and paranoia, as well as autism. Altered expression of two brain-expressed imprinted genes, MAGEL2 and NDN, mediates a suite of PWS-related phenotypes, including behaviour, in mice. We phenotyped a large population of typical individuals for schizophrenia-spectrum and autism-spectrum traits, and genotyped them for the single-nucleotide polymorphism rs850807, which is putatively functional and linked with MAGEL2 and NDN. Genetic variation in rs850807 was strongly and exclusively associated with the ideas of reference subscale of the schizophrenia spectrum, which is best typified as paranoia. These findings provide a single-locus genetic model for analysing the neurological and psychological bases of paranoid thinking, and implicate imprinted genes, and genomic conflicts, in human mentalistic thought. DOI
159.Crespi, BJ. (2018) The Paradox of Copy Number Variants in ASD and Schizophrenia: False Facts or False Hypotheses?Rev. J. Autism Dev. Disord. 5: 199-207 The Paradox of Copy Number Variants in ASD and Schizophrenia: False Facts or False Hypotheses?
ASD; Copy number variants; Schizophrenia; Brain size
A series of recent papers has demonstrated "mirror extreme" variation in measures of brain size, between individuals with deletions compared to duplications, for copy number variation loci. For most loci, ASD-associated CNVs involve larger brain sizes, and schizophrenia-associated CNVs involve smaller brain sizes, the same patterns also found for idiopathic cases of ASD and schizophrenia. However, some CNVs have been linked with both disorders. Taken together, these findings appear paradoxical and require explanation. One possibility is that the paradoxical CNV data represents, to some degree, false positive diagnoses. A second possibility is that the paradox is based on false premises. I review current evidence salient to the two hypotheses, and suggest future studies to test them in a definitive way. DOI
157. Del Giudice, M; Crespi, BJ. (2018) Basic functional trade-offs in cognition: An integrative framework.Cognition 179: 56-70 Basic functional trade-offs in cognition: An integrative framework
Design; Efficiency; Flexibility; Performance; Robustness; Trade-offs
Trade-offs between advantageous but conflicting properties (e.g., speed vs. accuracy) are ubiquitous in cognition, but the relevant literature is conceptually fragmented, scattered across disciplines, and has not been organized in a coherent framework. This paper takes an initial step toward a general theory of cognitive trade-offs by examining four key properties of goal-directed systems: performance, efficiency, robustness, and flexibility. These properties define a number of basic functional trade-offs that can be used to map the abstract "design space" of natural and artificial cognitive systems. Basic functional trade-offs provide a shared vocabulary to describe a variety of specific trade-offs including speed vs. accuracy, generalist vs. specialist, exploration vs. exploitation, and many others. By linking specific features of cognitive functioning to general properties such as robustness and efficiency, it becomes possible to harness some powerful insights from systems engineering and systems biology to suggest useful generalizations, point to under-explored but potentially important trade-offs, and prompt novel hypotheses and connections between disparate areas of research. DOI PubMed
156. Jha, S; Read, S; Hurd, P; Crespi, B. (2018) Segregating polymorphism in the NMDA receptor gene GRIN2A, schizotypy, and mental rotation among healthy individuals.Neuropsychologia 117 Segregating polymorphism in the NMDA receptor gene GRIN2A, schizotypy, and mental rotation among healthy individuals
Schizotypy; Mental rotation; GRIN2A; NMDA receptor; Imagery
Common alleles associated with psychiatric disorders are often regarded as deleterious genes that influence vulnerability to disease, but they may also be considered as mediators of variation in adaptively structured cognitive phenotypes among healthy individuals. The schizophrenia-associated gene GRIN2A (glutamate ionotropic receptor NMDA type subunit 2a) codes for a protein subunit of the NMDA (N-methyl-D-aspartate) receptor that underlies central aspects of human cognition. Pharmacological NMDA blockage recapitulates the major features of schizophrenia in human subjects, and represents a key model for the neurological basis of this disorder. We genotyped two functional GRIN2A polymorphisms in a large population of healthy individuals who were scored for schizotypy and mental imagery/manipulation (the mental rotation test). Rare-allele homozygosity of the promoter microsatellite rs3219790 was associated with high total schizotypy (after adjustment for multiple comparisons) and with enhanced mental rotation ability (nominally, but not after adjustment for multiple comparisons), among males. These findings provide preliminary evidence regarding a genetic basis to previous reports of enhanced mental imagery in schizophrenia and schizotypy. The results also suggest that some schizophrenia-related alleles may be subject to cognitive tradeoffs involving both positive and negative effects on psychological phenotypes, which may help to explain the maintenance of psychiatric-disorder risk alleles in human populations. DOI PubMed
155. Mokkonen, M; Koskela, E; Procyshyn, T; Crespi, B. (2018) Socio-reproductive Conflicts and the Father's Curse Dilemma.Am. Nat. 192 Socio-reproductive Conflicts and the Father's Curse Dilemma
genomic conflict; sexual conflict; parent-offspring conflict; testosterone; oxytocin; bank vole
Evolutionary conflicts between males and females can manifest over sexually antagonistic interactions at loci or over sexually antagonistic interests within a locus. The latter form of conflict, intralocus sexual conflict, arises from sexually antagonistic selection and constrains the fitness of individuals through a phenotypic compromise. These conflicts, and socio-reproductive interactions in general, are commonly mediated by hormones, and thus predictive insights can be gained from studying their mediating effects. Here, we integrate several lines of evidence to describe a novel, hormonally mediated reproductive dilemma that we call the father's curse, which results from an intralocus conflict between mating and parental efforts. Essentially, a genetic locus exerts pleiotropic and antagonistic effects on the mating effort of one individual and the parental effort of a related individual who is the primary provider of parental care. We outline the criteria for operation of the father's curse dilemma, provide evidence of the phenomenon, and discuss the predictions and outcomes arising from its dynamics. By integrating the effects of hormones into socio-reproductive conflicts and socio-reproductive effort, clearer links between genotypes, phenotypes, and fitness can be established. DOI PubMed
154. Nosil, P; Villoutreix, R; de Carvalho, CF; Farkas, TE; Soria-Carrasco, V; Feder, JL; Crespi, BJ; Gompert, Z. (2018) Natural selection and the predictability of evolution in Timema stick insects.Science 359: 765-770 Natural selection and the predictability of evolution in Timema stick insects
Predicting evolution remains difficult. We studied the evolution of cryptic body coloration and pattern in a stick insect using 25 years of field data, experiments, and genomics. We found that evolution is more difficult to predict when it involves a balance between multiple selective factors and uncertainty in environmental conditions than when it involves feedback loops that cause consistent back-and-forth fluctuations. Specifically, changes in color-morph frequencies are modestly predictable through time (r(2) = 0.14) and driven by complex selective regimes and yearly fluctuations in climate. In contrast, temporal changes in pattern-morph frequencies are highly predictable due to negative frequency-dependent selection (r(2) = 0.86). For both traits, however, natural selection drives evolution around a dynamic equilibrium, providing some predictability to the process. DOI PubMed
153. Armeanu, R; Mokkonen, M; Crespi, B. (2017) Meta-Analysis of BDNF Levels in Autism.Cell. Mol. Neurobiol. 37: 949-954 Meta-Analysis of BDNF Levels in Autism
Autism; BDNF; Meta-analysis; Schizophrenia; Bipolar disorder; Depression
Brain-derived neurotrophic factor (BDNF) centrally mediates growth, differentiation and survival of neurons, and the synaptic plasticity that underlies learning and memory. Recent meta-analyses have reported significantly lower peripheral BDNF among individuals with schizophrenia, bipolar disorder, and depression, compared with controls. To evaluate the role of BDNF in autism, and to compare autism to psychotic-affective disorders with regard to BDNF, we conducted a meta-analysis of BDNF levels in autism. Inclusion criteria were met by 15 studies, which included 1242 participants. The meta-analysis estimated a significant summary effect size of 0.33 (95 % CI 0.21-0.45, P < 0.001), suggesting higher BDNF in autism than in controls. The studies showed notable heterogeneity, but no evidence of publication biases. Higher peripheral BDNF in autism is concordant with several neurological and psychological theories on the causes and symptoms of this condition, and it contrasts notably with the lower levels of BDNF found in schizophrenia, bipolar disorder, and depression. DOI
152.Crespi, B; Read, S; Hurd, P. (2017) Segregating polymorphisms of FOXP2 are associated with measures of inner speech, speech fluency and strength of handedness in a healthy population.Brain Lang. 173: 33-40 Segregating polymorphisms of FOXP2 are associated with measures of inner speech, speech fluency and strength of handedness in a healthy population
FOXP2; Inner speech; Fluency; Handedness; Schizotypy; Evolution
We genotyped a healthy population for three haplotype-tagging FOXP2 SNPs, and tested for associations of these SNPs with strength of handedness and questionnaire-based metrics of inner speech characteristics (ISP) and speech fluency (FLU), as derived from the Schizotypal Personality Questionnaire-BR. Levels of mixed-handedness were positively correlated with ISP and FLU, supporting prior work on these two domains. Genotype for rs7799109, a SNP previously linked with lateralization of left frontal regions underlying language, was associated with degree of mixed handedness and with scores for ISP and FLU phenotypes. Genotype of rs1456031, which has previously been linked with auditory hallucinations, was also associated with ISP phenotypes. These results provide evidence that FOXP2 SNPs influence aspects of human inner speech and fluency that are related to lateralized phenotypes, and suggest that the evolution of human language, as mediated by the adaptive evolution of FOXP2, involved features of inner speech. (C) 2017 Elsevier Inc. All rights reserved. DOI
150.Crespi, BJ; Procyshyn, TL. (2017) Williams syndrome deletions and duplications: Genetic windows to understanding anxiety, sociality, autism, and schizophrenia.Neurosci. Biobehav. Rev. 79: 14-26 Williams syndrome deletions and duplications: Genetic windows to understanding anxiety, sociality, autism, and schizophrenia
Williams syndrome; Prosociality; Anxiety; Oxytocin; Autism; Schizophrenia
We describe and evaluate an integrative hypothesis for helping to explain the major neurocognitive features of individuals with Williams syndrome region deletions and duplications. First, we demonstrate how the cognitive differences between Williams syndrome individuals, individuals with duplications of this region, and healthy individuals parallel the differences between individuals subject to effects of increased or decreased oxytocin. Second, we synthesize evidence showing that variation in expression of the gene GTF2I (General Transcription Factor II-I) underlies the primary social phenotypes of Williams syndrome and that common genetic variation in GTF2I mediates oxytocin reactivity, and its correlates, in healthy populations. Third, we describe findings relevant to the hypothesis that the GTF2I gene is subject to parent of origin effects whose behavioral expression fits with predictions from the kinship theory of genomic imprinting. Fourth, we describe how Williams syndrome can be considered, in part, as an autistic syndrome of Lorna Wing's 'active-but-odd' autism subtype, in contrast to associations of duplications with both schizophrenia and autism. DOI
149. Dinsdale, NL; Crespi, BJ. (2017) Revisiting the wandering womb: Oxytocin in endometriosis and bipolar disorder.Horm. Behav. 96: 69-83 Revisiting the wandering womb: Oxytocin in endometriosis and bipolar disorder
Oxytocin; Endometriosis; Bipolar disorder; Hysteria; Pleiotropy; Evolutionary medicine; Psychiatry; Mania; Hippocrates; Mind-body
Hippocrates attributed women's high emotionality hysteria - to a 'wandering womb'. Although hysteria diagnoses were abandoned along with the notion that displaced wombs cause emotional disturbance, recent research suggests that elevated levels of oxytocin occur in both bipolar disorder and endometriosis, a gynecological condition involving migration of endometrial tissue beyond the uterus. We propose and evaluate the hypothesis that elevated oxytocinergic system activity jointly contributes to bipolar disorder and endometriosis. First, we provide relevant background on endometriosis and bipolar disorder, and then we examine evidence for co-morbidity between these conditions. We next: (1) review oxytocin's associations with personality traits, especially extraversion and openness, and how they overlap with bipolar spectrum traits; (2) describe evidence for higher oxytocinergic activity in both endometriosis and bipolar disorder; (3) examine altered hypothalamic pituitary -gonadal axis functioning in both conditions; (4) describe data showing that medications that treat one condition can improve symptoms of the other; (5) discuss fitness-related impacts of endometriosis and bipolar disorder; and (6) review a pair of conditions, polycystic ovary syndrome and autism, that show evidence of involving reduced oxytocinergic activity, in direct contrast to endometriosis and bipolar disorder. Considered together, the bipolar spectrum and endometriosis appear to involve dysregulated high extremes of normally adaptive pleiotropy in the female oxytocin system, whereby elevated levels of oxytocinergic activity coordinate outgoing sociality with heightened fertility, apparently characterizing, overall, a faster life history. These findings should prompt a re-examination of how mind-body interactions, and the pleiotropic endocrine systems that underlie them, contribute to health and disease. DOI
148. Procyshyn, TL; Hurd, PL; Crespi, BJ. (2017) Association Testing of Vasopressin Receptor 1a Microsatellite Polymorphisms in Non-Clinical Autism Spectrum Phenotypes.Autism Res. 10: 750-756 Association Testing of Vasopressin Receptor 1a Microsatellite Polymorphisms in Non-Clinical Autism Spectrum Phenotypes
attention; autism quotient; autism spectrum; avpr1a; microsatellite analysis; rs1; rs3; vasopressin
Variation in the AVPR1a gene, which codes for a receptor for the neurohormone vasopressin, has been found to relate to autism risk. Interestingly, variation in this gene also relates to differences in social behaviour in non-clinical populations. Variation in this gene may affect expression of AVPR1a receptors in brain areas involved in social behaviour. Here, we tested whether AVPR1a variation was associated with Autism Quotient (AQ) scores, a questionnaire that measures non-clinical manifestations of autism, in a population of 873 healthy university students. The AVPR1a RS1 and RS3 microsatellites were examined, and variants were categorized as "long" or "short". The RS3 long/long genotype was significantly associated with a higher AQ score (i.e., a more autistic-like phenotype) for the combined population and for females only. Further examination showed that this relationship was due to a specific RS3 variant, termed the "target allele", which previous research has linked to reduced altruism and increased marital problems in healthy individuals. We also observed that the relationship between RS3 genotype and AQ score was mainly due to the "attention switching" (the ability to shift attention from one task to another) component of the questionnaire; this ability is commonly impaired in autism spectrum disorders. Overall, our study establishes continuity between the existing AVPR1a research in clinical and non-clinical populations. Our results suggest that vasopressin may exert its effects on social behaviour in part by modulating attentional focus between social and non-social cues. (C) 2016 International Society for Autism Research, Wiley Periodicals, Inc. DOI
147. Procyshyn, TL; Spence, J; Read, S; Watson, NV; Crespi, BJ. (2017) The Williams syndrome prosociality gene GTF21 mediates oxytocin reactivity and social anxiety in a healthy population.Biology Letters 13 The Williams syndrome prosociality gene GTF21 mediates oxytocin reactivity and social anxiety in a healthy population
oxytocin; social anxiety; GTF21 gene; Williams syndrome; prosociality
The neurohormone oxytocin plays a central role in human social behaviour and cognition, and oxytocin dysregulation may contribute to psychiatric disorders. However, genetic factors influencing individual variation in the oxytocinergic system remain poorly understood. We genotyped 169 healthy adults for a functional polymorphism in GTF2I (general transcription factor II-I), a gene associated with high prosociality and reduced social anxiety in Williams syndrome, a condition reported to involve high oxytocin levels and reactivity. Participants' salivary oxytocin levels were measured before and after watching a validated empathy-inducing video. Oxytocin reactivity, defined as pre- to post-video percentage change in salivary oxytocin, varied substantially and significantly between individuals with different GTF2I genotypes, with, additionally, a trend towards an interaction between genotype and sex. Individuals with more oxytocin-reactive genotypes also reported significantly lower social anxiety. These findings suggest a model whereby GTF2I has a continuum of effects on human sociality, from the extreme social phenotypes and oxytocin dysregulation associated with gene deletion in Williams syndrome, to individual differences in oxytocin reactivity and sociality associated with common polymorphisms in healthy populations. DOI
146. Riesch, R; Muschick, M; Lindtke, D; Villoutreix, R; Comeault, AA; Farkas, TE; Lucek, K; Hellen, E; Soria-Carrasco, V; Dennis, SR; de Carvalho, CF; Safran, RJ; Sandoval, CP; Feder, J; Gries, R; Crespi, BJ; Gries, G; Gompert, Z; Nosil, P. (2017) Transitions between phases of genomic differentiation during stick-insect speciation.Nature Ecology & Evolution 1 Transitions between phases of genomic differentiation during stick-insect speciation
Speciation can involve a transition from a few genetic loci that are resistant to gene flow to genome-wide differentiation. However, only limited data exist concerning this transition and the factors promoting it. Here, we study phases of speciation using data from >100 populations of 11 species of Timema stick insects. Consistent with early phases of genie speciation, adaptive colour-pattern loci reside in localized genetic regions of accentuated differentiation between populations experiencing gene flow. Transitions to genome-wide differentiation are also observed with gene flow, in association with differentiation in polygenic chemical traits affecting mate choice. Thus, intermediate phases of speciation are associated with genome-wide differentiation and mate choice, but not growth of a few genomic islands. We also find a gap in genomic differentiation between sympatric taxa that still exchange genes and those that do not, highlighting the association between differentiation and complete reproductive isolation. Our results suggest that substantial progress towards speciation may involve the alignment of multi-faceted aspects of differentiation. DOI
145.Crespi, B; Leach, E; Dinsdale, N; Mokkonena, M; Hurd, P. (2016) Imagination in human social cognition, autism, and psychotic-affective conditions.Cognition 150: 181-199 Imagination in human social cognition, autism, and psychotic-affective conditions
Imagination; Autism; Schizophrenia; Creativity; Polygenic risk score; Autism Spectrum Quotient
Complex human social cognition has evolved in concert with risks for psychiatric disorders. Recently, autism and psychotic-affective conditions (mainly schizophrenia, bipolar disorder, and depression) have been posited as psychological 'opposites' with regard to social-cognitive phenotypes. Imagination, considered as 'forming new ideas, mental images, or concepts', represents a central facet of human social evolution and cognition. Previous studies have documented reduced imagination in autism, and increased imagination in association with psychotic-affective conditions, yet these sets of findings have yet to be considered together, or evaluated in the context of the diametric model. We first review studies of the components, manifestations, and neural correlates of imagination in autism and psychotic affective conditions. Next, we use data on dimensional autism in healthy populations to test the hypotheses that: (1) imagination represents the facet of autism that best accounts for its strongly male-biased sex ratio, and (2) higher genetic risk of schizophrenia is associated with higher imagination, in accordance with the predictions of the diametric model. The first hypothesis was supported by a systematic review and meta-analysis showing that Imagination exhibits the strongest male bias of all Autism Quotient (AQ) subscales, in non-clinical populations. The second hypothesis was supported, for males, by associations between schizophrenia genetic risk scores, derived from a set of single-nucleotide polymorphisms, and the AQ Imagination subscale. Considered together, these findings indicate that imagination, especially social imagination as embodied in the default mode human brain network, mediates risk and diametric dimensional phenotypes of autism and psychotic-affective conditions. (C) 2016 Elsevier B.V. All rights reserved. DOI
144.Crespi, BJ. (2016) Autism As a Disorder of High Intelligence.Frontiers in Neuroscience 10 Autism As a Disorder of High Intelligence
intelligence; autism; schizophrenia; genetic correlation; pleiotropy; evolution
A suite of recent studies has reported positive genetic correlations between autism risk and measures of mental ability. These findings indicate that alleles for autism overlap broadly with alleles for high intelligence, which appears paradoxical given that autism is characterized, overall, by below-average IQ. This paradox can be resolved under the hypothesis that autism etiology commonly involves enhanced, but imbalanced, components of intelligence. This hypothesis is supported by convergent evidence showing that autism and high 10 share a diverse set of convergent correlates, including large brain size, fast brain growth, increased sensory and visual-spatial abilities, enhanced synaptic functions, increased attentional focus, high socioeconomic status, more deliberative decision-making, profession and occupational interests in engineering and physical sciences, and high levels of positive assortative mating. These findings help to provide an evolutionary basis to understanding autism risk as underlain in part by dysregulation of intelligence, a core human-specific adaptation. In turn, integration of studies on intelligence with studies of autism should provide novel insights into the neurological and genetic causes of high mental abilities, with important implications for cognitive enhancement, artificial intelligence, the relationship of autism with schizophrenia, and the treatment of both autism and intellectual disability. DOI
143.Crespi, BJ. (2016) Oxytocin, testosterone, and human social cognition.Biological Reviews 91: 390-408 Oxytocin, testosterone, and human social cognition
oxytocin; testosterone; social cognition; autism; schizophrenia; depression
I describe an integrative social-evolutionary model for the adaptive significance of the human oxytocinergic system. The model is based on a role for this hormone in the generation and maintenance of social familiarity and affiliation across five homologous, functionally similar, and sequentially co-opted contexts: mothers with offspring, female and male mates, kin groups, individuals with reciprocity partners, and individuals within cooperating and competing social groups defined by culture. In each situation, oxytocin motivates, mediates and rewards the cognitive and behavioural processes that underlie the formation and dynamics of a more or less stable social group, and promotes a relationship between two or more individuals. Such relationships may be positive (eliciting neurological reward, reducing anxiety and thus indicating fitness-enhancing effects), or negative (increasing anxiety and distress, and thus motivating attempts to alleviate a problematic, fitness-reducing social situation). I also present evidence that testosterone exhibits opposite effects from oxytocin on diverse aspects of cognition and behaviour, most generally by favouring self-oriented, asocial and antisocial behaviours. I apply this model for effects of oxytocin and testosterone to understanding human psychological disorders centrally involving social behaviour. Reduced oxytocin and higher testosterone levels have been associated with under-developed social cognition, especially in autism. By contrast, some combination of oxytocin increased above normal levels, and lower testosterone, has been reported in a notable number of studies of schizophrenia, bipolar disorder and depression, and, in some cases, higher oxytocin involves maladaptively 'hyper-developed' social cognition in these conditions. This pattern of findings suggests that human social cognition and behaviour are structured, in part, by joint and opposing effects of oxytocin and testosterone, and that extremes of such joint effects partially mediate risks and phenotypes of autism and psychotic-affective conditions. These considerations have direct implications for the development of therapies for alleviating disorders of social cognition, and for understanding how such disorders are associated with the evolution of human cognitive-affective architecture. DOI
142.Crespi, BJ. (2016) The convergent and divergent evolution of social-behavioral economics.Behavioral and Brain Sciences 39 The convergent and divergent evolution of social-behavioral economics
Human hunter-gatherers share a suite of traits with social insects, which demonstrates convergent social evolution of these taxa prior to agriculture. Humans differ from social insects in that their divisions of labor are more competitive than cooperative. Resulting higher within-group competition in humans has been alleviated by religion and culturally imposed monogamy, both of which also find parallels among social insects. DOI
141. Dinsdale, N; Mokkonen, M; Crespi, B. (2016) The 'extreme female brain': increased cognitive empathy as a dimension of psychopathology.Evolution and Human Behavior 37: 323-336 The 'extreme female brain': increased cognitive empathy as a dimension of psychopathology
Empathizing; Female brain; Autism; Depression; Borderline personality
Baron-Cohen's 'extreme male brain' theory postulates that autism involves exaggerated male-typical psychology, with reduced empathizing (considered here as social-emotional interest, motivation and abilities) and increased systemizing (non-social, physical-world and rule-based interest, motivation and abilities), in association with its male-biased sex ratio. The concept of an 'extreme female brain', involving some combination of increased empathizing and reduced systemizing, and its possible role in psychiatric conditions, has been considerably less well investigated. Female-biased sex ratios have been described in two conditions, depression and borderline personality disorder (BPD), that also show evidence of increases in aspects of empathy in some studies. We evaluated the hypothesis that BPD and depression can be conceptualized in the context of the 'extreme female brain' by: (1) describing previous conceptualizations of the extreme female brain model, (2) reviewing evidence of female-biased sex ratios in BPD and depression, (3) conducting meta-analyses of performance on the Reading the Mind in the Eyes test (RMET) among individuals with BPD, clinical or sub-clinical depression, and other psychiatric conditions involving altered social cognition and mood (schizophrenia, bipolar disorder, eating disorders, and autism), in relation to disorder sex ratios, and (4) evaluating previous evidence of increased empathic performance in these, and related, psychiatric conditions, and (5) synthesizing these lines of evidence into models for causes and effects of an 'extreme female brain'. Our primary empirical results are that RMET performance is enhanced in sub-clinical depression, preserved in borderline personality disorder, and reduced in other disorders (by meta-analyses), and that across disorders, more male-biased patient sex ratios are strongly associated with worse RMET performance of patients relative to controls. Our findings, in conjunction with previous work, suggest that increased cognitive empathizing mediates risk and expression of some psychiatric conditions with evidence of female biases, especially sub-clinical depression and borderline personality disorder, in association with increased attention to social stimuli, higher levels of social and emotional sensitivity, negative emotion biases, and over-developed mentalist thought. These results link evolved human sex differences with psychiatric vulnerabilities and symptoms, and lead to specific suggestions for future work. (C) 2016 Elsevier Inc. All rights reserved. DOI
140. Robinson, KJ; Hurd, PL; Read, S; Crespi, BJ. (2016) The PCSK6 gene is associated with handedness, the autism spectrum, and magical ideation in a non-clinical population.Neuropsychologia 84: 205-212 The PCSK6 gene is associated with handedness, the autism spectrum, and magical ideation in a non-clinical population
Handedness; Lateralization; PCSK6 gene; VNTR; Autism; Schizotypy
Common polymorphisms in the gene PCSK6, whose protein product mediates the development of brain and body asymmetry through the NODAL pathway, have recently been associated with handedness in three studies, making it a key candidate gene for understanding the developmental and expression of human lateralization. We tested the hypothesis that the PCSK6 VNTR polymorphism rs1053972 influences the expression of handedness and aspects of dimensional schizotypy and autism. For a sample of 709 healthy individuals, rs1053972 genotype was significantly associated with categorical measures of handedness, and with dimensional handedness in subsets of the population with high schizotypy and magical ideation or a lack of strong right-handedness. Both findings showed evidence of stronger or exclusive effects among females, compared to males. Genotypes of PCSK6 also showed significant sex limited associations with magical ideation, a component of positive schizotypal cognition measured using the Schizotypal Personality Questionnaire, and total autism score, measured using the Autism Spectrum Quotient. These results partially replicate previous studies on effects of PCSK6 rs1053972 genetic variation on handedness phenotypes, link the PCSK6 gene with the dimensional expression of neurodevelopmental conditions in healthy individuals, and show that associations of this gene with handedness and psychological phenotypes exhibit evidence of sex-limited effects. (C) 2016 Elsevier Ltd. All rights reserved. DOI PubMed
139. Arbuthnott, D; Crespi, BJ; Schwander, T. (2015) Female Stick Insects Mate Multiply to Find Compatible Mates.American Naturalist 186: 519-530 Female Stick Insects Mate Multiply to Find Compatible Mates
polyandry; mate choice; genetic compatibility; sexual selection; phasmid
Why females of many species mate multiply in the absence of direct benefits remains an open question in evolutionary ecology. Interacting and mating with multiple males can be costly to females in terms of time, resources, predation risk, and disease transmission. A number of indirect genetic benefits have been proposed to explain such behaviors, but the relative importance of these mechanisms in natural systems remains unclear. We tested for several direct and indirect benefits of polyandry in the walking stick Timema cristinae. We found no evidence of direct benefits with respect to longevity or fecundity. However, male x female genotypic interactions affected egg-hatching success and offspring production independent of relatedness, suggesting that mating with certain males benefits females and that the best male may differ for each female. Furthermore, multiply mated females biased paternity toward one or few males, and the extent of this bias was positively correlated to egg-hatching success. Our data, therefore, provide evidence for indirect benefits through compatibility effects in this species. By mating multiply, females may improve their chances of mating with a compatible male if compatibility cannot be assessed before mating. Such compatibility effects can explain the evolution and maintenance of polyandry in Timema and many other species. DOI
138. Arnal, A; Ujvari, B; Crespi, B; Gatenby, RA; Tissot, T; Vittecoq, M; Ewald, PW; Casali, A; Ducasse, H; Jacqueline, C; Misse, D; Renaud, F; Roche, B; Thomas, F. (2015) Evolutionary perspective of cancer: myth, metaphors, and reality.Evolutionary Applications 8: 541-544 Evolutionary perspective of cancer: myth, metaphors, and reality
adaptationism; cancer; evolutionary processes
The evolutionary perspective of cancer (which origins and dynamics result from evolutionary processes) has gained significant international recognition over the past decade and generated a wave of enthusiasm among researchers. In this context, several authors proposed that insights into evolutionary and adaptation dynamics of cancers can be gained by studying the evolutionary strategies of organisms. Although this reasoning is fundamentally correct, in our opinion, it contains a potential risk of excessive adaptationism, potentially leading to the suggestion of complex adaptations that are unlikely to evolve among cancerous cells. For example, the ability of recognizing related conspecifics and adjusting accordingly behaviors as in certain free-living species appears unlikely in cancer. Indeed, despite their rapid evolutionary rate, malignant cells are under selective pressures for their altered lifestyle for only few decades. In addition, even though cancer cells can theoretically display highly sophisticated adaptive responses, it would be crucial to determine the frequency of their occurrence in patients with cancer, before therapeutic applications can be considered. Scientists who try to explain oncogenesis will need in the future to critically evaluate the metaphorical comparison of selective processes affecting cancerous cells with those affecting organisms. This approach seems essential for the applications of evolutionary biology to understand the origin of cancers, with prophylactic and therapeutic applications. DOI
137.Crespi, BJ. (2015) Cognitive trade-offs and the costs of resilience.Behavioral and Brain Sciences 38 Cognitive trade-offs and the costs of resilience
Genetic, endocrinological, and psychological evidence demonstrates that resilience commonly trades off with sensitivity. The existence of such trade-offs indicates that resilience bears costs as well as benefits, and that some disorders can best be conceptualized in terms of extremes of trade-offs rather than expression of deficits. Testing for cognitive trade-offs should be a priority for psychiatry, psychology, neuroscience, and genetics. DOI
136.Crespi, BJ; Hurd, PL. (2015) Genetically based correlates of serum oxytocin and testosterone in autism and schizotypy.Personality and Individual Differences 79: 39-43 Genetically based correlates of serum oxytocin and testosterone in autism and schizotypy
Testosterone; Oxytocin; Autism; Schizotypy; Social cognition
The hormones oxytocin and testosterone have been implicated in autism spectrum and schizophrenia-spectrum cognition and disorders, but their roles in mediating these psychological phenotypes remain largely unknown. We genotyped a large set of healthy individuals for loci that represent established genetic indicators of serum testosterone and oxytocin levels, and tested for associations of these genetic indices of hormone levels with self-report measures of autistic and schizotypal cognition. A low genetic index of testosterone, a high genetic index of oxytocin, and/or a low ratio of testosterone to oxytocin indices were positively correlated with high imagination (by the Autism Quotient) and high positive and total schizotypy (by the Schizotypal Personality Questionnaire). The genetic indices for oxytocin, and testosterone relative to oxytocin, also showed significant correlations with a metric of positive schizotypy relative to autism, implicating higher oxytocin and lower testosterone in increased positively-schizotypal traits combined with decreased autism-associated traits. These results link genetic indicators of serum hormone levels with measures of schizotypy and autism among healthy individuals. (C) 2015 Elsevier Ltd. All rights reserved. DOI
135. Elliot, MG; Crespi, BJ. (2015) Genetic recapitulation of human pre-eclampsia risk during convergent evolution of reduced placental invasiveness in eutherian mammals.Philosophical Transactions of the Royal Society B-Biological Sciences 370 Genetic recapitulation of human pre-eclampsia risk during convergent evolution of reduced placental invasiveness in eutherian mammals
placentation; pre-eclampsia; positive selection; candidate genes; Darwinian medicine
The relationship between phenotypic variation arising through individual development and phenotypic variation arising through diversification of species has long been a central question in evolutionary biology. Among humans, reduced placental invasion into endometrial tissues is associated with diseases of pregnancy, especially pre-eclampsia, and reduced placental invasiveness has also evolved, convergently, in at least 10 lineages of eutherian mammals. We tested the hypothesis that a common genetic basis underlies both reduced placental invasion arising through a developmental process in human placental disease and reduced placental invasion found as a derived trait in the diversification of Euarchontoglires (rodents, lagomorphs, tree shrews, colugos and primates). Based on whole-genome analyses across 18 taxa, we identified 1254 genes as having evolved adaptively across all three lineages exhibiting independent evolutionary transitions towards reduced placental invasion. These genes showed strong evidence of enrichment for associations with pre-eclampsia, based on genetic-association studies, gene-expression analyses and gene ontology. We further used in silico prediction to identify a subset of 199 genes that are likely targets of natural selection during transitions in placental invasiveness and which are predicted to also underlie human placental disorders. Our results indicate that abnormal ontogenies can recapitulate major phylogenetic shifts in mammalian evolution, identify new candidate genes for involvement in pre-eclampsia, imply that study of species with less-invasive placentation will provide useful insights into the regulation of placental invasion and pre-eclampsia, and recommend a novel comparative functional-evolutionary approach to the study of genetically based human disease and mammalian diversification. DOI PubMed
134. Mokkonen, M; Crespi, BJ. (2015) Genomic conflicts and sexual antagonism in human health: insights from oxytocin and testosterone.Evolutionary Applications 8: 307-325 Genomic conflicts and sexual antagonism in human health: insights from oxytocin and testosterone
genomic imprinting; kinship theory; parental antagonism; parent-offspring conflict; sexual antagonism; sexual conflict
We review the hypothesized and observed effects of two of the major forms of genomic conflicts, genomic imprinting and sexual antagonism, on human health. We focus on phenotypes mediated by peptide and steroid hormones (especially oxytocin and testosterone) because such hormones centrally mediate patterns of physical and behavioral resource allocation that underlie both forms of conflict. In early development, a suite of imprinted genes modulates the human oxytocinergic system as predicted from theory, with paternally inherited gene expression associated with higher oxytocin production, and increased solicitation to mothers by infants. This system is predicted to impact health through the incompatibility of paternal-gene and maternal-gene optima and increased vulnerability of imprinted gene systems to genetic and epigenetic changes. Early alterations to oxytocinergic systems have long-term negative impacts on human psychological health, especially through their effects on attachment and social behavior. In contrast to genomic imprinting, which generates maladaptation along an axis of mother-infant attachment, sexual antagonism is predicted from theory to generate maladaptation along an axis of sexual dimorphism, modulated by steroid and peptide hormones. We describe evidence of sexual antagonism from studies of humans and other animals, demonstrating that sexually antagonistic effects on sex-dimorphic phenotypes, including aspects of immunity, life history, psychology, and behavior, are commonly observed and lead to forms of maladaptation that are demonstrated, or expected, to impact human health. Recent epidemiological and psychiatric studies of schizophrenia in particular indicate that it is mediated, in part, by sexually antagonistic alleles. The primary implication of this review is that data collection focused on (i) effects of imprinted genes that modulate the oxytocin system, and (ii) effects of sexually antagonistic alleles on sex-dimorphic, disease-related phenotypes will lead to novel insights into both human health and the evolutionary dynamics of genomic conflicts. DOI PubMed
133. Ablard, KM; Simonetto, K; Weir, LK; Crespi, BJ; Schaefer, PW; Gries, G. (2014) First-male sperm precedence and precopulatory and postcopulatory rituals in the parasitoid wasp Ooencyrtus kuvanae (Hymenoptera: Encyrtidae).Canadian Entomologist 146: 548-559 First-male sperm precedence and precopulatory and postcopulatory rituals in the parasitoid wasp Ooencyrtus kuvanae (Hymenoptera: Encyrtidae)
Sperm competition generates selection for male traits to prevent it. These traits remain unclear in species where males compete for a virgin who is briefly receptive. Males of the parasitoid wasp Ooencyrtus kuvanae Howard (Hymenoptera: Encyrtidae) compete over females following emergence from host egg masses. Males engage virgins in a precopulatory ritual, mate, and then immediately perform a postcopulatory ritual after which the female becomes unreceptive. Often, sneaker (M-2) males copulate with a female while she is engaged in the postcopulatory ritual, and they also perform the postcopulatory ritual. We investigated (i) paternity of M-1 and M-2 males using DNA microsatellite analysis, (ii) copulation and postcopulatory behaviour of both males, and (iii) morphological adaptations of the aedeagus for sperm removal. Eighty-eight percent of M1 males sired all daughters when they were first to perform the precopulatory and postcopulatory ritual, suggesting a linked effect of both rituals on paternity. The number and length of copulations by both males did not affect paternity, and the shape of the aedeagus does not seem to facilitate sperm removal. Our results are consistent with the hypothesis that postcopulatory rituals represent forms of mate guarding that function to increase paternity in the context of sperm competition. DOI
132.Crespi, B. (2014) The Insectan Apes.Human Nature-An Interdisciplinary Biosocial Perspective 25: 6-27 The Insectan Apes
Eusociality; Cooperative breeding; Social insects; Convergence
I present evidence that humans have evolved convergently to social insects with regard to a large suite of social, ecological, and reproductive phenotypes. Convergences between humans and social insects include: (1) groups with genetically and environmentally defined structures; (2) extensive divisions of labor; (3) specialization of a relatively restricted set of females for reproduction, with enhanced fertility; (4) extensive extramaternal care; (5) within-group food sharing; (6) generalized diets composed of high-nutrient-density food; (7) solicitous juveniles, but high rates of infanticide; (8) ecological dominance; (9) enhanced colonizing abilities; and (10) collective, cooperative decision-making. Most of these convergent phenotypic adaptations stem from reorganization of key life-history trade-offs due to behavioral, physiological, and life-historical specializations. Despite their extensive socioreproductive overlap with social insects, humans differ with regard to the central aspect of eusociality: reproductive division of labor. This difference may be underpinned by the high energetic costs of producing offspring with large brains. DOI
131.Crespi, B; Foster, K; Ubeda, F. (2014) First principles of Hamiltonian medicine.Philosophical Transactions of the Royal Society B-Biological Sciences 369 First principles of Hamiltonian medicine
inclusive fitness; health; disease; kinship
We introduce the field of Hamiltonian medicine, which centres on the roles of genetic relatedness in human health and disease. Hamiltonian medicine represents the application of basic social-evolution theory, for interactions involving kinship, to core issues in medicine such as pathogens, cancer, optimal growth and mental illness. It encompasses three domains, which involve conflict and cooperation between: (i) microbes or cancer cells, within humans, (ii) genes expressed in humans, (iii) human individuals. A set of six core principles, based on these domains and their interfaces, serves to conceptually organize the field, and contextualize illustrative examples. The primary usefulness of Hamiltonian medicine is that, like Darwinian medicine more generally, it provides novel insights into what data will be productive to collect, to address important clinical and public health problems. Our synthesis of this nascent field is intended predominantly for evolutionary and behavioural biologists who aspire to address questions directly relevant to human health and disease. DOI
130.Crespi, B; Summers, K. (2014) Inclusive fitness theory for the evolution of religion.Animal Behaviour 92: 313-323 Inclusive fitness theory for the evolution of religion
inclusive fitness; kinship; religious behaviour
We describe and evaluate an integrative hypothesis for the origin and evolution of human religious cognition and behaviour, based on maximization of inclusive fitness. By this hypothesis, the concept of God is represented by one's circle of kin and social salience, such that serving God and serving this circle become synonymous. The theory is supported by data from anthropology, evolutionary theory, psychology, neuroscience, psychiatry, endocrinology and genetics. It is largely compatible with, yet can subsume, previous theories of religion that are also based on adaptation and natural selection. (C) 2014 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. DOI
129.Crespi, BJ; Hurd, PL. (2014) Cognitive-behavioral phenotypes of Williams syndrome are associated with genetic variation in the GTF2I gene, in a healthy population.BMC Neuroscience 15 Cognitive-behavioral phenotypes of Williams syndrome are associated with genetic variation in the GTF2I gene, in a healthy population
Social behavior; Anxiety; Williams syndrome; Autism; GTF2I gene
Background: Individuals with Williams syndrome, a neurogenetic condition caused by deletion of a set of genes at chromosomal location 7q11.23, exhibit a remarkable suite of traits including hypersociality with high, nonselective friendliness and low social anxiety, expressive language relatively well-developed but under-developed social-communication skills overall, and reduced visual-spatial abilities. Deletions and duplications of the Williams-syndrome region have also been associated with autism, and with schizophrenia, two disorders centrally involving social cognition. Several lines of evidence have linked the gene GTF2I (General Transcription Factor lli) with the social phenotypes of Williams syndrome, but a role for this gene in sociality within healthy populations has yet to be investigated. Results: We genotyped a large set of healthy individuals for two single-nucleotide polymorphisms in the GTF2I gene that have recently been significantly associated with autism, and thus apparently exhibit functional effects on autism-related social phenotypes. GTF2I genotypes for these SNPs showed highly significant association with low social anxiety combined with reduced social-communication abilities, which represents a metric of the Williams-syndrome cognitive profile as described from previous studies. Conclusions: These findings implicate the GTF2I gene in the neurogenetic basis of social communication and social anxiety, both in Williams syndrome and among individuals in healthy populations. DOI PubMed
128. Soria-Carrasco, V; Gompert, Z; Comeault, AA; Farkas, TE; Parchman, TL; Johnston, JS; Buerkle, CA; Feder, JL; Bast, J; Schwander, T; Egan, SP; Crespi, BJ; Nosil, P. (2014) Stick Insect Genomes Reveal Natural Selection's Role in Parallel Speciation.Science 344: 738-742 Stick Insect Genomes Reveal Natural Selection's Role in Parallel Speciation
Natural selection can drive the repeated evolution of reproductive isolation, but the genomic basis of parallel speciation remains poorly understood. We analyzed whole-genome divergence between replicate pairs of stick insect populations that are adapted to different host plants and undergoing parallel speciation. We found thousands of modest-sized genomic regions of accentuated divergence between populations, most of which are unique to individual population pairs. We also detected parallel genomic divergence across population pairs involving an excess of coding genes with specific molecular functions. Regions of parallel genomic divergence in nature exhibited exceptional allele frequency changes between hosts in a field transplant experiment. The results advance understanding of biological diversification by providing convergent observational and experimental evidence for selection's role in driving repeatable genomic divergence. DOI
127.Crespi, B. (2013) Developmental heterochrony and the evolution of autistic perception, cognition and behavior.BMC Medicine 11 Developmental heterochrony and the evolution of autistic perception, cognition and behavior
HIGH-FUNCTIONING AUTISM; COMPULSIVE-LIKE BEHAVIOR; WEAK CENTRAL COHERENCE; EMBEDDED FIGURES TEST; SPECTRUM DISORDERS; HUMAN BRAIN; ABSOLUTE PITCH; SCHIZOPHRENIC-PATIENTS; CORTICAL CONNECTIVITY; HIERARCHICAL PATTERNS
Background: Autism is usually conceptualized as a disorder or disease that involves fundamentally abnormal neurodevelopment. In the present work, the hypothesis that a suite of core autism-related traits may commonly represent simple delays or non-completion of typical childhood developmental trajectories is evaluated. Discussion: A comprehensive review of the literature indicates that, with regard to the four phenotypes of (1) restricted interests and repetitive behavior, (2) short-range and long-range structural and functional brain connectivity, (3) global and local visual perception and processing, and (4) the presence of absolute pitch, the differences between autistic individuals and typically developing individuals closely parallel the differences between younger and older children. Summary: The results of this study are concordant with a model of 'developmental heterochrony', and suggest that evolutionary extension of child development along the human lineage has potentiated and structured genetic risk for autism and the expression of autistic perception, cognition and behavior. DOI
126.Crespi, B. (2013) Diametric gene-dosage effects as windows into neurogenetic architecture.Current Opinion in Neurobiology 23: 143-151 Diametric gene-dosage effects as windows into neurogenetic architecture
17Q21.31 MICRODELETION SYNDROME; PRADER-WILLI-SYNDROME; BEHAVIORAL PHENOTYPES; BIPOLAR DISORDER; UP-REGULATION; KANSL1 CAUSE; AUTISM; SCHIZOPHRENIA; MICE; 16P11.2
Gene expression can be modulated in two opposite directions, towards higher or lower amounts of product. How do diametric changes in gene dosage influence neurological development and function? Recent studies of transgenic and knockout mouse models, genomic copy-number variants, imprinted-gene expression alterations, and sex-chromosome aneuploidies are revealing examples of 'mirror-extreme' brain and behavior phenotypes, which provide unique insights into neurodevelopmental architecture. These convergent studies quantitatively connect gene dosages with specific trajectories and outcomes, with important implications for the experimental dissection of normal neurological functions, the genetic analysis of psychiatric disorders, the development of pharmacological therapies, and mechanisms for the evolution of human brain and behavior. DOI
125.Crespi, B; Nosil, P. (2013) Conflictual speciation: species formation via genomic conflict.Trends in Ecology & Evolution 28: 48-57 Conflictual speciation: species formation via genomic conflict
SELFISH GENETIC ELEMENTS; HYBRID MALE-STERILITY; FEMALE MEIOTIC DRIVE; REPRODUCTIVE ISOLATION; TRANSPOSABLE ELEMENTS; X-CHROMOSOME; DROSOPHILA-MELANOGASTER; ECOLOGICAL SPECIATION; SEXUAL-DIMORPHISM; FLOWERING PLANTS
A remarkable suite of forms of genomic conflict has recently been implicated in speciation. We propose that these diverse roles of genomic conflict in speciation processes can be unified using the concept of 'conflictual speciation'. Conflictual speciation centers on the evolution of reproductive isolation as a byproduct of antagonistic selection among genomic elements with divergent fitness interests. Intragenomic conflicts are expected to readily generate Dobzhansky-Muller incompatibilities, due to population-specific interactions between opposing elements, and thus they could be especially important in speciation. Moreover, selection from genomic conflicts should be relatively unrelenting across ecological and evolutionary time scales. We explain how intra-genomic conflicts can promote, or sometimes constrain, speciation, and describe evidence relating conflicts to the evolution of reproductive isolation. DOI
124. Crosley, EJ; Elliot, MG; Christians, JK; Crespi, BJ. (2013) Placental invasion, preeclampsia risk and adaptive molecular evolution at the origin of the great apes: Evidence from genome-wide analyses.Placenta 34: 127-132 Placental invasion, preeclampsia risk and adaptive molecular evolution at the origin of the great apes: Evidence from genome-wide analyses
DEEP TROPHOBLAST INVASION; MATRIX-METALLOPROTEINASES; NONHUMAN-PRIMATES; INSULIN-RECEPTORS; LOWLAND GORILLA; GENE-EXPRESSION; CELL INVASION; ACTIVIN-A; PREGNANCY; INHIBIN
Introduction: Recent evidence from chimpanzees and gorillas has raised doubts that preeclampsia is a uniquely human disease. The deep extravillous trophoblast (EVT) invasion and spiral artery remodeling that characterizes our placenta (and is abnormal in preeclampsia) is shared within great apes, setting Homininae apart from Hylobatidae and Old World Monkeys, which show much shallower trophoblast invasion and limited spiral artery remodeling. We hypothesize that the evolution of a more invasive placenta in the lineage ancestral to the great apes involved positive selection on genes crucial to EVT invasion and spiral artery remodeling. Furthermore, identification of placentally-expressed genes under selection in this lineage may identify novel genes involved in placental development. Methods: We tested for positive selection in approximately 18,000 genes using the ratio of non-synonymous to synonymous amino acid substitution for protein-coding DNA. DAVID Bioinformatics Resources identified biological processes enriched in positively selected genes, including processes related to EVT invasion and spiral artery remodeling. Results: Analyses revealed 295 and 264 genes under significant positive selection on the branches ancestral to Hominidae (Human, Chimp, Gorilla, Orangutan) and Homininae (Human, Chimp, Gorilla), respectively. Gene ontology analysis of these gene sets demonstrated significant enrichments for several functional gene clusters relevant to preeclampsia risk, and sets of placentally-expressed genes that have been linked with preeclampsia and/or trophoblast invasion in other studies. Conclusion: Our study represents a novel approach to the identification of candidate genes and amino acid residues involved in placental pathologies by implicating them in the evolution of highly-invasive placenta. (C) 2012 Elsevier Ltd. All rights reserved. DOI
123. Dinsdale, N; Crespi, BJ. (2013) THE BORDERLINE EMPATHY PARADOX: EVIDENCE AND CONCEPTUAL MODELS FOR EMPATHIC ENHANCEMENTS IN BORDERLINE PERSONALITY DISORDER.Journal of Personality Disorders 27: 172-195 THE BORDERLINE EMPATHY PARADOX: EVIDENCE AND CONCEPTUAL MODELS FOR EMPATHIC ENHANCEMENTS IN BORDERLINE PERSONALITY DISORDER
HIGH-FUNCTIONING AUTISM; EMOTIONAL INTELLIGENCE; FACIAL EXPRESSIONS; ASPERGER-SYNDROME; REJECTION SENSITIVITY; SOCIAL COGNITION; MIND; RECOGNITION; SCHIZOPHRENIA; ADULTS
Empirical evidence and therapeutic interactions have suggested that individuals with borderline personality disorder (BPD) may demonstrate enhancements in aspects of social-emotional cognition. To assess the empirical evidence for this phenomenon, and to comprehensively evaluate alternative hypotheses for its possible role in BPD etiology and symptoms, the authors systematically searched the literature for investigations of empathy in BPD and reviewed 28 studies assessing a range of empathic abilities. Considered together, these data demonstrated comparable levels of evidence for enhanced, preserved, and reduced empathic skills in individuals with BPD. Evidence for empathic enhancements is thus substantial but inconsistent across studies, being found mainly under more socially interactive experimental paradigms. Based on the results of the review and previous explanations for BPD symptoms, the authors propose a new model for explaining the borderline paradox: that a combination of increased attention to social stimuli and dysfunctional social information processing may account in part for the specific empathic enhancements and reduced overall social functioning in BPD.
122. Dinsdale, NL; Hurd, PL; Wakabayashi, A; Elliot, M; Crespi, BJ. (2013) How Are Autism and Schizotypy Related? Evidence from a Non-Clinical Population.PLOS One 8 How Are Autism and Schizotypy Related? Evidence from a Non-Clinical Population
SPECTRUM QUOTIENT AQ; HIGH-FUNCTIONING AUTISM; GENERAL-POPULATION; MAGICAL IDEATION; MIXED-HANDEDNESS; HAND PREFERENCE; SEX-DIFFERENCES; SOCIAL BRAIN; SCHIZOPHRENIA; DISORDERS
Both autism spectrum conditions (ASCs) and schizophrenia spectrum conditions (SSCs) involve altered or impaired social and communicative functioning, but whether these shared features indicate overlapping or different etiological factors is unknown. We outline three hypotheses (overlapping, independent, and diametric) for the possible relationship between ASCs and SSCs, and compare their predictions for the expected relationships between autistic and schizotypal phenotypes using the Autism Spectrum Quotient and the Schizotypal Personality Questionnaire-Brief Revised from a large non-clinical sample of undergraduate students. Consistent with previous research, autistic features were positively associated with several schizotypal features, with the most overlap occurring between interpersonal schizotypy and autistic social and communication phenotypes. The first component of a principal components analysis (PCA) of subscale scores reflected these positive correlations, and suggested the presence of an axis (PC1) representing general social interest and aptitude. By contrast, the second principal component (PC2) exhibited a pattern of positive and negative loadings indicative of an axis from autism to positive schizotypy, such that positive schizotypal features loaded in the opposite direction to core autistic features. These overall PCA patterns were replicated in a second data set from a Japanese population. To evaluate the validity of our interpretation of the PCA results, we measured handedness and mental rotation ability, as these are established correlates of SSCs and ASCs, respectively. PC2 scores were significantly associated with hand preference, such that increasingly 'schizotypal' scores predicted reduced strength of handedness, which is consistent with previous research. PC1 scores were positively related to performance on the mental rotation task, suggesting trade-offs between social skills and visual-spatial ability. These results provide novel evidence for an autism-positive schizotypy axis, and highlight the importance of recognizing that psychological variation involving reduced social interest and functioning may have diverse causes. DOI
121. Konefal, S; Elliot, M; Crespi, B. (2013) The adaptive significance of adult neurogenesis: an integrative approach.Frontiers in Neuroanatomy 7 The adaptive significance of adult neurogenesis: an integrative approach
LONG-TERM POTENTIATION; NEURAL STEM-CELLS; GENERATED GRANULE CELLS; ENHANCED SYNAPTIC PLASTICITY; BORN HIPPOCAMPAL-NEURONS; OLFACTORY-BULB NEURONS; DENTATE GYRUS; PATTERN SEPARATION; ENTORHINAL CORTEX; NEWBORN NEURONS
Adult neurogenesis in mammals is predominantly restricted to two brain regions, the dentate gyrus (DG) of the hippocampus and the olfactory bulb (OB), suggesting that these two brain regions uniquely share functions that mediate its adaptive significance. Benefits of adult neurogenesis across these two regions appear to converge on increased neuronal and structural plasticity that subserves coding of novel, complex, and fine-grained information, usually with contextual components that include spatial positioning. By contrast, costs of adult neurogenesis appear to center on potential for dysregulation resulting in higher risk of brain cancer or psychological dysfunctions, but such costs have yet to be quantified directly. The three main hypotheses for the proximate functions and adaptive significance of adult neurogenesis, pattern separation, memory consolidation, and olfactory spatial, are not mutually exclusive and can be reconciled into a simple general model amenable to targeted experimental and comparative tests. Comparative analysis of brain region sizes across two major social ecological groups of primates, gregarious (mainly diurnal haplorhines, visually-oriented, and in large social groups) and solitary (mainly noctural, territorial, and highly reliant on olfaction, as in most rodents) suggest that solitary species, but not gregarious species, show positive associations of population densities and home range sizes with sizes of both the hippocampus and OB, implicating their functions in social territorial systems mediated by olfactory cues. Integrated analyses of the adaptive significance of adult neurogenesis will benefit from experimental studies motivated and structural by ecologically and socially relevant selective contexts. DOI
120. Leach, EL; Hurd, PL; Crespi, BJ. (2013) Schizotypy, cognitive performance, and genetic risk for schizophrenia in a non-clinical population.Personality and Individual Differences 55: 334-338 Schizotypy, cognitive performance, and genetic risk for schizophrenia in a non-clinical population
MENTAL ROTATION ABILITY; SEX-DIFFERENCES; ASSOCIATION; GENOTYPE; TRAITS; DTNBP1; IMPACT; COMT
Schizophrenia risk alleles are expected to mediate effects on cognitive task performance, and aspects of personality including schizotypy, in nonclinical populations. We investigated how 32 of the best-validated schizophrenia risk alleles, singly and as summed genetic risk, were related to measures of schizotypal personality and measures of two aspects of cognitive performance, verbal skills (vocabulary) and visual-spatial skills (mental rotation), in healthy individuals. Summed genetic risk score was not associated with levels of total schizotypy or its three main subscales. Similarly, genotypic variation at none of the individual risk loci was related to cognitive performance measures, after correction for multiple tests. Higher overall genetic risk score was, however, associated with lower performance on the mental rotation test in males, with a broad set of loci contributing to this effect. These results imply that there is a lack of linear, genetically-based continuity connecting schizotypal cognition with the expression of schizophrenia itself, and indicate that, for males, higher genetic risk of schizophrenia exerts negative effects on visual-spatial skills, as measured by mental rotation. (c) 2013 Elsevier Ltd. All rights reserved. DOI
119. Ryan, CP; Crespi, BJ. (2013) Androgen receptor polyglutamine repeat number: models of selection and disease susceptibility.Evolutionary Applications 6: 180-196 Androgen receptor polyglutamine repeat number: models of selection and disease susceptibility
PROSTATE-CANCER RISK; BULBAR MUSCULAR-ATROPHY; GENE CAG REPEAT; SIMPLE SEQUENCE REPEATS; CORONARY-ARTERY-DISEASE; BONE-MINERAL DENSITY; ACID TANDEM REPEATS; HUMAN BREAST-CANCER; MALE-INFERTILITY; PERSONALITY-TRAITS
Variation in polyglutamine repeat number in the androgen receptor (AR CAGn) is negatively correlated with the transcription of androgen-responsive genes and is associated with susceptibility to an extensive list of human disease. Only a small portion of the heritability for many of these diseases is explained by conventional SNP-based genome-wide association studies, and the forces shaping AR CAGn among humans remains largely unexplored. Here, we propose evolutionary models for understanding selection at the AR CAG locus, namely balancing selection, sexual conflict, accumulation-selection, and antagonistic pleiotropy. We evaluate these models by examining AR CAGn-linked susceptibility to eight extensively studied diseases representing the diverse physiological roles of androgens, and consider the costs of these diseases by their frequency and fitness effects. Five diseases could contribute to the distribution of AR CAGn observed among contemporary human populations. With support for disease susceptibilities associated with long and short AR CAGn, balancing selection provides a useful model for studying selection at this locus. Gender-specific differences AR CAGn health effects also support this locus as a candidate for sexual conflict over repeat number. Accompanied by the accumulation of AR CAGn in humans, these models help explain the distribution of repeat number in contemporary human populations. DOI
118. Schwander, T; Arbuthnott, D; Gries, R; Gries, G; Nosil, P; Crespi, BJ. (2013) Hydrocarbon divergence and reproductive isolation in Timema stick insects.BMC Evolutionary Biology 13 Hydrocarbon divergence and reproductive isolation in Timema stick insects
HOST-PLANT ADAPTATION; CRISTINAE WALKING-STICKS; MALE MATE CHOICE; CUTICULAR HYDROCARBONS; SEXUAL SELECTION; DROSOPHILA-MOJAVENSIS; MORPHOLOGICAL EVOLUTION; CACTOPHILIC DROSOPHILA; INCIPIENT SPECIATION; MATING PREFERENCES
Background: Individuals commonly prefer certain trait values over others when choosing their mates. If such preferences diverge between populations, they can generate behavioral reproductive isolation and thereby contribute to speciation. Reproductive isolation in insects often involves chemical communication, and cuticular hydrocarbons, in particular, serve as mate recognition signals in many species. We combined data on female cuticular hydrocarbons, interspecific mating propensity, and phylogenetics to evaluate the role of cuticular hydrocarbons in diversification of Timema walking-sticks. Results: Hydrocarbon profiles differed substantially among the nine analyzed species, as well as between partially reproductively-isolated T. cristinae populations adapted to different host plants. In no-choice trials, mating was more likely between species with similar than divergent hydrocarbon profiles, even after correcting for genetic divergences. The macroevolution of hydrocarbon profiles, along a Timema species phylogeny, fits best with a punctuated model of phenotypic change concentrated around speciation events, consistent with change driven by selection during the evolution of reproductive isolation. Conclusion: Altogether, our data indicate that cuticular hydrocarbon profiles vary among Timema species and populations, and that most evolutionary change in hydrocarbon profiles occurs in association with speciation events. Similarities in hydrocarbon profiles between species are correlated with interspecific mating propensities, suggesting a role for cuticular hydrocarbon profiles in mate choice and speciation in the genus Timema. DOI
117. Schwander, T; Crespi, BJ; Gries, R; Gries, G. (2013) Neutral and selection-driven decay of sexual traits in asexual stick insects.Proceedings of the Royal Society B-Biological Sciences 280 Neutral and selection-driven decay of sexual traits in asexual stick insects
TIMEMA WALKING-STICKS; WOLBACHIA-INDUCED PARTHENOGENESIS; LEPTOPILINA-CLAVIPES HYMENOPTERA; EVOLUTION; REPRODUCTION; ANCIENT; VESTIGIALIZATION; PHYLOGENETICS; PARASITOIDS; APHELINIDAE
Environmental shifts and lifestyle changes may result in formerly adaptive traits becoming non-functional or maladaptive. The subsequent decay of such traits highlights the importance of natural selection for adaptations, yet its causes have rarely been investigated. To study the fate of formerly adaptive traits after lifestyle changes, we evaluated sexual traits in five independently derived asexual lineages, including traits that are specific to males and therefore not exposed to selection. At least four of the asexual lineages retained the capacity to produce males that display normal courtship behaviours and are able to fertilize eggs of females from related sexual species. The maintenance of male traits may stem from pleiotropy, or from these traits only regressing via drift, which may require millions of years to generate phenotypic effects. By contrast, we found parallel decay of sexual traits in females. Asexual females produced altered airborne and contact signals, had modified sperm storage organs, and lost the ability to fertilize their eggs, impeding reversals to sexual reproduction. Female sexual traits were decayed even in recently derived asexuals, suggesting that trait changes following the evolution of asexuality, when they occur, proceed rapidly and are driven by selective processes rather than drift. DOI
116. Stencel, A; Crespi, B. (2013) What is a genome?Molecular Ecology 22: 3437-3443 What is a genome?
HORIZONTAL GENE-TRANSFER; TRANSPOSABLE ELEMENTS; EVOLUTION; CHROMOSOME; HISTORY; ENCODE; DNA; INTROGRESSION; DIVERSITY; SEQUENCES
The field of genomics is expanding rapidly, yet the meanings of the word genome' have yet to be conceptualized in explicit, coherent and useful frameworks. We develop and apply an evolutionary conceptualization of the genome, which represents a logical extension of the evolutionary definition of a gene developed by George C. Williams. An evolutionary genome thus represents a set of genetic material, in a lineage, that due to common interests tends to favour the same or similar phenotypes. This conceptualization provides novel perspectives on genome functions, boundaries and evolution, which should help to guide theoretical and empirical genomics research. DOI
115. Antolin, MF; Jenkins, KP; Bergstrom, CT; Crespi, BJ; De, S; Hancock, A; Hanley, KA; Meagher, TR; Moreno-Estrada, A; Nesse, RM; Omenn, GS; Stearns, SC. (2012) EVOLUTION AND MEDICINE IN UNDERGRADUATE EDUCATION: A PRESCRIPTION FOR ALL BIOLOGY STUDENTS.Evolution 66: 1991-2006 EVOLUTION AND MEDICINE IN UNDERGRADUATE EDUCATION: A PRESCRIPTION FOR ALL BIOLOGY STUDENTS
Biomedical research; evolution of disease; host-pathogen interactions; human genetics; medical practice; mismatch hypothesis; premedical curriculum; public health; science education
The interface between evolutionary biology and the biomedical sciences promises to advance understanding of the origins of genetic and infectious diseases in humans, potentially leading to improved medical diagnostics, therapies, and public health practices. The biomedical sciences also provide unparalleled examples for evolutionary biologists to explore. However, gaps persist between evolution and medicine, for historical reasons and because they are often perceived as having disparate goals. Evolutionary biologists have a role in building a bridge between the disciplines by presenting evolutionary biology in the context of human health and medical practice to undergraduates, including premedical and preprofessional students. We suggest that students will find medical examples of evolution engaging. By making the connections between evolution and medicine clear at the undergraduate level, the stage is set for future health providers and biomedical scientists to work productively in this synthetic area. Here, we frame key evolutionary concepts in terms of human health, so that biomedical examples may be more easily incorporated into evolution courses or more specialized courses on evolutionary medicine. Our goal is to aid in building the scientific foundation in evolutionary biology for all students, and to encourage evolutionary biologists to join in the integration of evolution and medicine. DOI
114.Crespi, B; Schwander, T. (2012) Asexual evolution: do intragenomic parasites maintain sex?Molecular Ecology 21: 3893-3895 Asexual evolution: do intragenomic parasites maintain sex?
adaptation; animal mating; breeding systems; ecological genetics; evolution of sex
Resolving the paradox of sex, with its twofold cost to genic transmission, remains one of the major unresolved questions in evolutionary biology. Counting this genetic cost has now gone genomic. In this issue of Molecular Ecology, Kraaijeveld (2012) describe the first genome-scale comparative study of related sexual and asexual animal lineages, to test the hypothesis that asexuals bear heavier loads of deleterious transposable elements. A much higher density of such parasites might be expected, due to the inability of asexual lineages to purge transposons via mechanisms exclusive to sexual reproduction. They find that the answer is yesand nodepending upon the family of transposons considered. Like many such advances in testing theory, more questions are raised by this study than answered, but a door has been opened to molecular evolutionary analyses of how responses to selection from intragenomic parasites might mediate the costs of sex. DOI
111. Henry, L; Schwander, T; Crespi, BJ. (2012) Deleterious Mutation Accumulation in Asexual Timema Stick Insects.Molecular Biology and Evolution 29: 401-408 Deleterious Mutation Accumulation in Asexual Timema Stick Insects
CYTOCHROME-OXIDASE-I; FRESH-WATER SNAIL; SEXUAL REPRODUCTION; ANCIENT ASEXUALITY; BDELLOID ROTIFERS; EVOLUTION; SELECTION; PATTERNS; PARTHENOGENESIS; RECOMBINATION
Sexual reproduction is extremely widespread in spite of its presumed costs relative to asexual reproduction, indicating that it must provide significant advantages. One postulated benefit of sex and recombination is that they facilitate the purging of mildly deleterious mutations, which would accumulate in asexual lineages and contribute to their short evolutionary life span. To test this prediction, we estimated the accumulation rate of coding (nonsynonymous) mutations, which are expected to be deleterious, in parts of one mitochondrial (COI) and two nuclear (Actin and Hsp70) genes in six independently derived asexual lineages and related sexual species of Timema stick insects. We found signatures of increased coding mutation accumulation in all six asexual Timema and for each of the three analyzed genes, with 3.6- to 13.4-fold higher rates in the asexuals as compared with the sexuals. In addition, because coding mutations in the asexuals often resulted in considerable hydrophobicity changes at the concerned amino acid positions, coding mutations in the asexuals are likely associated with more strongly deleterious effects than in the sexuals. Our results demonstrate that deleterious mutation accumulation can differentially affect sexual and asexual lineages and support the idea that deleterious mutation accumulation plays an important role in limiting the long-term persistence of all-female lineages. DOI
110. Joy, JB; Crespi, BJ. (2012) Island phytophagy: explaining the remarkable diversity of plant-feeding insects.Proceedings of the Royal Society B-Biological Sciences 279: 3250-3255 Island phytophagy: explaining the remarkable diversity of plant-feeding insects
macroevolution; plant-insect interactions; diversification; island biogeography; plant genetic distinctiveness; insularity
Plant-feeding insects have undergone unparalleled diversification among different plant taxa, yet explanations for variation in their diversity lack a quantitative, predictive framework. Island biogeographic theory has been applied to spatially discrete habitats but not to habitats, such as host plants, separated by genetic distance. We show that relationships between the diversity of gall-inducing flies and their host plants meet several fundamental predictions from island biogeographic theory. First, plant-taxon genetic distinctiveness, an integrator for long-term evolutionary history of plant lineages, is a significant predictor of variance in the diversity of gall-inducing flies among host-plant taxa. Second, range size and structural complexity also explain significant proportions of the variance in diversity of gall-inducing flies among different host-plant taxa. Third, as with other island systems, plant-lineage age does not predict species diversity. Island biogeographic theory, applied to habitats defined by genetic distance, provides a novel, comprehensive framework for analysing and explaining the diversity of plant-feeding insects and other host-specific taxa. DOI
107.Crespi, B. (2011) The evolutionary biology of child health.Proceedings of the Royal Society B-Biological Sciences 278: 1441-1449 The evolutionary biology of child health
evolutionary medicine; child health; cancer; growth
I apply evolutionary perspectives and conceptual tools to analyse central issues underlying child health, with emphases on the roles of human-specific adaptations and genomic conflicts in physical growth and development. Evidence from comparative primatology, anthropology, physiology and human disorders indicates that child health risks have evolved in the context of evolutionary changes, along the human lineage, affecting the timing, growth-differentiation phenotypes and adaptive significance of prenatal stages, infancy, childhood, juvenility and adolescence. The most striking evolutionary changes in humans are earlier weaning and prolonged subsequent pre-adult stages, which have structured and potentiated maladaptations related to growth and development. Data from human genetic and epigenetic studies, and mouse models, indicate that growth, development and behaviour during pre-adult stages are mediated to a notable degree by effects from genomic conflicts and imprinted genes. The incidence of cancer, the primary cause of non-infectious childhood mortality, mirrors child growth rates from birth to adolescence, with paediatric cancer development impacted by imprinted genes that control aspects of growth. Understanding the adaptive significance of child growth and development phenotypes, in the context of human-evolutionary changes and genomic conflicts, provides novel insights into the causes of disease in childhood. DOI
103.Crespi, BJ. (2011) The emergence of human-evolutionary medical genomics.Evolutionary Applications 4 The emergence of human-evolutionary medical genomics
disease risk; evolutionary medicine; genetics; genome-wide; human evolution
In this review, I describe how evolutionary genomics is uniquely suited to spearhead advances in understanding human disease risk, owing to the privileged position of genes as fundamental causes of phenotypic variation, and the ability of population genetic and phylogenetic methods to robustly infer processes of natural selection, drift, and mutation from genetic variation at the levels of family, population, species, and clade. I first provide an overview of models for the origins and maintenance of genetically based disease risk in humans. I then discuss how analyses of genetic disease risk can be dovetailed with studies of positive and balancing selection, to evaluate the degree to which the 'genes that make us human' also represent the genes that mediate risk of polygenic disease. Finally, I present four basic principles for the nascent field of human evolutionary medical genomics, each of which represents a process that is nonintuitive from a proximate perspective. Joint consideration of these principles compels novel forms of interdisciplinary analyses, most notably studies that (i) analyze tradeoffs at the level of molecular genetics, and (ii) identify genetic variants that are derived in the human lineage or in specific populations, and then compare individuals with derived versus ancestral alleles. DOI
102.Crespi, BJ; Thiselton, DL. (2011) Comparative immunogenetics of autism and schizophrenia.Genes Brain and Behavior 10: 689-701 Comparative immunogenetics of autism and schizophrenia
ARTHRITIS-SHARED EPITOPE; HLA CLASS-II; NITRIC-OXIDE METABOLITES; GENOME-WIDE ASSOCIATION; RHEUMATOID-ARTHRITIS; SPECTRUM DISORDERS; AUTOIMMUNE-DISEASES; LINKAGE DISEQUILIBRIUM; CHROMOSOME 6P21.3; FAMILY-HISTORY
Autism and schizophrenia are highly heritable neurodevelopmental disorders, each mediated by a diverse suite of genetic and environmental risk factors. Comorbidity and familial aggregation of such neurodevelopmental disorders with other disease-related conditions can provide important insights into their etiology. Epidemiological studies have documented reduced rates of rheumatoid arthritis, a systemic autoimmune condition, in schizophrenia, and recent work has shown increased rates of rheumatoid arthritis in first-degree relatives of autistic individuals, especially mothers. Advances in understanding the genetic basis of rheumatoid arthritis have shown that much of the genetic liability to this condition is due to risk and protective alleles at the HLA DRB1 locus. These data allow robust testing of the hypotheses that allelic variation at DRB1 pleiotropically modulates risk of rheumatoid arthritis, autism and schizophrenia. Systematic review of the literature indicates that reported associations of DRB1 variants with these three conditions are congruent with a pleiotropic model: DRB1*04 alleles have been associated with increased risk of rheumatoid arthritis and autism but decreased risk of schizophrenia, and DRB1*13 alleles have been associated with protection from rheumatoid arthritis and autism but higher risk of schizophrenia. These convergent findings from genetics and epidemiology imply that a subset of autism and schizophrenia cases may be underlain by genetically based neuroimmune alterations, and that analyses of the causes of risk and protective effects from DRB1 variants may provide new approaches to therapy. DOI
101. Frank, SA; Crespi, BJ. (2011) Pathology from evolutionary conflict, with a theory of X chromosome versus autosome conflict over sexually antagonistic traits.Proceedings of the National Academy of Sciences of the United States of America 108: 10886-10893 Pathology from evolutionary conflict, with a theory of X chromosome versus autosome conflict over sexually antagonistic traits
BECKWITH-WIEDEMANN-SYNDROME; PRADER-WILLI-SYNDROME; SILVER-RUSSELL-SYNDROME; ANGELMAN-SYNDROME; TUMOR RISK; PARENTAL ANTAGONISM; GENE-EXPRESSION; BIRTH-WEIGHT; FETAL-GROWTH; SELECTION
Evolutionary conflicts cause opponents to push increasingly hard and in opposite directions on the regulation of traits. One can see only the intermediate outcome from the balance of the exaggerated and opposed forces. Intermediate expression hides the underlying conflict, potentially misleading one to conclude that trait regulation is designed to achieve efficient and robust expression, rather than arising by the precarious resolution of conflict. Perturbation often reveals the underlying nature of evolutionary conflict. Upon mutation or knockout of one side in the conflict, the other previously hidden and exaggerated push on the trait may cause extreme, pathological expression. In this regard, pathology reveals hidden evolutionary design. We first review several evolutionary conflicts between males and females, including conflicts over mating, fertilization, and the growth rate of offspring. Perturbations of these conflicts lead to infertility, misregulated growth, cancer, behavioral abnormalities, and psychiatric diseases. We then turn to antagonism between the sexes over traits present in both males and females. For many traits, the different sexes favor different phenotypic values, and constraints prevent completely distinct expression in the sexes. In this case of sexual antagonism, we present a theory of conflict between X-linked genes and autosomal genes. We suggest that dysregulation of the exaggerated conflicting forces between the X chromosome and the autosomes may be associated with various pathologies caused by extreme expression along the male-female axis. Rapid evolution of conflicting X-linked and autosomal genes may cause divergence between populations and speciation. DOI
100. Schwander, T; Henry, L; Crespi, BJ. (2011) Molecular Evidence for Ancient Asexuality in Timema Stick Insects.Current Biology 21: 1129-1134 Molecular Evidence for Ancient Asexuality in Timema Stick Insects
SEXUAL REPRODUCTION; BDELLOID ROTIFERS; HYBRID ORIGINS; DNA-SEQUENCES; EVOLUTION; RECOMBINATION; POPULATION; LINEAGES; PARTHENOGENESIS; PATTERNS
Asexuality is rare in animals in spite of its apparent advantage relative to sexual reproduction, indicating that it must be associated with profound costs [1-9]. One expectation is that reproductive advantages gained by new asexual lineages will be quickly eroded over time [3, 5-7]. Ancient asexual taxa that have evolved and adapted without sex would be "scandalous" exceptions to this rule, but it is often difficult to exclude the possibility that putative asexuals deploy some form of "cryptic" sex, or have abandoned sex more recently than estimated from divergence times to sexual relatives [10]. Here we provide evidence, from high intraspecific divergence of mitochondrial sequence and nuclear allele divergence patterns, that several independently derived Timema stick-insect lineages have persisted without recombination for more than a million generations. Nuclear alleles in the asexual lineages displayed significantly higher intraindividual divergences than in related sexual species. In addition, within two asexuals, nuclear allele phylogenies suggested the presence of two clades, with sequences from the same individual appearing in both clades. These data strongly support ancient asexuality in Timema and validate the genus as an exceptional opportunity to attack the question of how asexual reproduction can be maintained over long periods of evolutionary time. DOI
99. Somjee, U; Ablard, K; Crespi, B; Schaefer, PW; Gries, G. (2011) Local mate competition in the solitary parasitoid wasp Ooencyrtus kuvanae.Behavioral Ecology and Sociobiology 65: 1071-1077 Local mate competition in the solitary parasitoid wasp Ooencyrtus kuvanae
Local mate competition; Ooencyrtus kuvanae; Solitary egg parasitoid; Sex ratio; Local resource
Local mate competition (LMC) occurs when brothers compete with each other for mating opportunities, resulting in selection for a female-biased sex ratio within local groups. If multiple females oviposit in the same patch, their sons compete for mating opportunities with non-brothers. Females, in the presence of other females, should thus produce relatively more sons. Sex ratio theory also predicts a more female-biased sex ratio when ovipositing females are genetically related, and sex-ratio responses to foundress size if it differentially affects fitness gains from sons versus daughters. The mating system of the parasitoid wasp Ooencyrtus kuvanae meets assumptions of LMC. Females insert a single egg into each accessible egg of gypsy moth, Lymantria dispar, host egg masses. Wasps complete development inside host eggs and emerge en masse, as sexually mature adults, resulting in intense competition among brothers. We tested the hypothesis that O. kuvanae exhibits LMC by manipulating the number of wasp foundresses on egg masses with identical numbers of eggs. As predicted by LMC theory, with increasing numbers of wasp foundresses on an egg mass, the proportions of emerging sons increased. In contrast, the presence of a sibling compared to a non-sibling female during oviposition, or the size of a female, did not affect the number or sex ratio of offspring produced. The O. kuvanae system differs from others in that larvae do not compete for local resources and thus do not distort the sex ratio in favor of sons. With no resource competition among O. kuvanae larvae, the sex ratio of emergent son and daughter wasps is due entirely to the sex allocation by ovipositing wasp foundresses on host egg masses.Website DOI
98. Springer, SA; Crespi, BJ; Swanson, WJ. (2011) Beyond the phenotypic gambit: molecular behavioural ecology and the evolution of genetic architecture.Molecular Ecology 20: 2240-2257 Beyond the phenotypic gambit: molecular behavioural ecology and the evolution of genetic architecture
adaptation; behaviour; social evolution; evolutionary conflict; genetic architecture
Most studies of behaviour examine traits whose proximate causes include sensory input and neural decision-making, but conflict and collaboration in biological systems began long before brains or sensory systems evolved. Many behaviours result from non-neural mechanisms such as direct physical contact between recognition proteins or modifications of development that coincide with altered behaviour. These simple molecular mechanisms form the basis of important biological functions and can enact organismal interactions that are as subtle, strategic and interesting as any. The genetic changes that underlie divergent molecular behaviours are often targets of selection, indicating that their functional variation has important fitness consequences. These behaviours evolve by discrete units of quantifiable phenotypic effect (amino acid and regulatory mutations, often by successive mutations of the same gene), so the role of selection in shaping evolutionary change can be evaluated on the scale at which heritable phenotypic variation originates. We describe experimental strategies for finding genes that underlie biochemical and developmental alterations of behaviour, survey the existing literature highlighting cases where the simplicity of molecular behaviours has allowed insight to the evolutionary process and discuss the utility of a genetic knowledge of the sources and spectrum of phenotypic variation for a deeper understanding of how genetic and phenotypic architectures evolve. DOI
97. Arbuthnott, D; Elliot, MG; Mcpeek, MA; Crespi, BJ. (2010) Divergent patterns of diversification in courtship and genitalic characters of Timema walking-sticks.Journal of Evolutionary Biology 23: 1399-1411 Divergent patterns of diversification in courtship and genitalic characters of Timema walking-sticks
courtship evolution; genitalia; phylogenetics; reproductive isolation; speciation
Understanding the patterns of diversification in sexual traits and the selection underlying such diversification represents a major unresolved question in evolutionary biology. We examined the phylogenetic diversification for courtship and external genitalic characters across ten species of Timema walking-sticks, to infer the tempos and modes of character change in these sexual traits and to draw inferences regarding the selective pressures underlying speciation and diversification in this clade. Rates of inferred change in male courtship behaviours were proportional to speciation events, but male external genitalic structures showed a pattern of continuous change across evolutionary time, with divergence proportional to branch lengths. These findings suggest that diversification of courtship behaviour is mediated by processes that occur in association with speciation, whereas diversification of genitalia occurs more or less continuously, most likely driven by forces of sexual selection. DOI
96.Crespi, B; Stead, P; Elliot, M. (2010) Comparative genomics of autism and schizophrenia.Proceedings of the National Academy of Sciences of the United States of America 107: 1736-1741 Comparative genomics of autism and schizophrenia
genetics; evolution; psychiatry
We used data from studies of copy-number variants (CNVs), single-gene associations, growth-signaling pathways, and intermediate phenotypes associated with brain growth to evaluate four alternative hypotheses for the genomic and developmental relationships between autism and schizophrenia: (i) autism subsumed in schizophrenia, (ii) independence, (iii) diametric, and (iv) partial overlap. Data from CNVs provides statistical support for the hypothesis that autism and schizophrenia are associated with reciprocal variants, such that at four loci, deletions predispose to one disorder, whereas duplications predispose to the other. Data from single-gene studies are inconsistent with a hypothesis based on independence, in that autism and schizophrenia share associated genes more often than expected by chance. However, differentiation between the partial overlap and diametric hypotheses using these data is precluded by limited overlap in the specific genetic markers analyzed in both autism and schizophrenia. Evidence from the effects of risk variants on growth-signaling pathways shows that autism-spectrum conditions tend to be associated with up-regulation of pathways due to loss of function mutations in negative regulators, whereas schizophrenia is associated with reduced pathway activation. Finally, data from studies of head and brain size phenotypes indicate that autism is commonly associated with developmentally-enhanced brain growth, whereas schizophrenia is characterized, on average, by reduced brain growth. These convergent lines of evidence appear most compatible with the hypothesis that autism and schizophrenia represent diametric conditions with regard to their genomic underpinnings, neurodevelopmental bases, and phenotypic manifestations as reflecting under-development versus dysregulated over-development of the human social brain. DOI
95.Crespi, B; Summers, K; Dorus, S. (2010) Evolutionary genomics of human intellectual disability.Evolutionary Applications 3: 52-63 Evolutionary genomics of human intellectual disability
LINKED MENTAL-RETARDATION; NIJMEGEN-BREAKAGE-SYNDROME; AARSKOG-SCOTT-SYNDROME; REGULATING BRAIN SIZE; RHO-FAMILY GTPASES; FRAGILE-X-SYNDROME; POSITIVE SELECTION; DNA-DAMAGE; ADAPTIVE EVOLUTION; COGNITIVE-ABILITY
Previous studies have postulated that X-linked and autosomal genes underlying human intellectual disability may have also mediated the evolution of human cognition. We have conducted the first comprehensive assessment of the extent and patterns of positive Darwinian selection on intellectual disability genes in humans. We report three main findings. First, as noted in some previous reports, intellectual disability genes with primary functions in the central nervous system exhibit a significant concentration to the X chromosome. Second, there was no evidence for a higher incidence of recent positive selection on X-linked than autosomal intellectual disability genes, nor was there a higher incidence of selection on such genes overall, compared to sets of control genes. However, the X-linked intellectual disability genes inferred to be subject to recent positive selection were concentrated in the Rho GTP-ase pathway, a key signaling pathway in neural development and function. Third, among all intellectual disability genes, there was evidence for a higher incidence of recent positive selection on genes involved in DNA repair, but not for genes involved in other functions. These results provide evidence that alterations to genes in the Rho GTP-ase and DNA-repair pathways may play especially-important roles in the evolution of human cognition and vulnerability to genetically-based intellectual disability. DOI
94.Crespi, Bernard J. (2010) The origins and evolution of genetic disease risk in modern humans.Ann N Y Acad Sci 1206: 80-109 The origins and evolution of genetic disease risk in modern humans.
human evolution;polygenic disease;genetics
Patterns and risks of human disease have evolved. In this article, I review evidence regarding the importance of recent adaptive evolution, positive selection, and genomic conflicts in shaping the genetic and phenotypic architectures of polygenic human diseases. Strong recent selection in human populations can create and maintain genetically based disease risk primarily through three processes: increased scope for dysregulation from recent human adaptations, divergent optima generated by intraspecific genomic conflicts, and transient or stable deleterious by-products of positive selection caused by antagonistic pleiotropy, ultimately due to trade-offs at the levels of molecular genetics, development, and physiology. Human disease due to these processes appears to be concentrated in three sets of phenotypes: cognition and emotion, reproductive traits, and life-history traits related to long life-span. Diverse, convergent lines of evidence suggest that a small set of tissues whose pleiotropic patterns of gene function and expression are under especially strong selection-brain, placenta, testis, prostate, breast, and ovary-has mediated a considerable proportion of disease risk in modern humans. @ 2010 New York Academy of Sciences. DOI
92. Schwander, T; Vuilleumier, S; Dubman, J; Crespi, BJ. (2010) Positive feedback in the transition from sexual reproduction to parthenogenesis.Proceedings of the Royal Society B-Biological Sciences 277: 1435-1442 Positive feedback in the transition from sexual reproduction to parthenogenesis
Understanding how new phenotypes evolve is challenging because intermediate stages in transitions from ancestral to derived phenotypes often remain elusive. Here we describe and evaluate a new mechanism facilitating the transition from sexual reproduction to parthenogenesis. In many sexually reproducing species, a small proportion of unfertilized eggs can hatch spontaneously ('tychoparthenogenesis') and develop into females. Using an analytical model, we show that if females are mate-limited, tychoparthenogenesis can result in the loss of males through a positive feedback mechanism whereby tychoparthenogenesis generates female-biased sex ratios and increasing mate limitation. As a result, the strength of selection for tychoparthenogenesis increases in concert with the proportion of tychoparthenogenetic offspring in the sexual population. We then tested the hypothesis that mate limitation selects for tychoparthenogenesis and generates female-biased sex ratios, using data from natural populations of sexually reproducing Timema stick insects. Across 41 populations, both the tychoparthenogenesis rates and the proportions of females increased exponentially as the density of individuals decreased, consistent with the idea that low densities of individuals result in mate limitation and selection for reproductive insurance through tychoparthenogenesis. Our model and data from Timema populations provide evidence for a simple mechanism through which parthenogenesis can evolve rapidly in a sexual population. DOI
91. Summers, K; Crespi, BJ. (2010) Xmrks the spot: life history tradeoffs, sexual selection and the evolutionary ecology of oncogenesis.Molecular Ecology 19: 3022-3024 Xmrks the spot: life history tradeoffs, sexual selection and the evolutionary ecology of oncogenesis
In a classic paper, George Williams (1957) argued that alleles promoting reproductive success early in life may be favoured by selection, even if they reduce the lifespan of individuals that bear the allele. A variety of evidence supports the theory that such 'antagonistic pleiotropy' is a major factor contributing to the evolution of senescence (Ljubuncic & Reznick 2009), but examples of specific alleles known to fulfil Williams' criteria remain rare, in both humans and other animals (e.g. Alexander et al. 2007; Kulminski et al. 2010). An intriguing example in this issue of Molecular Ecology (Fernandez & Bowser 2010) demonstrates that both natural and sexual selection may favour melanoma-promoting oncogene alleles in the fish genus Xiphophorus. DOI
90. Arbuthnott, D; Crespi, BJ. (2009) Courtship and mate discrimination within and between species of Timema walking-sticks.Animal Behaviour 78: 53-59 Courtship and mate discrimination within and between species of Timema walking-sticks
HOST-PLANT ADAPTATION; SEXUAL SELECTION; REPRODUCTIVE ISOLATION; MATING-BEHAVIOR; DROSOPHILA-MELANOGASTER; SYMPATRIC SPECIATION; PREMATING ISOLATION; VISUAL PREDATION; FIELD CRICKETS; FEMALE-CHOICE
The evolution of premating isolation via divergence in mating behaviour has been strongly implicated in the process of speciation. Timema walking-sticks show weak to moderate reproductive isolation between populations of the same species on different host plants, and high levels of isolation between species. In this paper we conducted experimental studies of within-species and between-species mating behaviour in Timema to address two central issues pertaining to the influence of behaviour on speciation: ( 1) how divergence in courtship influences reproductive isolation within and between species, and ( 2) whether the same or different traits mediate premating isolation within and between species. Mating behaviour involves three phases: pairing ( whereby the male climbs onto the female's dorsal surface), courtship ( which involves leg and antenna waving), and copulation. We found that courtship was qualitatively similar across the genus, but there were statistically significant quantitative differences in leg and antenna waving frequencies between Timema species. However, no-choice trials within and between species showed that discrimination within species is a function of whether males will court females after pairing, while discrimination between species is a function of whether males and females will pair. Because in both cases mate discrimination occurs before courtship is performed, we infer that courtship does not directly influence reproductive isolation in Timema. Moreover, because within-species and between-species discrimination take place at different stages in the mating sequence, intraspecific mate discrimination and species recognition appear to represent distinct processes. These findings suggest that, at least in Timema, speciation may involve the accumulation or replacement of mate discrimination mechanisms used within species. (C) 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. DOI
89.Crespi, B. (2009) Gender, biology, and mathematics performance.Proceedings of the National Academy of Sciences of the United States of America 106: E102-E102 Gender, biology, and mathematics performance
DOI
88.Crespi, B; Summers, K; Dorus, S. (2009) Genomic sister-disorders of neurodevelopment: an evolutionary approach.Evolutionary Applications 2: 81-100 Genomic sister-disorders of neurodevelopment: an evolutionary approach
SMITH-MAGENIS-SYNDROME; 22Q11.2 DELETION SYNDROME; WILLIAMS-BEUREN-SYNDROME; AUTISM-SPECTRUM DISORDERS; CARDIO-FACIAL SYNDROME; COPY-NUMBER VARIATION; POTOCKI-LUPSKI-SYNDROME; LINKED GENE-EXPRESSION; SYNDROME DEL 17P11.2; TURNER-SYNDROME
Genomic sister-disorders are defined here as diseases mediated by duplications versus deletions of the same region. Such disorders can provide unique information concerning the genomic underpinnings of human neurodevelopment because effects of diametric variation in gene copy number on cognitive and behavioral phenotypes can be inferred. We describe evidence from the literature on deletions versus duplications for the regions underlying the best-known human neurogenetic sister-disorders, including Williams syndrome, Velocardiofacial syndrome, and Smith-Magenis syndrome, as well as the X-chromosomal conditions Klinefelter and Turner syndromes. These data suggest that diametric copy-number alterations can, like diametric alterations to imprinted genes, generate contrasting phenotypes associated with autistic-spectrum and psychotic-spectrum conditions. Genomically based perturbations to the development of the human social brain are thus apparently mediated to a notable degree by effects of variation in gene copy number. We also conducted the first analyses of positive selection for genes in the regions affected by these disorders. We found evidence consistent with adaptive evolution of protein-coding genes, or selective sweeps, for three of the four sets of sister-syndromes analyzed. These studies of selection facilitate identification of candidate genes for the phenotypes observed and lend a novel evolutionary dimension to the analysis of human cognitive architecture and neurogenetic disorders. DOI
87.Crespi, B. J. (2009) Evolutionary genetics of affective disorders. In: Depression: Translational Approaches to Understanding and Treating, Edited by C. Pariante and R. Nesse. Oxford University Press. pp. 37-54. Evolutionary genetics of affective disorders.
85. Elliot, MG; Crespi, BJ. (2009) Phylogenetic Evidence for Early Hemochorial Placentation in Eutheria.Placenta 30: 949-967 Phylogenetic Evidence for Early Hemochorial Placentation in Eutheria
CAMEL CAMELUS-DROMEDARIUS; PACA AGOUTI-PACA; TADARIDA BRASILIENSIS CYNOCEPHALA; ELECTRON-MICROSCOPIC OBSERVATIONS; SCHREIBERSII-FULIGINOSUS HODGSON; MONKEY CERCOPITHECUS-AETHIOPS; ELEPHANT LOXODONTA-AFRICANA; EARLY EMBRYONIC-DEVELOPMENT; CHORIO-ALLANTOIC PLACENTA; CROCUTA-CROCUTA ERXLEBEN
The eutherian placenta is remarkable for its structural and functional variability. In order to construct and test comparative hypotheses relating ecological, behavioral and physiological traits to placental characteristics it is first necessary to reconstruct the historical course of placental evolution. Previous attempts to do so have yielded inconsistent results, particularly with respect to the early evolution of structural relationships between fetal and maternal circulatory systems. Here, we bring a battery of phylogenetic methods - including parsimony, likelihood and Bayesian approaches - to bear on the question of placental evolution. All of these approaches are consistent in indicating that highly invasive hemochorial placentation, as found in human beings and numerous other taxa, was an early evolutionary innovation present in the most ancient ancestors of the living placental mammals. (C) 2009 Elsevier Ltd. All rights reserved. DOI
84. Parent, CE; Crespi, BJ. (2009) Ecological Opportunity in Adaptive Radiation of Galapagos Endemic Land Snails.American Naturalist 174: 898-905 Ecological Opportunity in Adaptive Radiation of Galapagos Endemic Land Snails
THAIS-EMARGINATA PROSOBRANCHIA; SHELL-SHAPE VARIATION; CHARACTER DISPLACEMENT; INTERSPECIFIC COMPETITION; LITTORINA-SAXATILIS; NUCELLA-LAPILLUS; BEMBICIUM-VITTATUM; INTERTIDAL SNAIL; BONIN ISLANDS; SELECTION
The classic evolutionary hypothesis of ecological opportunity proposes that both heterogeneity of resources and freedom from enemies promote phenotypic divergence as a response to increased niche availability. Although phenotypic divergence and speciation have often been inferred to be the primary consequences of the release from competition or predation that accompanies a shift to a new adaptive zone, increased phenotypic variation within species is expected to represent the first stage resulting from such a shift. Using measures of intraspecific morphological variation of 30 species of Galapagos endemic land snails in a phylogenetically controlled framework, we show that the number of local congeners and the number of local plant species are associated with lower and higher intraspecific phenotypic variation, respectively. In this clade, ecological opportunity thus explicitly links the role of competition from congeners and the heterogeneity of resources to the extent of intraspecific phenotypic divergence as adaptive radiation proceeds. DOI
83. Schwander, T; Crespi, BJ. (2009) MULTIPLE DIRECT TRANSITIONS FROM SEXUAL REPRODUCTION TO APOMICTIC PARTHENOGENESIS IN TIMEMA STICK INSECTS.Evolution 63: 84-103 MULTIPLE DIRECT TRANSITIONS FROM SEXUAL REPRODUCTION TO APOMICTIC PARTHENOGENESIS IN TIMEMA STICK INSECTS
CRISTINAE WALKING-STICKS; DROSOPHILA-MERCATORUM; PHYLOGENETIC-RELATIONSHIPS; GEOGRAPHIC PARTHENOGENESIS; LEAF BEETLES; GENE FLOW; EVOLUTION; SELECTION; HYBRIDIZATION; ADAPTATION
Transitions from sexual reproduction to parthenogenesis may occur along multiple evolutionary pathways and involve various cytological mechanisms to produce diploid eggs. Here, we investigate routes to parthenogenesis in Timema stick insects, a genus comprising five obligate parthenogens. By combining information from microsatellites and karyotypes with a previously published mitochondrial phylogeny, we show that all five parthenogens likely evolved spontaneously from sexually reproducing species, and that the sexual ancestor of one of the five parthenogens was probably of hybrid origin. The complete maintenance of heterozygosity between generations in the five parthenogens strongly suggests that eggs are produced by apomixis. Virgin females of the sexual species were also able to produce parthenogenetic offspring, but these females produced eggs by automixis. High heterozygosity levels stemming from conserved ancestral alleles in the parthenogens suggest, however, that automixis has not generated the current parthenogenetic Timema lineages but that apomixis appeared abruptly in several sexual species. A direct transition from sexual reproduction to (at least functional) apomixis results in a relatively high level of allelic diversity and high efficiency for parthenogenesis. Because both of these traits should positively affect the demographic success of asexual lineages, spontaneous apomixis may have contributed to the origin and maintenance of asexuality in Timema. DOI
82. Schwander, T; Crespi, BJ. (2009) Twigs on the tree of life? Neutral and selective models for integrating macroevolutionary patterns with microevolutionary processes in the analysis of asexuality.Molecular Ecology 18: 28-42 Twigs on the tree of life? Neutral and selective models for integrating macroevolutionary patterns with microevolutionary processes in the analysis of asexuality
NEW-ZEALAND SNAIL; MITOCHONDRIAL-DNA SEQUENCES; EVOLUTIONARY DEAD-END; GEOGRAPHICAL PARTHENOGENESIS; PHYLOGENETIC-RELATIONSHIPS; DELETERIOUS MUTATIONS; BDELLOID ROTIFERS; POTAMOPYRGUS-ANTIPODARUM; MOLECULAR PHYLOGENETICS; ENDOSYMBIOTIC BACTERIA
Neutral models characterize evolutionary or ecological patterns expected in the absence of specific causal processes, such as natural selection or ecological interactions. In this study, we describe and evaluate three neutral models that can, in principle, help to explain the apparent 'twigginess' of asexual lineages on phylogenetic trees without involving the negative consequences predicted for the absence of recombination and genetic exchange between individuals. Previously, such phylogenetic twiggyness of asexual lineages has been uncritically interpreted as evidence that asexuality is associated with elevated extinction rates and thus represents an evolutionary dead end. Our first model uses simple phylogenetic simulations to illustrate that, with sexual reproduction as the ancestral state, low transition rates to stable asexuality, or low rates of ascertained 'speciation' in asexuals, can generate twiggy distributions of asexuality, in the absence of high extinction rates for asexual lineages. The second model, developed by Janko et al. (2008), shows that a dynamic equilibrium between origins and neutral losses of asexuals can, under some conditions, generate a relatively low mean age of asexual lineages. The third model posits that the risk of extinction for asexual lineages may be higher than that of sexuals simply because asexuals inhabit higher latitudes or altitudes, and not due to effects of their reproductive systems. Such neutral models are useful in that they allow quantitative evaluation of whether empirical data, such as phylogenetic and phylogeographic patterns of sex and asexuality, indeed support the idea that asexually reproducing lineages persist over shorter evolutionary periods than sexual lineages, due to such processes as mutation accumulation, slower rates of adaptive evolution, or relatively lower levels of genetic variability. DOI
80. Bono, JM; Crespi, BJ. (2008) Cofoundress relatedness and group productivity in colonies of social Dunatothrips (Insecta : Thysanoptera) on Australian Acacia.Behavioral Ecology and Sociobiology 62: 1489-1498 Cofoundress relatedness and group productivity in colonies of social Dunatothrips (Insecta : Thysanoptera) on Australian Acacia
pleometrosis; evolution of cooperation; sex ratio; social evolution; life history
Facultative joint colony founding by social insects provides opportunities to analyze the roles of genetic and ecological factors in the evolution of cooperation. Although cooperative nesting is observed in range of social insect taxa, the most detailed studies of this behavior have been conducted with Hymenoptera (ants, bees, and wasps). Here, we show that foundress associations in the haplodiploid social thrips Dunatothrips aneurae (Insecta: Thysanoptera) are most often comprised of close relatives (sisters), though groups with unrelated foundresses are also found. Associations among relatives appear to be facilitated by limited female dispersal, which results in viscous population structure. In addition, we found that per capita productivity declined with increasing group size, sex ratios were female-biased, and some female offspring apparently remained in their natal domicile for some time following eclosion. D. aneurae thus exhibits a suite of similarities with eusocial Hymenoptera, providing evidence for the convergent evolution of associated social and life-history traits in Hymenoptera and Thysanoptera. DOI
78.Crespi, B. (2008) Genomic imprinting in the development and evolution of psychotic spectrum conditions.Biological Reviews 83: 441-493 Genomic imprinting in the development and evolution of psychotic spectrum conditions
schizophrenia; psychosis; autism; genomic imprinting; evolution; genomic conflict PRADER-WILLI-SYNDROME; BIPOLAR AFFECTIVE-DISORDER; PARENT-OF-ORIGIN; MATERNAL UNIPARENTAL DISOMY; FAMILY-BASED ASSOCIATION; SMITH-MAGENIS-SYNDROME; ATTENTION-DEFICIT/HYPERACTIVITY DISORDER; LINKED MENTAL-RETARDATION; GENOMEWIDE LINKAGE SCAN; FACTOR BDNF GENE
I review and evaluate genetic and genomic evidence salient to the hypothesis that the development and evolution of psychotic spectrum conditions have been mediated in part by alterations of imprinted genes expressed in the brain. Evidence from the genetics and genomics of schizophrenia, bipolar disorder, major depression, Prader-Willi syndrome, Klinefelter syndrome, and other neurogenetic conditions support the hypothesis that the etiologies of psychotic spectrum conditions commonly involve genetic and epigenetic imbalances in the effects of imprinted genes, with a bias towards increased relative effects from imprinted genes with maternal expression or other genes favouring maternal interests. By contrast, autistic spectrum conditions, including Kanner autism, Asperger syndrome, Rett syndrome, Turner syndrome, Angelman syndrome, and Beckwith-Wiedemann syndrome, commonly engender increased relative effects from paternally expressed imprinted genes, or reduced effects from genes favouring maternal interests. Imprinted-gene effects on the etiologies of autistic and psychotic spectrum conditions parallel the diametric effects of imprinted genes in placental and foetal development, in that psychotic spectrum conditions tend to be associated with undergrowth and relatively-slow brain development, whereas some autistic spectrum conditions involve brain and body overgrowth, especially in foetal development and early childhood. An important role for imprinted genes in the etiologies of psychotic and autistic spectrum conditions is consistent with neurodevelopmental models of these disorders, and with predictions from the conflict theory of genomic imprinting. DOI
77.Crespi, B. (2008) Turner syndrome and the evolution of human sexual dimorphism.Evolutionary Applications 1: 449-461 Turner syndrome and the evolution of human sexual dimorphism
MAGNETIC-RESONANCE-SPECTROSCOPY; WILLIAMS-BEUREN-SYNDROME; LINKED GENE-EXPRESSION; X-CHROMOSOME; GROWTH-HORMONE; KLINEFELTER-SYNDROME; PARENTAL ORIGIN; COGNITIVE FUNCTION; HEARING-LOSS; CLINICAL PHENOTYPE
Turner syndrome is caused by loss of all or part of an X chromosome in females. A series of recent studies has characterized phenotypic differences between Turner females retaining the intact maternally inherited versus paternally inherited X chromosome, which have been interpreted as evidence for effects of X-linked imprinted genes. In this study I demonstrate that the differences between Turner females with a maternal X and a paternal X broadly parallel the differences between males and normal females for a large suite of traits, including lipid profile and visceral fat, response to growth hormone, sensorineural hearing loss, congenital heart and kidney malformations, neuroanatomy (sizes of the cerebellum, hippocampus, caudate nuclei and superior temporal gyrus), and aspects of cognition. This pattern indicates that diverse aspects of human sex differences are mediated in part by X-linked genes, via genomic imprinting of such genes, higher rates of mosaicism in Turner females with an intact X chromosome of paternal origin, karyotypic differences between Turner females with a maternal versus paternal X chromosome, or some combination of these phenomena. Determining the relative contributions of genomic imprinting, karyotype and mosaicism to variation in Turner syndrome phenotypes has important implications for both clinical treatment of individuals with this syndrome, and hypotheses for the evolution and development of human sexual dimorphism. DOI
76.Crespi, B; Badcock, C. (2008) Psychosis and autism as diametrical disorders of the social brain.Behavioral and Brain Sciences 31: 241-+ Psychosis and autism as diametrical disorders of the social brain
autism; cognition; genomic conflict; genomic imprinting; hyper-mentalism; psychosis; schizophrenia PRADER-WILLI-SYNDROME; HIGH-FUNCTIONING AUTISM; WHITE-MATTER VOLUME; EARLY-ONSET SCHIZOPHRENIA; MIRROR NEURON SYSTEM; PERVASIVE DEVELOPMENTAL DISORDER; SCHIZOTYPAL PERSONALITY-DISORDER; OBSESSIVE-COMPULSIVE SYMPTOMS; LANGUAGE-ASSOCIATION CORTEX; SUPERIOR TEMPORAL GYRUS
Autistic-spectrum conditions and psychotic-spectrum conditions (mainly schizophrenia, bipolar disorder, and major depression) represent two major suites of disorders of human cognition, affect, and behavior that involve altered development and function of the social brain. We describe evidence that a large set of phenotypic traits exhibit diametrically opposite phenotypes in autistic-spectrum versus psychotic-spectrum conditions, with a focus on schizophrenia. This suite of traits is inter-correlated, in that autism involves a general pattern of constrained overgrowth, whereas schizophrenia involves undergrowth. These disorders also exhibit diametric patterns for traits related to social brain development, including aspects of gaze, agency, social cognition, local versus global processing, language, and behavior. Social cognition is thus underdeveloped in autistic-spectrum conditions and hyper-developed on the psychotic spectrum. We propose and evaluate a novel hypothesis that may help to explain these diametric phenotypes: that the development of these two sets of conditions is mediated in part by alterations of genomic imprinting. Evidence regarding the genetic, physiological, neurological, and psychological underpinnings of psychotic-spectrum conditions supports the hypothesis that the etiologies of these conditions involve biases towards increased relative effects from imprinted genes with maternal expression, which engender a general pattern of undergrowth. By contrast, autistic-spectrum conditions appear to involve increased relative bias towards effects of paternally expressed genes, which mediate overgrowth. This hypothesis provides a simple yet comprehensive theory, grounded in evolutionary biology and genetics, for understanding the causes and phenotypes of autistic-spectrum and psychotic-spectrum conditions. DOI
75.Crespi, B; Badcock, C. (2008) The evolutionary social brain: From genes to psychiatric conditions.Behavioral and Brain Sciences 31: 284-320 The evolutionary social brain: From genes to psychiatric conditions
SMITH-MAGENIS-SYNDROME; PRADER-WILLI-SYNDROME; FRAGILE-X-SYNDROME; CHILDHOOD-ONSET SCHIZOPHRENIA; BIPOLAR AFFECTIVE-DISORDER; AUTISM SPECTRUM DISORDERS; HEAD CIRCUMFERENCE GROWTH; HIGH-FUNCTIONING AUTISM; SYNDROME DEL 17P11.2; TURNER-SYNDROME
The commentaries on our target article, "Psychosis and Autism as Diametrical Disorders of the Social Brain," reflect the multidisciplinary yet highly fragmented state of current studies of human social cognition. Progress in our understanding of the human social brain must come from studies that integrate across diverse analytic levels, using conceptual frameworks grounded in evolutionary biology. DOI
72. Elliot, MG; Crespi, BJ. (2008) Placental invasiveness and brain-body allometry in eutherian mammals.Journal of Evolutionary Biology 21: 1763-1778 Placental invasiveness and brain-body allometry in eutherian mammals
brain size; encephalization; Eutheria; evolution; fatty acids; fetal nutrition; life history; placentation; pregnancy FREE FATTY-ACIDS; EXPENSIVE-TISSUE HYPOTHESIS; MATERNO-FETAL EXCHANGES; NEOCORTEX SIZE; BEHAVIORAL ECOLOGY; RABBIT PLACENTA; LATE-GESTATION; GUINEA-PIG; LINOLEIC ACIDS; SOCIAL BRAIN
Brain growth is a key trait in the evolution of mammalian life history. Brain development should be mediated by placentation, which determines patterns of resource transfer from mothers to fetal offspring. Eutherian placentation varies in the extent to which a maternal barrier separates fetal tissues from maternal blood. We demonstrate here that more invasive forms of placentation are associated with substantially steeper brain-body allometry, faster prenatal brain growth and slower prenatal body growth. On the basis of the physiological literature we suggest a simple mechanism for these differences: in species with invasive placentation, where the placenta is bathed directly in maternal blood, fatty acids essential for brain development can be readily extracted by the fetus, but in species with less invasive placentation they must be synthesized by the fetus. Hence, with regard to brain-body allometry and prenatal growth patterns, eutherian mammals are structured into distinct groups differing in placental invasiveness. DOI
71. Parent, CE; Wu, SST; Keays, A; Crespi, BJ. (2008) Characterization of eight microsatellite loci in the Galapagos endemic land snail Bulimulus reibischi, and their cross-species amplification.Molecular Ecology Resources 8: 1091-1094 Characterization of eight microsatellite loci in the Galapagos endemic land snail Bulimulus reibischi, and their cross-species amplification
Bulimulidae; DNA markers; Galapagos; heterozygosity; microsatellites; Mollusca
Variation in and amplification conditions for eight polymorphic microsatellite loci initially identified from Bulimulus akamatus, a pulmonate land snail from Galapagos, are described. Intraspecific polymorphism and heterozygosity of the eight markers were studied in 19 populations of Bulinulus reibischi, a closely related species of B. akamatus. Furthermore, the eight loci were also cross-amplified in six other closely related bulimulid species. The number of alleles across populations of B. reibischi at six loci is moderate (three to 10), but considerable for two other loci (19 and 20). There is no strong evidence for linkage among any of the loci examined. DOI
70. Sandoval, CP; Crespi, BJ. (2008) Adaptive evolution of cryptic coloration: the shape of host plants and dorsal stripes in Timema walking-sticks.Biological Journal of the Linnean Society 94: 1-5 Adaptive evolution of cryptic coloration: the shape of host plants and dorsal stripes in Timema walking-sticks
crypsis; host specialization; phylogeny; timematidae
The adaptive significance of cryptic colour patterns has seldom been analysed in a phylogenetic context. We mapped data on the presence vs. absence of dorsal stripes, and the use of needle-like vs. broad foliage, onto a recent phylogeny of Timema walking-sticks, in order to infer the evolutionary history of these traits and test the hypothesis that the dorsal stripe is an adaptation for crypsis on needle-like leaves. By maximum parsimony optimization, the dorsal stripe has evolved five or six times in this clade, each time in association with the use of vegetation with needle-like leaves. Maddison's concentrated changes test showed that this association between morphology and habitat was statistically significant. By contrast, results based on Pagel's maximum likelihood analyses did not reach significance, probably because the large number of origins of dorsal stripe introduces statistical uncertainty. These results suggest that the adaptations for crypsis can arise readily and in parallel, in the appropriate selective environment. However, they may also constrain the evolution of host-plant use, as there is no unambiguous case of Timema species with dorsal stripes shifting to broad-leaved plants. (C) 2008 The Linnean Society of London.
69. Summers, K; Crespi, B. (2008) Molecular evolution of the prostate cancer susceptibility locus RNASEL: Evidence for positive selection.Infection Genetics and Evolution 8: 297-301 Molecular evolution of the prostate cancer susceptibility locus RNASEL: Evidence for positive selection
XMRV; prostate cancer; virus; RNASEL; coevolution; positive selection
Recent research implicates viral infection as a factor that may contribute to the risk of prostate cancer. Allelic variation at the RNASEL locus is associated with the risk of infection by a newly discovered retrovirus called XMRV, and with hereditary risk of prostate cancer. This evidence suggests that the RNASEL locus has undergone antagonistic coevolution with the retrovirus over evolutionary time. If this is the case, then both the RNASEL locus and the retrovirus should show evidence of positive selection. Here we use molecular-evolutionary methods to investigate the prediction that the RNASEL locus will exhibit evidence of positive selection. We find evidence that positive selection has acted on this locus over evolutionary time. We further find, using a Bayesian estimation procedure, that Asp541Glu, which was found to be associated with prostate cancer risk in Caucasians in a recent meta-analysis, shows an elevated probability of positive selection. Previous studies provide evidence for rapid evolution of the infection-mediating gag gene in the XMRV retrovirus. Taken together, these results suggest that antagonistic coevolution may have occurred between a specific host locus involved in immune defense (RNASEL) and a viral pathogen. In turn, genetic variation associated with this apparent coevolution may influence susceptibility to prostate cancer. (c) 2008 Elsevier B.V. All rights reserved. DOI
68. Summers, K; Crespi, B. (2008) The androgen receptor and prostate cancer: A role for sexual selection and sexual conflict?Medical Hypotheses 70: 435-443 The androgen receptor and prostate cancer: A role for sexual selection and sexual conflict?
We propose and evaluate the hypothesis that the CAG repeat region of the androgen receptor represents a locus of antagonistic pleiotropy in the context of sexual selection and sexual conflict. Short repeats are associated with increased transactivation of the androgen receptor at the molecular level, and increased fertility at the phenotypic level. However, short repeats are also associated with increased risk of prostate cancer, and with more aggressive forms of the disease. The somatic evolution of cancer cell lineages also shows a repeated pattern of shortening of the CAG repeat in association with cancer progression, apparently as a result of positive selection among cell lineages. We further postulate that other genes associated with prostate cancer are likely to mediate antagonistic pleiotropy in the context of sexual selection and sexual conflict. A key prediction of this hypothesis is that the genes mediating antagonistic pleiotropy will show historical evidence of positive selection, particularly in the context of sexual conflict. Previous research on the molecular evolution of specific genes associated with prostate cancer supports this prediction, and we suggest further critical tests of the role for genomic conflicts and tradeoffs in the evolution of cancer risk. (c) 2007 Elsevier Ltd. All rights reserved. DOI
66.Crespi, B.J., K. Summers and S. Dorus. (2007) Adaptive evolution of genes underlying schizophrenia.Proceedings of the Royal Society B-Biological Sciences 274:2801-2810. Adaptive evolution of genes underlying schizophrenia.
64. Joy, JB; Crespi, BJ. (2007) Adaptive radiation of gall-inducing insects within a single host-plant species.Evolution 61: 784-795 Adaptive radiation of gall-inducing insects within a single host-plant species
adaptive radiation; Asphondylia; ecological shifts; galling; insect-plant interactions; plant-part specific specialization; speciation
Speciation of plant-feeding insects is typically associated with host-plant shifts, with subsequent divergent selection and adaptation to the ecological conditions associated with the new plant. However, a few insect groups have apparently undergone speciation while remaining on the same host-plant species, and such radiations may provide novel insights into the causes of adaptive radiation. We used mitochondrial and nuclear DNA to infer a phylogeny for 14 species of gall-inducing Asphondylia flies (Diptera: Cecidomyiidae) found on Larrea tridentata (creosote bush), which have been considered to be monophyletic based on morphological evidence. Our phylogenetic analyses provide strong support for extensive within-host plant speciation in this group, and it demonstrates that diversification has involved numerous shifts between different plant organs (leaves, buds, flowers, and stems) of the same host-plant species. Within-plant speciation of Asphondylia is thus apparently facilitated by the opportunity to partition the plant ecologically. One clade exhibits temporal isolation among species, which may have facilitated divergence via allochronic shifts. Using a novel method based on Bayesian reconstruction, we show that the rate of change in an ecomorphological trait, ovipositor length, was significantly higher along branches with inferred shifts between host-plant organs than along branches without such shifts. This finding suggests that Larrea gall midges exhibit close morphological adaptation to specific host-plant parts, which may mediate ecological transitions via disruptive selection.PDF DOI
63. McLeish, MJ; Crespi, BJ; Chapman, TW; Schwarz, MP. (2007) Parallel diversification of Australian gall-thrips on Acacia.Molecular Phylogenetics and Evolution 43: 714-725 Parallel diversification of Australian gall-thrips on Acacia
parallel divergence; cospeciation; host-switch; phylogenetics; gall-thrips; Acacia
The diversification of gall-inducing Australian Kladothrips (Insecta: Thysanoptera) on Acacia has produced a pair of sister-clades, each of which includes a suite of lineages that utilize virtually the same set of 15 closely related host plant species. This pattern of parallel insect-host plant radiation may be driven by cospeciation, host-shifting to the same set of host plants, or some combination of these processes. We used molecular-phylogenetic data on the two gall-thrips clades to analyze the degree of concordance between their phylogenies, which is indicative of parallel divergence. Analyses of phylogenetic concordance indicate statistically- significant similarity between the two clades. Their topologies also fit with a hypothesis of some degree of host-plant tracking. Based on phylogenetic and taxonomic information regarding the phylogeny of the Acacia host plants in each clade, one or more species has apparently shifted to more-divergent Acacia host-plant species, and in each case these shifts have resulted in notable divergence in aspects of the phenotype including morphology, life history and behaviour. Our analyses indicate that gall-thrips on Australian Acacia have undergone parallel diversification as a result of some combination of cospeciation, highly restricted host-plant shifting, or both processes, but that the evolution of novel phenotypic diversity in this group is a function of relatively few shifts to divergent host plants. This combination of ecologically restricted and divergent radiation may represent a microcosm for the macroevolution of host plant relationships and phenotypic diversity among other phytophagous insects. (c) 2007 Elsevier Inc. All rights reserved. DOI
62. Nosil, P; Crespi, BJ; Gries, R; Gries, G. (2007) Natural selection and divergence in mate preference during speciation.Genetica 129: 309-327 Natural selection and divergence in mate preference during speciation
speciation; hybrid fitness; mate choice; reproductive isolation; pheromones
Sexual isolation can evolve due to natural selection against hybrids (reinforcement). However, many different forms of hybrid dysfunction, and selective processes that do not involve hybrids, can contribute to the evolution of sexual isolation. Here we review how different selective processes affect the evolution of sexual isolation, describe approaches for distinguishing among them, and assess how they contribute to variation in sexual isolation among populations of Timema cristinae stick-insects. Pairs of allopatric populations of T. cristinae living on different host-plant species exhibit greater sexual isolation than those on the same host, indicating that some sexual isolation has evolved due to host adaptation. Sexual isolation is strongest in regions where populations on different hosts are in geographic contact, a pattern of reproductive character displacement that is indicative of reinforcement. Ecological costs to hybridization do occur but traits under ecological selection (predation) do not co-vary strongly with the probability of between-population mating such that selection on ecological traits is not predicted to produce a strong correlated evolutionary response in mate preference. Moreover, F1 hybrid egg inviability is lacking and the factors contributing to reproductive character displacement require further study. Finally, we show that sexual isolation involves, at least in part, olfactory communication. Our results illustrate how understanding of the evolution of sexual isolation can be enhanced by isolating the roles of diverse ecological and evolutionary processes. DOI
61. Springer, SA; Crespi, BJ. (2007) Adaptive gamete-recognition divergence in a hybridizing Mytilus population.Evolution 61: 772-783 Adaptive gamete-recognition divergence in a hybridizing Mytilus population
adaptive evolution; gamete-recognition; hybridization; Mytilus; prezygotic isolation; reinforcement; sexual conflict
Gamete-recognition proteins often evolve rapidly, but it is not known if their divergence occurs within species and corresponds with the evolution of reproductive isolation, or if divergence typically accumulates between already isolated lineages. We examined the evolution of a candidate gamete-recognition protein in several sympatric and allopatric populations of Mytilus blue mussels, species that hybridize in nature. Within a single species, Mytilus galloprovincialis, we found adaptive divergence of Lysin-M7, a sperm acrosomal protein that dissolves the egg vitelline envelope during fertilization. Mytilus galloprovincialis Lysin-M7 alleles group into two distinct clades (termed G and G(D)) and individual alleles in these clades are separated from each other by at least three and up to eleven amino-acid substitutions. Maximum-likelihood estimates of selective pressure (dN/dS = omega) implicate selection in the divergence between M. galloprovincialis Lysin-M7 clades, and within the G(D) clade. Exact tests of population differentiation indicate that the relative frequency of G and G(D) Lysin-M7 alleles differs significantly among M. galloprovincialis populations. Compared with allopatric Mediterranean samples, Lysin-M7 alleles in the G(D) clade are found at elevated frequency in samples from the East Atlantic and California, areas of secondary contact and hybridization between Mytilus species, and Australia, an area of unknown species composition. Adaptive divergence between the alleles most common in allopatry and those found at elevated frequency in samples from sympatry suggests that selection pressures acting in hybridizing populations, likely following Pleistocene secondary contact with M. edulis in the East Atlantic, drove the divergence of Lysin-M7 in M. galloprovincialis. DOI
60. Thompson, GJ; Lenz, M; Crozier, RH; Crespi, BJ. (2007) Molecular-genetic analyses of dispersal and breeding behaviour in the Australian termite Coptotermes lacteus: evidence for non-random mating in a swarm-dispersal mating system.Australian Journal of Zoology 55: 219-227 Molecular-genetic analyses of dispersal and breeding behaviour in the Australian termite Coptotermes lacteus: evidence for non-random mating in a swarm-dispersal mating system
isoptera; microsatellites; population genetics; social insects
We used microsatellite DNA markers to infer the dispersal and breeding behaviour of Coptotermes lacteus, a termite whose large mounds are a conspicuous feature of Australia's central east coast. We genotyped a subsample of neuter offspring for each of 38 colonies sampled over two spatially separated populations, one in a natural forest and the other in an exotic radiata pine plantation. All colonies showed offspring genotype frequencies consistent with a single reproductive pair. This result confirms that stable monogamy is the normal breeding arrangement for this species and that multi-reproductive colonies are rare. The two study populations were significantly differentiated and the distance separating them (similar to 150 km) is therefore an effective constraint on gene flow. The populations themselves, however, were not noticeably subdivided above the level of colony. This lack of within-population viscosity is unexpected for weakly dispersing species and suggests that local gamete dispersal is in fact quite effective in C. lacteus. Nonetheless, dispersing sexuals do not appear to mate randomly. Instead, all four microsatellite loci are deficient in heterozygotes, indicating that populations are substantially inbred, irrespective of habitat. Evidence from hierarchical F-statistics, spatial genetic autocorrelation and relatedness calculations suggests that deviations from Hardy-Weinberg equilibrium may result from either a preference for non-sibling relatives over totally unrelated mates, or from random mating with viscosity-though evidence for the latter hypothesis was not detected. These findings suggest that swarm-dispersal mating systems, usually considered to produce outbreeding and panmixia, can instead involve a notable degree of non-random mating. DOI
59. Badcock, C; Crespi, B. (2006) Imbalanced genomic imprinting in brain development: an evolutionary basis for the aetiology of autism.J Evolution Biol 19: 1007-1032 Imbalanced genomic imprinting in brain development: an evolutionary basis for the aetiology of autism
autism; evolution; genomic imprinting; social behaviour
We describe a new hypothesis for the development of autism, that it is driven by imbalances in brain development involving enhanced effects of paternally expressed imprinted genes, deficits of effects from maternally expressed genes, or both. This hypothesis is supported by: (1) the strong genomic-imprinting component to the genetic and developmental mechanisms of autism, Angelman syndrome, Rett syndrome and Turner syndrome; (2) the core behavioural features of autism, such as self-focused behaviour, altered social interactions and language, and enhanced spatial and mechanistic cognition and abilities, and (3) the degree to which relevant brain functions and structures are altered in autism and related disorders. The imprinted brain theory of autism has important implications for understanding the genetic, epigenetic, neurological and cognitive bases of autism, as ultimately due to imbalances in the outcomes of intragenomic conflict between effects of maternally vs. paternally expressed genes.
55.Crespi, BJ; Summers, K. (2006) Positive selection in the evolution of cancer.Biol Rev 81: 407-424 Positive selection in the evolution of cancer
positive selection; antagonistic coevolution; oncogenes; tumour suppressors; molecular evolution
We hypothesize that forms of antagonistic coevolution have forged strong links between positive select' n at the molecular level and increased cancer risk. By this hypothesis, evolutionary conflict between males and females, mothers and foetuses, hosts and parasites, and other parties with divergent fitness interests has led to rapid evolution of genetic systems involved in control over fertilization and cellular resources. The genes involved in such systems promote cancer risk as a secondary effect of their roles in antagonistic coevolution, which generates evolutionary, disequflibrium and malaclaptation. Evidence from two sources: (1) studies on specific genes, including SPAXV cancer/ testis antigen genes, several Y-linked genes, thepem homebox gene, centromeric histone genes, die breast cancer gene BRCA1, the angiogenesis gene AXG, cadherin genes, cytochrome P450 genes, and viral oncogenes; and (2) large-scale database studies of selection on different functional categories of genes, supports our hypothesis. These results have important implications for understanding the evolutionary underpinnings of cancer and the dynamics of antagonistically-coevolving molecular systems.
54. Elliot, MG; Crespi, BJ. (2006) Placental invasiveness mediates the evolution of hybrid inviability in mammals.American Naturalist 168: 114-120 Placental invasiveness mediates the evolution of hybrid inviability in mammals
reproductive isolation; mammals; placentation; hybrid inviability; immunology
A central question in evolutionary biology is why animal lineages differ strikingly in rates and patterns of the evolution of reproductive isolation. Here, we show that the maximum genetic distance at which interspecific mammalian pregnancies yield viable neonates is significantly greater in clades with invasive (hemochorial) placentation than in clades with noninvasive (epitheliochorial or endotheliochorial) placentation. Moreover, sister species with invasive placentation exhibit higher allopatry in their geographic ranges, suggesting that formerly separated populations in mammals with this placental type fuse more readily on recontact. These differences are apparently driven by the stronger downregulation of maternal immune responses under invasive placentation, where fetal antigens directly contact the maternal bloodstream. Our results suggest that placental invasiveness mediates a major component of reproductive isolation in mammals.
53. McLeish, MJ; Chapman, TW; Crespi, BJ. (2006) Inbreeding ancestors: The role of sibmating in the social evolution of gall thrips.J Hered 97: 31-38 Inbreeding ancestors: The role of sibmating in the social evolution of gall thrips
We used microsatellite data to estimate levels of inbreeding in four species of solitary gall thrips that are in the same clade as the six species with soldier castes. Three of the four species were highly inbred (F-is 0.54 - 0.68), and the other apparently mated randomly ( Fis near zero). These estimates, combined with previous data from species with soldiers, suggest that inbreeding is a pervasive life-history feature of the gall-inducing thrips on Australian Acacia. Mapping of inbreeding estimates onto the phylogeny of the gall inducers showed that the ancestral lineage that gave rise to soldiers was apparently highly inbred, and therefore, inbreeding could have played a role in the origin of sociality within this group. Moreover, there was a trend from high levels of inbreeding at the origin of soldiers to low levels in the most derived species with soldiers, which exhibits the highest levels of reproductive division of labor and soldier altruism. These patterns are consistent with considerations from population genetics, which show that the likelihood of the origin of soldier altruism is higher in inbreeding populations but that, once soldiers have evolved, a reduction in inbreeding levels may facilitate the evolution of enhanced division of labor and reproductive skew.
52. Nosil, P; Crespi, BJ. (2006) Ecological divergence promotes the evolution of cryptic reproductive isolation.Proc R Soc B 273: 991-997 Ecological divergence promotes the evolution of cryptic reproductive isolation
speciation; mating success; natural selection; sexual selection; walking sticks
Speciation can involve the evolution of 'cryptic' reproductive isolation that occurs after copulation but before hybrid offspring are produced. Because such cryptic barriers to gene exchange involve post-mating sexual interactions, analyses of their evolution have focused on sexual conflict or traditional sexual selection. Here, we show that ecological divergence between populations of herbivorous walking sticks is integral to the evolution of cryptic reproductive isolation. Low female fitness following between-population mating can reduce gene exchange between populations, thus acting as a form of cryptic isolation. Female walking sticks show reduced oviposition rate and lower lifetime fecundity following between-population versus within-population mating, but only for mating between populations using different host-plant species. Our results indicate that even inherently sexual forms of reproductive isolation can evolve as a by-product of ecological divergence and that post-mating sexual interactions do not necessarily evolve independently of the ecological environment.
51. Nosil, P; Crespi, BJ. (2006) Experimental evidence that predation promotes divergence in adaptive radiation.Proc Nat Acad Sci Usa 103: 9090-9095 Experimental evidence that predation promotes divergence in adaptive radiation
crypsis; natural selection; Timema walking stick; divergent selection; host adaptation
Adaptive radiation is the evolution of ecological and phenotypic diversity within a rapidly multiplying lineage. Recent studies have identified general patterns in adaptive radiation and inferred that resource competition is a primary factor driving phenotypic divergence. The role and importance of other processes, such as predation, remains controversial. Here we use Timema stick insects to show that adaptive radiation can be driven by divergent selection from visual predators. Ecotypes using different host-plant species satisfy criteria for the early stages of adaptive radiation and differ in quantitative aspects of color, color pattern, body size, and body shape. A manipulative field experiment demonstrates that the direction and strength of divergent selection on these traits is strongly positively correlated with the direction and magnitude of their population divergence in nature but only when selection is estimated in the presence of predation. Our results indicate that both competition and predation may commonly serve as mechanisms of adaptive radiation.
50. Nosil, P; Crespi, BJ; Sandoval, CP; Kirkpatrick, M. (2006) Migration and the genetic covariance between habitat preference and performance.American Naturalist 167: E66-E78 Migration and the genetic covariance between habitat preference and performance
phytophagous insects; quantitative genetics; host preference; crypsis; population genetics
Studies of the genetic covariance between habitat preference and performance have reported conflicting outcomes ranging from no covariance to strong covariance. The causes of this variability remain unclear. Here we show that variation in the magnitude of genetic covariance can result from variability in migration regimes. Using data from walking stick insects and a mathematical model, we find that genetic covariance within populations between host plant preference and a trait affecting performance on different hosts ( cryptic color pattern) varies in magnitude predictably among populations according to migration regimes. Specifically, genetic covariance within populations is high in heterogeneous habitats where migration between populations locally adapted to different host plants generates nonrandom associations ( i. e., linkage disequilibrium) between alleles at color pattern and host preference loci. Conversely, genetic covariance is low in homogeneous habitats where a single host exists and migration between hosts does not occur. Our results show that habitat structure and patterns of migration can strongly affect the evolution and variability of genetic covariance within populations.
49. Nosil, P; Sandoval, CP; Crespi, BJ. (2006) The evolution of host preference in allopatric vs. parapatric populations of Timema cristinae walking-sticks.J Evolution Biol 19: 929-942 The evolution of host preference in allopatric vs. parapatric populations of Timema cristinae walking-sticks
assortative mating; crypsis; ecological speciation; host preference; reproductive isolation
Divergent habitat preferences can contribute to speciation, as has been observed for host-plant preferences in phytophagous insects. Geographic variation in host preference can provide insight into the causes of preference evolution. For example, selection against maladaptive host-switching occurs only when multiple hosts are available in the local environment and can result in greater divergence in regions with multiple vs. a single host. Conversely, costs of finding a suitable host can select for preference even in populations using a single host. Some populations of Timema cristinae occur in regions with only one host-plant species present (in allopatry, surrounded by unsuitable hosts) whereas others occur in regions with two host-plant species adjacent to one another (in parapatry). Here, we use host choice and reciprocal-rearing experiments to document genetic divergence in host preference among 33 populations of T. cristinae. Populations feeding on Ceanothus exhibited a stronger preference for Ceanothus than did populations feeding on Adenostoma. Both allopatric and parapatric pairs of populations using the different hosts exhibited divergent host preferences, but the degree of divergence tended to be greater between allopatric pairs. Thus, gene flow between parapatric populations apparently constrains divergence. Host preferences led to levels of premating isolation between populations using alternate hosts that were comparable in magnitude to previously documented premating isolation caused by natural and sexual selection against migrants between hosts. Our findings demonstrate how gene flow and different forms of selection interact to determine the magnitude of reproductive isolation observed in nature.
48. Parent, CE; Crespi, BJ. (2006) Sequential colonization and diversification of Galapagos endemic land snail genus Bulimulus (Gastropoda, Stylommatophora).Evolution 60: 2311-2328 Sequential colonization and diversification of Galapagos endemic land snail genus Bulimulus (Gastropoda, Stylommatophora)
adaptive radiation; colonization; Galapagos; land snails; speciation; species richness
Species richness on island or islandlike systems is a function of colonization, within-island speciation, and extinction. Here we evaluate the relative importance of the first two of these processes as a function of the biogeographical and ecological attributes of islands using the Galapagos endemic land snails of the genus Bulimulus, the most species-rich radiation of these islands. Species in this clade have colonized almost all major islands and are found in five of the six described vegetation zones. We use molecular phylogenetics (based on COI and ITS1 sequence data) to infer the diversification patterns of extant species of Bulimulus, and multiple regression to investigate the causes of variation among islands in species richness. Maximum-likelihood, Bayesian, and maximum-parsimony analyses yield well-resolved trees with similar topologies. The phylogeny obtained supports the progression rule hypothesis, with species found on older emerged islands connecting at deeper nodes. For all but two island species assemblages we find support for only one or two colonization events, indicating that within-island speciation has an important role in the formation of species on these islands. Even though speciation through colonization is not common, island insularity (distance to nearest major island) is a significant predictor of species richness resulting from interisland colonization alone. However, island insularity has no effect on the overall bulimulid species richness per island. Habitat diversity (measured as plant species diversity), island elevation, and island area, all of which are indirect measures of niche space, are strong predictors of overall bulimulid land snail species richness. Island age is also an important independent predictor of overall species richness, with older islands harboring more species than younger islands. Taken together, our results demonstrate that the diversification of Galapagos bulimulid land snails has been driven by a combination of geographic factors (island age, size, and location), which affect colonization patterns, and ecological factors, such as plant species diversity, that foster within-island speciation.
47.Crespi, B; Summers, K. (2005) Evolutionary biology of cancer.Trends in Ecology & Evolution 20: 545-552 Evolutionary biology of cancer
Cancer is driven by the somatic evolution of cell lineages that have escaped controls on replication and by the population-level evolution of genes that influence cancer risk. We describe here how recent evolutionary ecological studies have elucidated the roles of predation by the immune system and competition among normal and cancerous cells in the somatic evolution of cancer. Recent analyses of the evolution of cancer at the population level show how rapid changes in human environments have augmented cancer risk, how strong selection has frequently led to increased cancer risk as a byproduct, and how anticancer selection has led to tumor-suppression systems, tissue designs that slow somatic evolution, constraints on morphological evolution and even senescence itself. We discuss how applications of the tools of ecology and evolutionary biology are poised to revolutionize our understanding and treatment of this disease.
45. Summers, K; Crespi, B. (2005) Cadherins in maternal-foetal interactions: red queen with a green beard?Proceedings of the Royal Society B-Biological Sciences 272: 643-649 Cadherins in maternal-foetal interactions: red queen with a green beard?
cadherin; selection; placenta; green-beard
Cadherins are homophilic cell surface adhesion proteins, some of which mediate interactions between maternal and foetal tissues during mammalian pregnancy. David Haig suggested that these proteins may exhibit 'green-beard gene' effects, whereby the nature of binding between identical alleles in mother and foetus leads to differential levels of resource transfer. The selfish effects of such self-recognizing alleles should, however, be suppressed over evolutionary time by unlinked genes, which is expected to lead to antagonistic coevolution between placentally expressed cadherins and unlinked modifiers. Such molecular coevolution should leave a signature of positive selection, with high ratios of non-synonymous to synonymous amino acid substitution. We present evidence that three placentally expressed cadherin genes, E-cadherin, P-cadherin and VE-cadherin, have been subject to positive selection. By contrast, a 'control' cadherin that is not expressed in the placenta, H-cadherin, showed no evidence of selection. These results provide support for the hypothesis that the cadherin genes involved in maternal-foetal interactions have been subject to green-beard-effect mutations over the course of evolutionary history, leading to antagonistic coevolution with suppressing elements from the parliament of genes.
44.Crespi, B; Semeniuk, C. (2004) Parent-offspring conflict in the evolution of vertebrate reproductive mode.American Naturalist 163: 635-653 Parent-offspring conflict in the evolution of vertebrate reproductive mode
viviparity; parent-offspring conflict; placentation; reproductive mode
We propose and evaluate the hypothesis that parent-offspring conflict over the degree of maternal investment has been one of the main selective factors in the evolution of vertebrate reproductive mode. This hypothesis is supported by data showing that the assumptions of parent-offspring conflict theory are met for relevant taxa; the high number of independent origins of viviparity, matrotrophy ( direct maternal-fetal nutrient transfer), and hemochorial placentation ( direct fetal access to the maternal bloodstream); the extreme diversity in physiological and morphological aspects of viviparity and placentation, which usually cannot be ascribed adaptive significance in terms of ecological factors; and divergent and convergent patterns in the diversification of placental structure, function, and developmental genetics. This hypothesis is also supported by data demonstrating that embryos and fetuses actively manipulate their interaction with the mother, thereby garnishing increased maternal resources. Our results indicate that selection may favor adaptations of the mother, the fetus, or both in traits related to reproductive mode and that integration of physiological and morphological data with evolutionary ecological data will be required to understand the adaptive significance of interspecific variation in viviparity, matrotrophy, and placentation.
43.Crespi, BJ. (2004) Vicious circles: positive feedback in major evolutionary and ecological transitions.Trends in Ecology & Evolution 19: 627-633 Vicious circles: positive feedback in major evolutionary and ecological transitions
Evolutionary biologists and ecologists often focus on equilibrium states that are subject to forms of negative feedback, such as optima for phenotypic traits or regulation of population sizes. However, recent theoretical and empirical studies show how positive feedback can be instrumental in driving many of the most important and spectacular processes in evolutionary ecology, including the evolution of sex and genetic systems, mating systems, life histories, complex cooperation in insects and humans, ecological specialization, species diversity, species ranges, speciation and extinction. Taken together, this work suggests that positive feedback is more common than is generally appreciated, and that its self-reinforcing dynamics generate the conditions for changes that might otherwise be difficult or impossible for selection or other mechanisms to achieve. Testing for positive feedback requires analysing each causal link in feedback loops, tracking genetic, character and population-dynamic changes across generations, and elucidating the conditions that can result in self-reinforcing change.
42.Crespi, BJ; Fulton, MJ. (2004) Molecular systematics of Salmonidae: combined nuclear data yields a robust phylogeny.Molecular Phylogenetics and Evolution 31: 658-679 Molecular systematics of Salmonidae: combined nuclear data yields a robust phylogeny
Salmonidae; phylogeny; total evidence; anadromy
The phylogeny of salmonid fishes has been the focus of intensive study for many years. but some of the most important relationships within this group remain unclear. We used 269 Genbank sequences of mitochondrial DNA (from 16 genes) and nuclear DNA (from nine genes) to infer phylogenies for 30 species of salmonids. We used maximum parsimony and maximum likelihood to analyze each gene separately, the mtDNA data combined, the nuclear data combined, and all of the data together. The phylogerly with the best overall resolution and support from bootstrapping and Bayesian analyses was inferred from the combined nuclear DNA data set. for which the different genes reinforced and complemented one another to a considerable degree. Addition of the mitochondrial DNA degraded the phylogenetic signal, apparently as a result of saturation, hybridization, selection, or some combination of these processes. By the nuclear-DNA phylogeny: (1) (Hucho hucho. Brachymystax lenok) form the sister group to (Salmo. Salvelinus. Oncorhynchus H. perryi): (2) Salmo is the sister-group to (Oncorhynchus, Salvelinus); (3) Salvelinus is the sister-group to Oncorhynchus: and (4) Oncorhynchus masou forms a monophyletic group with O. mykiss and O. clarki. with these three taxa constituting the sister-group to the five other Oncorhynchus species. Species-level relationships within Oncorhynchus and Salvelinus were well Supported by bootstrap levels and Bayesian analyses. These findings have important implications for understanding the evolution of behavior, ecology and life-history in Salmonidae. (C) 2003 Elsevier Inc. All rights reserved.
41. Hallett, RH; Crespi, BJ; Borden, JH. (2004) Synonymy of Rhynchophorus ferrugineus (Olivier), 1790 and R-vulneratus (Panzer), 1798 (Coleoptera, Curculionidae, Rhynchophorinae).Journal of Natural History 38: 2863-2882 Synonymy of Rhynchophorus ferrugineus (Olivier), 1790 and R-vulneratus (Panzer), 1798 (Coleoptera, Curculionidae, Rhynchophorinae)
Asian palm weevil; red palm weevil; cross-breeding; mitochondrial DNA sequencing; morphological comparisons; RAPD analyses; Rhynchophorinae; Rhynchophorus ferrugineus; Rhynchophorus vulneratus; synonymization
Morphological, molecular-genetic and breeding data were collected to investigate the species status of the Asian palm weevils, Rhynchophorus ferrugineus (Olivier) and R. vulneratus (Panzer) (Coleoptera: Curculionidae). These weevils are distinguished by characteristic colouring of the pronota and elytra, but naturally occurring colour intermorphs were observed. Contrary to the literature, quantitative measurements of the concavity of subgenal sutures and of pronotal shape indicated no differences between the two species. Larvae did not differ significantly in labral characteristics. Random amplified polymorphic DNA (RAPD) banding patterns were identical for nine of 14 primers, indicating that these weevils are very closely related. Sequences of the cytochrome oxidase gene for 201 base pairs read were identical for R. ferrugineus and R. vulneratus , but the congener R. bilineatus differed from them by 10%, suggesting divergence of these lineages about 5 million years ago. Hybrid F1s were obtained from all heterospecific crosses, and one surviving hybrid F1 female produced viable eggs. Previous studies have revealed no pheromonal differences. On the basis of this evidence, R. ferrugineus and R. vulneratus should be considered colour morphs of the same species and be synonymized under the name Rhynchophorus ferrugineus (Olivier), with the common name Asian palm weevil.
40. Nosil, P; Crespi, BJ. (2004) Does gene flow constrain adaptive divergence or vice versa? A test using ecomorphology and sexual isolation in Timema cristinae walking-sticks.Evolution 58: 102-112 Does gene flow constrain adaptive divergence or vice versa? A test using ecomorphology and sexual isolation in Timema cristinae walking-sticks
geographic variation; host-specific selection; migration; reproductive isolation; speciation; trait divergence; walking-sticks
Population differentiation often reflects a balance between divergent natural selection and the opportunity for homogenizing gene flow to erode the effects of selection. However, during ecological speciation, trait divergence results in reproductive isolation and becomes a cause, rather than a consequence, of reductions in gene flow. To assess both the causes and the reproductive consequences of morphological differentiation, we examined morphological divergence and sexual isolation among 17 populations of Timema cristinae walking-sticks. Individuals from populations adapted to using Adenostoma as a host plant tended to exhibit smaller overall body size, wide heads, and short legs relative to individuals using Ceonothus as a host. However, there was also significant variation in morphology among populations within host-plant species. Mean trait values for each single population could be reliably predicted based upon host-plant used and the potential for homogenizing gene flow, inferred from the size of the neighboring population using the alternate host and mitochondrial DNA estimates of gene flow. Morphology did not influence the probability of copulation in between-population mating trials. Thus, morphological divergence is facilitated by reductions in gene flow, but does not cause reductions in gene flow via the evolution of sexual isolation. Combined with rearing data indicating that size and shape have a partial genetic basis, evidence for parallel origins of the host-associated forms, and inferences from functional morphology, these results indicate that morphological divergence in T. cristinae reflects a balance between the effects of host-specific natural selection and gene flow. Our findings illustrate how data on mating preferences can help determine the causal associations between trait divergence and levels of gene flow.
39. Perry, SP; Chapman, TW; Schwarz, MP; Crespi, BJ. (2004) Proclivity and effectiveness in gall defence by soldiers in five species of gall-inducing thrips: benefits of morphological caste dimorphism in two species (Kladothrips intermedius and K-habrus).Behavioral Ecology and Sociobiology 56: 602-610 Proclivity and effectiveness in gall defence by soldiers in five species of gall-inducing thrips: benefits of morphological caste dimorphism in two species (Kladothrips intermedius and K-habrus)
caste; colony defence; eusociality; soldiers; thrips
The essence of eusociality is a trade-off between producing one's own offspring and helping collateral kin via such activities as defence, foraging and brood rearing. This trade-off often involves morphological differences between "helper" and "reproductive" castes, but the advantages, correlates and phylogenetic context of morphological caste differentiation have seldom been analysed. Six species of Australian gall-inducing thrips on Acacia show morphological polymorphism. One morph, referred to as a soldier, has reduced wings and antennae but greatly enlarged fore-femora, which are thought to be adaptations for gall defence. The other, dispersing morph, has fully developed wings and relatively slight fore-femora. Here, we quantify the defensive behaviour of soldier morphs, and compare soldier and foundresses, using behavioural assays designed to measure proclivity to attack kleptoparasites (specialised invaders in the genus Koptothrips) and effectiveness in killing them. In all five species investigated, soldiers were able to kill Koptothrips. Moreover, the effectiveness of soldiers was relatively high in the more-derived species in the phylogeny of the clade, Kladothrips intermedius, K. habrus and K. waterhousei. Soldiers of K. intermedius and K. habrus also killed kleptoparasites more effectively than did foundresses, and K. habrus soldiers exhibited higher proclivity to attack than did foundresses. Data from naturally invaded galls demonstrate that soldiers in the field do kill Koptothrips, and vice versa. These results show that soldiers of Australian gall thrips are motivated and effective for gall defence.
38. Willis, PM; Crespi, BJ; Dill, LM; Baird, RW; Hanson, MB. (2004) Natural hybridization between Dall's porpoises (Phocoenoides dalli) and harbour porpoises (Phocoena phocoena).Canadian Journal of Zoology-Revue Canadienne de Zoologie 82: 828-834 Natural hybridization between Dall's porpoises (Phocoenoides dalli) and harbour porpoises (Phocoena phocoena)
Natural hybridization occurs rarely in mammals compared with other taxonomic groups of animals. Cetaceans appear unique among mammals in exhibiting striking karyological uniformity, which suggests that they have the potential to produce hybrid offspring more readily than other mammals. However, the detection and accurate identification of wild mammalian hybrids is difficult, and molecular evidence for wild cetacean hybrids is extremely limited. Here, we present molecular and morphological evidence of frequent hybridization between free-ranging Dall's, Phocoenoides dalli (True, 1885), and harbour, Phocoena phocoena (L., 1758), porpoises. The study describes a temporally and geographically concentrated case of natural hybridization in large mammals. Molecular analyses of mitochondrial and nuclear DNA revealed the species identity, sex, and direction of cross of several hybrid individuals. In concert with morphological and behavioural observations, these data confirmed the hybrid status of putative crosses in the field, including reproductive females. All crosses examined had Dall's porpoise as the maternal parent. This directionality may reflect the indiscriminate pursuit of female porpoises by male harbour porpoises. Our finding of extensive localized hybridization, despite apparently strong isolation elsewhere in their range, suggests that ecological influences on mating behaviour may be of primary importance in the reproductive isolation of these, and possibly other, cetacean species.
36. Miller, DG; Crespi, B. (2003) The evolution of inquilinism, host-plant use and mitochondrial substitution rates in Tamalia gall aphids.Journal of Evolutionary Biology 16: 731-743 The evolution of inquilinism, host-plant use and mitochondrial substitution rates in Tamalia gall aphids
inquilinism; host-plant use; phylogeny; Tamalia aphids
We used mitochondrial DNA data to infer phylogenies for 28 samples of gall-inducing Tamalia aphids from 12 host-plant species, and for 17 samples of Tamalia inquilinus , aphid 'inquilines' that obligately inhabit galls of the gall inducers and do not form their own galls. Our phylogenetic analyses indicate that the inquilines are monophyletic and closely related to their host aphids. Tamalia coweni aphids from different host plants were, with one exception, very closely related to one another. By contrast, the T. inquilinus aphids were strongly genetically differentiated among most of their host plants. Comparison of branch lengths between the T. coweni clade and the T. inquilinus clade indicates that the T. inquilinus lineage evolves 2.5-3 times faster for the cytochrome oxidase I gene. These results demonstrate that: (1) Tamalia inquilines originated from their gall-inducing hosts, (2) communal (multi-female) gall induction apparently facilitated the origin of inquilinism, (3) diversification of the inquilines has involved rapid speciation along host-plant lines, or the rapid evolution of host-plant races, and (4) the inquilines have undergone accelerated molecular evolution relative to their hosts, probably due to reduced effective population sizes. Our findings provide insight into the behavioural causes and evolutionary consequences of transitions from resource generation to resource exploitation.
35. Nosil, P; Crespi, BJ; Sandoval, CP. (2003) Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement.Proceedings of the Royal Society of London Series B-Biological Sciences 270: 1911-1918 Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement
gene flow; hybridization; natural selection; speciation; Timema; walking-stick insects
Recent years have seen a resurgence of interest in the process of speciation but few studies have elucidated the mechanisms either driving or constraining the evolution of reproductive isolation. In theory, the direct effects of reinforcing selection for increased mating discrimination where interbreeding produces hybrid offspring with low fitness and the indirect effects of adaptation to different environments can both promote speciation. Conversely, high levels of homogenizing gene flow can counteract the forces of selection. We demonstrate the opposing effects of reinforcing selection and gene flow in Timema cristinae walking-stick insects. The magnitude of female mating discrimination against males from other populations is greatest when migration rates between populations adapted to alternate host plants are high enough to allow the evolution of reinforcement, but low enough to prevent gene flow from eroding adaptive divergence in mate choice. Moreover, reproductive isolation is strongest under the combined effects of reinforcement and adaptation to alternate host plants. Our findings demonstrate the joint effects of reinforcement, ecological adaptation and gene flow on progress towards speciation in the wild.
34. Chapman, TW; Kranz, BD; Bejah, KL; Morris, DC; Schwarz, MP; Crespi, BJ. (2002) The evolution of soldier reproduction in social thrips.Behavioral Ecology 13: 519-525 The evolution of soldier reproduction in social thrips
castes; inbreeding; microsatellites; soldiers; thrips
We estimated the degree of reproductive differentiation between foundresses and soldiers in multiple populations of five species of haplodiploid Australian gall-forming thrips rising microsatellite data, ovarian dissections, and census data. Microsatellite-based species estimates of average per capita reproductive output of soldiers relative to the foundresses ranged from 0.005 to 0.64, and dissection and census-based estimates ranged from 0.17 to 1.1. Mapping of these estimates onto a phylogeny showed that levels of soldier reproduction were apparently higher in three basal lineages than in two more derived lineages. We infer from this phylogenetic pattern that soldier morphology and behavior of thrips evolved in the presence of substantial levels of soldier reproduction. This pattern of evolutionary change is similar to that proposed for the origin of soldiers in aphids and termites, but it differs from the scenario proposed for the origin of workers in Hymenoptera, within which helping and strong reproductive division of labor apparently evolved before morphological differentiation. We suggest that this difference in evolutionary routes to eusociality between taxa with soldiers and taxa with foraging workers was driven by a weaker trade-off between helping and reproducing, and a greater ability of the helpers to withstand reproductive domination, in taxa with soldiers. This is the first study to analyze the social-evolutionary trajectories of reproductive, behavioral, and morphological differentiation in the context of a species-level phylogeny.
33.Crespi, BJ; Teo, R. (2002) Comparative phylogenetic analysis of the evolution of semelparity and life history in salmonid fishes.Evolution 56: 1008-1020 Comparative phylogenetic analysis of the evolution of semelparity and life history in salmonid fishes
life history; phylogenetics; salmonids; semelparity
The selective pressures involved in the evolution of semelparity and its associated life-history traits are largely unknown. We used species-level analyses, independent contrasts, and reconstruction of ancestral states to study the evolution of body length, fecundity, egg weight, gonadosomatic index, and parity (semelparity vs. degree of iteroparity) in females of 12 species of salmonid fishes. According to both species-level analysis and independent contrasts analysis, body length was positively correlated with fecundity, egg weight, and gonaosomatic index, and semelparous species exhibited a significantly steeper slope for the regression of egg weight on body length than did iteroparous species. Percent repeat breeding (degree of iteroparity) was negatively correlated with gonadosomatic index using independent contrasts analysis. Semelparous species had significantly larger eggs by species-level analysis, and the egg weight contrast for the branch on which semelparity was inferred to have originated was significantly larger than the other egg weight contrasts, corresponding to a remarkable increase in egg weight, Reconstruction of ancestral states showed that egg weight and body length apparently increased with the origin of semelparity, but fecundity and gonadosomatic index remained more or less constant or decreased. Thus, the strong evolutionary linkages between body size, fecundity, and gonadosomatic index were broken during the transition from iteroparity to semelparity. These findings suggest that long-distance migrations, which increase adult mortality between breeding episodes, may have been necessary for the origin of semelparity in Pacific salmon, but that increased egg weight, leading to increased juvenile survivorship. was crucial in driving the transition. Our analyses support the life-history hypotheses that a lower degree of repeat breeding is linked to higher reproductive investment per breeding episode, and that semelparity evolves under a combination of relatively high juvenile survivorship and relatively low adult survivorship.
32. Kranz, BD; Schwarz, MP; Morris, DC; Crespi, BJ. (2002) Life history of Kladothrips ellobus and Oncothrips rodwayi: insight into the origin and loss of soldiers in gall-inducing thrips.Ecological Entomology 27: 49-57 Life history of Kladothrips ellobus and Oncothrips rodwayi: insight into the origin and loss of soldiers in gall-inducing thrips
brood size; eusociality; gall thrips; loss of soldiers; sex ratio; social evolution
1. The evolution of eusociality in Australian gall-inducing thrips cannot be understood without comparisons among closely related solitary species. The life history of two solitary, gall-inducing thrips, Kladothrips ellobus and Oncothrips rodwayi, was investigated, and data for solitary and eusocial species from previous studies were re-analysed. Kladothrips ellobus is in a clade that is closely related to the eusocial species. Oncothrips rodwayi is in the same clade as the eusocial species and appears to have undergone an evolutionary loss of eusociality. It is the only galling thrips on Acacia in temperate environments. 2. The brood size of K. ellobus is eight to 23 times larger than broods of foundresses in eusocial species whereas the brood size of O. rodwayi is not significantly different from those of foundresses in eusocial species. 3. In K. ellobus, the mean sex ratio was not significantly different from parity but in O. rodwayi the mean sex ratio was 0.13 male. In O. rodwayi, 77% of females were inseminated by their brothers before dispersal. which is consistent with high levels of inbreeding in eusocial species of the same clade. Sex ratios suggest random mating in K. ellobus whereas female-biased sex ratios in O. rodwayi are consistent with inbreeding and local mate competition. 4. Comparisons among solitary and eusocial species suggest that large brood size is an ancestral trait for eusociality in thrips, and this trait persists in solitary species as an r-selection strategy. Soldiers may have evolved in and environments to minimise the risks of dispersal and the costs of latency to reproduction, and to maximise gall defence. 5. Temperate conditions could have facilitated the evolutionary loss of soldiers in O. rodwayi, as there should be a shorter, safer, more predictable window period between dispersal and gall induction, reducing the period of latency to reproduction following dispersal and lowering risks of dispersal. 6. The loss of soldiers in O. rodwayi is not associated with a reversion to the large brood sizes of solitary species in ancestral lineages.
31. Law, JH; Crespi, BJ. (2002) Recent and ancient asexuality in Timema walkingsticks.Evolution 56: 1711-1717 Recent and ancient asexuality in Timema walkingsticks
ancient asexuality; phylogenetics; walkingsticks
Determining the evolutionary age of asexual lineages should help in inferring the temporal scale under which asexuality and sex evolve and assessing selective factors involved in the evolution of asexuality. We used 416 bp of the mitochondrial COI gene to infer phylogenetic relationships of virtually all known Timema walkingstick species, including extensive intraspecific sampling for all five of the asexuals and their close sexual relatives. The asexuals T. douglasi and T. shepardii were very closely related to each other and evolutionarily young (less than 0.5 million years old). For the asexuals T. monikensis and T. tahoe, evidence for antiquity was weak since only one population of each was sampled, intraspecific divergences were low, and genetic distances to related sexuals were high: maximum-likelihood molecular-clock age estimates ranged from 0.26 to 2.39 million years in T. monikensis and from 0.29-1.06 million years in T. tahoe. By contrast, T. genevieve was inferred to be an ancient asexual, with an age of 0.81 to 1.42 million years. The main correlate of the age of asexual lineages was their geographic position, with younger asexuals being found further north.
30. Law, JH; Crespi, BJ. (2002) The evolution of geographic parthenogenesis in Timema walking-sticks.Molecular Ecology 11: 1471-1489 The evolution of geographic parthenogenesis in Timema walking-sticks
nested clade analysis; parthenogenesis; phylogeography; walking-sticks
Phylogenetic studies of asexual lineages and their sexual progenitors are useful for inferring the causes of geographical parthenogenesis and testing hypotheses regarding the evolution of sex. With five known parthenogens and well-studied ecology, Timema walking-sticks are a useful system for studying these questions. Timema are mainly endemic to California and they exhibit the common pattern of geographical parthenogenesis, with asexuals exhibiting more-northerly distributions. Neighbour-joining and maximum-parsimony analyses of 416 bp of mitochondrial cytochrome oxidase I (COI) from 168 individuals were used to infer general phylogenetic relationships, resulting in three major phylogeographical subdivisions: a Northern clade; a Santa Barbara clade; and a Southern clade. A nested cladistic analysis, comparing intra- and interspecific haplotypic variation on a geographical scale, revealed that the overall pattern of geographical parthenogenesis in Timema could be attributed to historical range expansion. These results suggest that geographical parthenogenesis is the result of more-extensive northerly dispersal of asexuals than sexuals.
29. Morris, DC; Schwarz, MP; Crespi, BJ. (2002) Pleometrosis in phyllode-glueing thrips (Thysanoptera : Phlaeothripidae) on Australian Acacia.Biological Journal of the Linnean Society 75: 467-474 Pleometrosis in phyllode-glueing thrips (Thysanoptera : Phlaeothripidae) on Australian Acacia
cofounding; Dunatothrips; haplometrosis; Lichanothrips; pleometrosis
Pleometrosis, or colony founding by more than one female, is common in various social insects and it engenders opportunities for social cooperation as well as cheating. The life cycles of four species of thrips on Australian Acacia trees were examined to elucidate the extent and nature of colony founding by multiple individuals. Data from colonies of three species of thrips from the genus Dunatothrips Moulton and one species of Lichanothrips Mound were used to infer the prevalence of pleometrosis in each species. The results indicate that Dunatothrips species show high levels of cofounding, with up to 50% of colonies having more than one foundress. By contrast, colonies of Lichanothrips are predominantly established by a female and a male. As in some communal insects, pleometrosis is facultative in Dunatothrips, foundresses show more or less constant per capita reproduction with foundress number, and the selective pressures for pleometrosis may involve predation pressure during founding or survivorship insurance for the brood. In Lichanothrips, male founders are probably engaging in mate guarding, which also occurs in some species of gall-inducing thrips on Acacia. The differences in founding patterns between Dunatothrips and Lichanothrips may be due in part the nature of their domiciles: Dunatothrips engage in extensive construction of a domicile using anal secretions, whereas many Lichanothrips primarily improve a pre-existing partial enclosure. (C) 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 75, 467-474.
28. Nosil, P; Crespi, BJ; Sandoval, CP. (2002) Host-plant adaptation drives the parallel evolution of reproductive isolation.Nature 417: 440-443 Host-plant adaptation drives the parallel evolution of reproductive isolation
Parallel evolution of similar traits in independent populations that inhabit ecologically similar environments strongly implicates natural selection as the cause of evolution(1). Parallel speciation is a special form of parallel evolution where traits that determine reproductive isolation evolve repeatedly, in closely related populations, as by-products of adaptation to ecological conditions(1,2). The outcome of such parallel evolution is that ecologically divergent pairs of populations exhibit greater levels of reproductive isolation than ecologically similar pairs of populations of a similar or younger age(2-4). The parallel evolution of reproductive isolation provides strong evidence for natural selection in the process of speciation(1), but only one conclusive example from nature is known(2). Populations of the walking-stick insect Timema cristinae that use different host-plant species have diverged in body size and shape, host preference, behaviour and the relative frequency of two highly cryptic colour-pattern morphs(5,6). Here we report that divergent selection for host adaptation, and not genetic drift, has promoted the parallel evolution of sexual isolation in this species. Our findings represent a clear demonstration that host-plant adaptation can play a crucial and repeatable role in the early stages of speciation.
25.Crespi, BJ. (2001) The evolution of social behavior in microorganisms.Trends in Ecology & Evolution 16: 178-183 The evolution of social behavior in microorganisms
Recent studies of microorganisms have revealed diverse complex social behaviors, including cooperation in foraging, building, reproducing, dispersing and communicating. These microorganisms should provide novel,tractable systems for the analysis of social evolution. The application of evolutionary and ecological theory to understanding their behavior will aid in developing better means to control the many pathogenic bacteria that use social interactions to affect humans.
24. Kranz, BD; Chapman, TW; Crespi, BJ; Schwarz, MP. (2001) Social biology and sex ratios in the gall-inducing thrips, Oncothrips waterhousei and Oncothrips habrus.Insectes Sociaux 48: 315-323 Social biology and sex ratios in the gall-inducing thrips, Oncothrips waterhousei and Oncothrips habrus
gall thrips; sex ratio; protogyny; inbreeding
We studied the life history and social biology of two haplodiploid eusocial gall-inducing thrips, Oncothrips waterhousei and O. habrus. Both species have alternating generations of non-dispersing, micropteran soldiers and macropteran dispersers. A single female induces a gall, and produces all of the soldiers, which are protogynous and have an overall female-biased sex ratio in both species. The soldiers sibmate and collectively produce about 80% and 50% of the dispersing generation in O. waterhousei and O. habrus, respectively. On a per capita basis soldiers produce about 0.47 and 0.15 the number of dispersers of the foundress in O. waterhousei and O. habrus, respectively. The dispersers have an unbiased sex ratio in both species, but sibmating and local mate competition between soldiers suggests that these sex ratios are not a result of panmictic conditions. A comparison of the proportion of the gall occupied by brood in O. waterhousei and another eusocial galling thrips, Kladothrips hamiltoni, suggests that local resource competition is higher in K. hamiltoni, which might partly explain the lack of sex ratio bias in soldiers of the latter species.
23. Kranz, BD; Schwarz, MP; Wills, TE; Chapman, TW; Morris, DC; Crespi, BJ. (2001) A fully reproductive fighting morph in a soldier clade of gall-inducing thrips (Oncothrips morrisi).Behavioral Ecology and Sociobiology 50: 151-161 A fully reproductive fighting morph in a soldier clade of gall-inducing thrips (Oncothrips morrisi)
soldiers; micropterous; reproductive skew; social evolution; gall thrips
We present the first life history data for Oncothrips morrisi, a species in a clade of haplodiploid, Australian gall-inducing thrips that has a micropteran fighting morph in the first generation of the gall. Micropterans in other species in the clade have lower fecundity than their mother, and these species are considered eusocial. There is no such reproductive skew in O. morrisi, and the species is not eusocial by any definition. The volume of O. morrisi galls is between 4 and 20 times greater in than eusocial species in the clade and the dispersing-brood size varies between 5 and 15 times larger than that of other species. The lack of skew in O. morrisi could be associated with large gall volume, reducing competition between females for space and feeding sites for their offspring. As O. morrisi is in a lineage basal to eusocial Oncothrips, we also discuss selective factors for the evolution of a non-dispersing fighting morph in this clade. The costs involved in dispersal and latency to reproduction may have lowered the selective threshold for the evolution of a non-dispersing morph. Once non-dispersal evolved, selection to defend one's offspring may have promoted the evolution of soldier-like morphology and behaviour.
22. Morris, DC; Schwarz, MP; Crespi, BJ; Cooper, SJB. (2001) Phylogenetics of gall-inducing thrips on Australian Acacia.Biological Journal of the Linnean Society 74: 73-86 Phylogenetics of gall-inducing thrips on Australian Acacia
Thysanoptera; Phlaeothripidae; kleptoparasite; soldier castes
Analysis of DNA sequence data from four genes (Elongation Factor-1 alpha, wingless, 16S rDNA and cytochrome oxidase I) yielded a well-resolved, well-supported phylogeny for all 21 species of gall-inducing thrips found on Australian Acacia. This phylogeny was then used to investigate the evolution of various behavioural and life history traits, and to examine the level of agreement with the taxonomy of the group. Our results suggest that there may have been a single origin of soldier castes in gall-inducing thrips. Examination of the distribution of the three primary life history strategies employed by these thrips (pupating in the gall, pupating in soil with soldier castes and pupating in soil without soldier castes) indicates that two of the strategies may have evolved as a result of factors associated with host plant affiliations or through parasite pressure. Our phylogeny does not support the existing generic classification of the group in that the genera are not monophyletic, nor does it lend itself to a clear solution to improve the classification in accordance with the phylogeny. (C) 2001 The Linnean Society of London.
21. Chapman, TW; Crespi, BJ; Kranz, BD; Schwarz, MP. (2000) High relatedness and inbreeding at the origin of eusociality in gall-inducing thrips.Proceedings of the National Academy of Sciences of the United States of America 97: 1648-1650 High relatedness and inbreeding at the origin of eusociality in gall-inducing thrips
Within the haplodiploid eusocial gall-inducing thrips, a species-level phylogeny combined with genetic data for five eusocial species enables an inference of levels of relatedness and inbreeding values for lineages at the origin of eusociality. Character optimization using data from five eusocial species indicates that the lineage or lineages where eusociality is inferred to have originated exhibit relatedness of 0.64-0.92, and F-IS of 0.33-0.64, The high inbreeding coefficients found in these eusocial thrips have increased relatedness among and within both sexes and have reduced the haplodiploidy-induced relatedness asymmetries [Hamilton, W. D. (1964) J. Theor, Biol, 7. 1-52]. These results indicate that unusually high relatedness is associated with the origin of eusociality, and they suggest a role for inbreeding in the evolution of bisexual helping.
20.Crespi, BJ. (2000) The evolution of maladaptation.Heredity 84: 623-629 The evolution of maladaptation
adaptation; adaptive peaks; evolution; maladaptation
This review contains a description of a research program for the study of maladaptation, defined here in terms of deviation from adaptive peaks. Maladaptation has many genetic causes, including mutation, inbreeding, drift, gene flow, heterozygote advantage and pleiotropy. Degrees of maladaptation are determined by genetic architecture and the relationship between the rates of selective, environmental change and the nature and extent of genetic responses to selection. The empirical analysis of maladaptation requires: (1) recognition of putative maladaptation, using methods from phylogenetics, teleonomy, development and genetics, followed by an assessment of the nature and degree of deviation from adaptation, using studies of natural selection and teleonomy; (2) determination of the causes of the deviation, using analyses of genetics, development, or other methods. Conditions for unambiguously identifying maladaptation are considerably more stringent than those for demonstrating adaptation and remarkably few studies have clearly identified and characterised maladaptative traits. A thorough understanding of the nature of phenotypic variation will never be achieved without an analysis of the scope and usual causes of maladaptation.
19.Crespi, BJ; Ragsdale, JE. (2000) A skew model for the evolution of sociality via manipulation: why it is better to be feared than loved.Proceedings of the Royal Society of London Series B-Biological Sciences 267: 821-828 A skew model for the evolution of sociality via manipulation: why it is better to be feared than loved
reproductive skew model; social behaviour; cooperation; manipulation
Concession-based reproductive skew models predict that social groups can form via persuasion, whereby dominant individuals forfeit some reproduction to subordinates as an incentive to stay and help. We have developed an alternative skew model based on manipulation, whereby dominant individuals coerce subordinates into staying and helping by imposing costs on their independent reproductive prospects. Stable groups can evolve under a much wider range of genetic and ecological conditions under this manipulation model than under concession models. We describe evidence that various forms of preemptive and ongoing manipulation occur in nature and we discuss the implications of the model for the development of a general theory of social evolution.
18.Crespi, BJ; Sandoval, CP. (2000) Phylogenetic evidence for the evolution of ecological specialization in Timema walking-sticks.Journal of Evolutionary Biology 13: 249-262 Phylogenetic evidence for the evolution of ecological specialization in Timema walking-sticks
crypsis; host-plants; phylogeny; specialization
We used phylogenetic and ecological information to study the evolution of host-plant specialization and colour polymorphism in the genus Timema, which comprises 14 species of walking-sticks that are subject to strong selection for cryptic coloration on their host-plants. Phylogenetic analysis indicated that this genus consists of three main lineages. Two of the lineages include highly generalized basal species and relatively specialized distal species, and one of the lineages comprises four specialized species. We tested for phylogenetic conservatism in the traits studied via randomizing host-plant use, and the four basic Timema colour patterns, across the tips of the phylogeny, and determining if the observed number of inferred changes was significantly low compared to the distribution of numbers of inferred changes expected under the null model. This analysis showed that (1) host-plant use has evolved nonrandomly, such that more closely related species tend to use similar sets of hosts and (2) colour pattern evolution exhibits considerable lability. Inference of ancestral states using maximum parsimony, under four models for the relative ease of gain and loss of plant hosts or colour morphs, showed that (1) for all models with gains of host-plants even marginally more difficult than losses, and for most optimizations with gains and losses equally difficult, the ancestral Timema were generalized, feeding on the chaparral plants Ceanothus and Adenostoma and possibly other taxa, and (2) for all models with gains of colour morphs more difficult than losses, the ancestral Timema were polymorphic for colour pattern. Generation of null distributions of inferred ancestral states showed that the maximum-parsimony inference of host-plant generalization was most robust for the most speciose of the three main Timema lineages. Ancestral states were also inferred using maximum likelihood, after recoding host-plant use and colour polymorphism as dichotomous characters. Likelihood analyses provided some support for inference of generalization in host-plant use at ancestral nodes of the two lineages exhibiting mixtures of generalists and specialists, although levels of uncertainty were high. By contrast, likelihood analysis did not estimate ancestral colour morph patterns with any confidence, due to inferred rates of change that were high with respect to speciation rates. Information from biogeography, floristic history and the timing of diversification of the genus are compatible with patterns of inferred ancestral host-plant use. Diversification in the genus Timema appears to engender three main processes: (1) increased specialization via loss of host-plants, (2) retention of the same, single, host-plant and (3) shifts to novel hosts to which lineages were 'preadapted' in colour pattern. Our evidence suggests that the radiation of this genus has involved multiple evolutionary transitions from individual-level specialization (multiple-niche polymorphism) to population-level and species-level specialization. Ecological studies of Timema suggest that such transitions are driven by diversifying selection for crypsis. This paper provides the first phylogeny-based evidence for the macroevolutionary importance of predation by generalist natural enemies in the evolution of specialization.
17. Giblin-Davis, RM; Gries, R; Crespi, B; Robertson, LN; Hara, AH; Gries, G; O'Brien, CW; Pierce, HD. (2000) Aggregation pheromones of two geographical isolates of the New Guinea sugarcane weevil, Rhabdoscelus obscurus.J. Chem. Ecol. 26: 2763-2780 Aggregation pheromones of two geographical isolates of the New Guinea sugarcane weevil, Rhabdoscelus obscurus
aggregation pheromones; Coleoptera; Curculionidae; cytochrome oxidase I; 2-methyl-4-heptanol; (E2)-6-methyl-2-hepten-4-ol; 2-methyl-4-octanol; mitochondrial DNA; New Guinea sugarcane weevil; palm weevil; Rhabdoscelus obscurus; rhynchophorol; sibling species; sugarcane
The aggregation pheromones were studied from two geographical isolates (Hakalau, Hawaii, and Silkwood, Queensland, Australia) of the New Guinea sugarcane weevil, Rhabdoscelus obscurus. Coupled gas chromatographic-electroantennographic detection (GC-EAD) and GC-mass spectrometric (MS) analyses of Porapak Q volatile extract from male and from female Hawaiian R. obscurus revealed a single EAD-active, male-specific candidate pheromone, which was identified as 2-methyl-4-octanol (1). Corresponding volatile analyses from male and from female Australian R. obscurus consistently revealed three EAD-active, male-specific candidate pheromone components that were identified as 1, (E2)-6-methyl-2-hepten-4-ol (rhynchophorol) (2), and 2-methyl-4-heptanol (3). In field experiment 1 in Hakalau, Hawaii, traps baited with a stereoisomeric mixture of synthetic 1 (3 mg/day) plus sugarcane captured more weevils than did traps baited with 1 or sugarcane alone or no bait, indicating that 1 is the pheromone of the Hawaiian R. obscurus population. In field experiment 2, conducted in Silkwood, Australia. traps baited with stereoisomeric mixtures of synthetic 1, 2. and 3 (3 mg/day each) plus sugarcane caught more weevils than did unbaited traps or traps baited with 1, 2, and 3 or sugarcane. Testing candidate pheromone components 1, 2, and 3 in experiments 2-5 in all possible binary, ternary, and quaternary combinations with sugarcane. indicated that 1 and 2 in combination, but not singly, are pheromone components of the Australian R. obscurus population. Weevils from several locations in Australia and Hawaii could not be differentiated using traditional morphological characters or ultrastructural comparisons with scanning electron microscopy (SEM). However, comparisons of mtDNA sequences (cytochrome oxidase I: regions 11 to M4; 201 base pairs) revealed 5.5% variation between the Hawaiian (N = 2) and the Australian (N = 4) samples. There was no intrapopulation variation in sequence data from the weevils from Hawaii versus Australia, suggesting that they are sibling species. DOI
16. Kranz, BD; Schwarz, MP; Giles, LC; Crespi, BJ. (2000) Split sex ratios and virginity in a gall-inducing thrips.Journal of Evolutionary Biology 13: 700-706 Split sex ratios and virginity in a gall-inducing thrips
galls; haplodiploidy; sociality; split-sex ratios; thrips; virginity
Split sex ratios have been predicted in haplodiploid populations with high proportions of reproductive virgins, but there has been little empirical support. We found such split sex ratios in the gall-inducing thrips, Kladothrips rugosus. Sex ratios of juveniles from 96 galls were determined using chaetotaxy over two consecutive summers. The population-wide sex ratio was unbiased, but bimodal. Twenty-four per cent of galls only contained male juveniles. These galls were induced by a female that was probably a virgin. The mean sex ratio of all other galls was 0.36 +/- 0.02, which is not significantly different from the theoretical evolutionarily stable sex ratio of 0.34, calculated from a previous model (Godfray, H.C.J. 1990. J. Evol. Biol. 3: 3-17) for 24% constrained females in a panmictic population. These data provide the first empirical support for the constrained sex allocation model of Godfray.
15.Crespi, B; Abbot, P. (1999) The behavioral ecology and evolution of kleptoparasitism in Australian gall thrips.Florida Entomologist 82: 147-164 The behavioral ecology and evolution of kleptoparasitism in Australian gall thrips
Acacia; cladistics; gall thrips; kleptoparasites; sociality
We used a combination of behavioral-ecological and molecular-phylogenetic data to analyze the origin and diversification of kleptoparasitic (gall-stealing) thrips in the genus Koptothrips, which comprises four described species that invade and breed in galls induced by species of Oncothrips and Kladothrips on Australian Acacia. The genus Koptothrips is apparently monophyletic and not closely related to its hosts. Two of the species, K. dyskritus and K. flavicornis, each appears to represent a suite of closely-related sibling species or host races. Three of the four Koptothrips species are facultatively kleptoparasitic, in that females can breed within damaged, open galls by enclosing themselves within cellophane-like partitions. Facultative kleptoparasitism may have served as an evolutionary bridge to the obligately kleptoparasitic habit found in K. flavicornis. Evidence from phylogenetics, and Acacia host-plant relationships of the kleptoparasites and the gall-inducers, suggests that this parasite-host system has undergone some degree of cospeciation, such that speciations of Koptothrips have tracked the speciations of the gall-inducers. Quantification of kleptoparasitism rates indicates that Koptothrips and other enemies represent extremely strong selective pressures on most species of gall-inducers. Although the defensive soldier morphs found in some gall-inducing species can successfully defend against Koptothrips invasion, species with soldiers are still subject to high rates of successful kleptoparasite attack. Gall-inducing thrips exhibit three main types of life-history adaptation that have apparently evolved in response to kleptoparasite pressure: (1) "fighters which exhibit long-lived galls and soldier morphs, (2) "runners", which have quite short-lived galls, from which offspring disperse as second instar larvae, and (3) "hiders", whose galls are long-lived, especially tight-sealing, and induced on a taxonomically-distinct group of Acacia host plants that is seldom attacked.
14. Harrison, MK; Crespi, BJ. (1999) Phylogenetics of Cancer crabs (Crustacea : Decapoda : Brachyura).Molecular Phylogenetics and Evolution 12: 186-199 Phylogenetics of Cancer crabs (Crustacea : Decapoda : Brachyura)
We used morphological, mitochondrial DNA sequence, paleontological, and biogeographical information to examine the evolutionary history of crabs of the genus Cancer. Phylogenies inferred from adult morphology and DNA sequence of the cytochrome oxidase I (COI) gene were each well resolved and well supported, but differed substantially in topology. Four lines of evidence suggested that the COI data set accurately reflected Cancer phylogeny: (1) in the phylogeny inferred from morphological data, each Atlantic species was sister taxon to an ecologically similar Pacific species, suggesting convergence in morphology; (2) a single trans-Arctic dispersal event, as indicated by the phylogeny inferred from COI, is more parsimonious than two such dispersal events, as inferred from morphology; (3) test and application of a maximum likelihood molecular clock to the COI data yielded estimates of origin and speciation times that fit well with the fossil record; and (4) the tree inferred from the combined COI and morphology data was closely similar to the trees inferred from COI, although notably less well supported by the bootstrap. The phylogeny inferred from maximum likelihood analysis of COI suggested that Cancer originated in the North Pacific in the early Miocene, that the Atlantic species arose from a North Pacific ancestor, and that Cancer crabs invaded the Atlantic from the North Pacific 6-12 mya, This inferred invasion time is notably prior to most estimates of the date of submergence of the Baring Strait and the trans-Arctic interchange, but it agrees with fossil evidence placing at least one Cancer species in the Atlantic about 8 mya. (C) 1999 Academic Press.
13. Harrison, MK; Crespi, BJ. (1999) A phylogenetic test of ecomorphological adaptation in Cancer crabs.Evolution 53: 961-965 A phylogenetic test of ecomorphological adaptation in Cancer crabs
body size; Cancer crabs; ecomorphological adaptation; evolutionary contrasts; habitat shift
We used McPeek's (1995a) method of evolutionary contrasts, and phylogenetic trees derived from maximum-parsimony, neighbor-joining, and maximum-likelihood analyses of data from the cytochrome oxidase I (COI) gene to evaluate the hypothesis that macroevolutionary changes in habitat use have driven the morphological diversification of Cancer crabs. All of our analyses suggested that habitat shifts from structurally complex substrates (e.g., the rocky intertidal zone) to more homogeneous substrates (e.g., sand or mud) have occurred independently in three Cancer lineages. Evolutionary contrasts analyses indicated that these habitat shifts were accompanied by increased morphological change toward larger body sizes. These macroevolutionary patterns support the hypothesis that the morphological diversification of Cancer crabs is strongly related to size-dependent habitat use; ancillary evidence suggests that increased predation pressure in homogeneous habitats represents the main selective agent for increased body size.
12. Kranz, BD; Schwarz, MP; Mound, LA; Crespi, BJ. (1999) Social biology and sex ratios of the eusocial gall-inducing thrips Kladothrips hamiltoni.Ecological Entomology 24: 432-442 Social biology and sex ratios of the eusocial gall-inducing thrips Kladothrips hamiltoni
galls; haplodiploidy; incest; local mate competition; local resource competition; sex ratio; thrips
1. Thrips comprise the only order besides Hymenoptera where females are diploid and males are haploid. This makes them useful insects for studying the roles of kin selection and ecology in social evolution. 2. Kladothrips hamiltoni is one of six species of Australian gall-inducing thrips that have been identified as eusocial. Galls are initiated by a single foundress, who rears her brood and remains within the enclosed gall for life. The adults of both sexes of her first brood cohort are morghologically distinct from the second generation, comprising a nondispersing soldier caste. The foundress and sib-mated soldiers jointly produce a second, dispersing generation, approximately 60-80% of which are produced by the soldiers. Mean per capita egg production of female soldiers is less than 33% that of the foundress. 3. Adult eclosion of soldiers is protandrous but the overall sex ratio of the soldiers lacks bias (52% male). Protandry of soldiers increases the probability that female soldiers will be inseminated soon after their eclosion and therefore lay fertilised, female eggs. The lack of bias could be due to a balance between local resource competition and local mate competition. Gender-specific defensive behaviour of soldiers with their enemies may also be important in explaining this unexpected sex ratio. 4. The dispersing generation has an overall extreme female bias (5.6% male). Soldier incest increases relatedness between females more than between males, such that the foundress is more related to her granddaughters than her daughters, and female soldiers are more related to their daughters than their sons (assuming within-gall relatedness <1). A female bias in the offspring of soldiers should be preferred by both the foundress and soldiers as they are more related to soldier-produced dispersing females than any other thrips in the gall. Female bias in the dispersing generation will also reduce local mate competition between males. Both soldier incest and local mate competition may therefore contribute to the extreme female bias in the dispersing generation. 5. Selection pressures for sociality in gall-inducing thrips appear to be more similar to those in gall-inducing aphids and naked mole rats than to those in Hymenoptera.
11. Morris, DC; Mound, LA; Schwarz, MP; Crespi, BJ. (1999) Morphological phylogenetics of Australian gall-inducing thrips and their allies: the evolution of host-plant affiliations, domicile use and social behaviour.Systematic Entomology 24: 289-299 Morphological phylogenetics of Australian gall-inducing thrips and their allies: the evolution of host-plant affiliations, domicile use and social behaviour
A phylogeny for seventy-two species of Australian thrips in the subfamily Phlaeothripinae, based on cladistic analysis of forty morphological adult characters, is presented. We use this phylogeny to infer the evolutionary history of host-plant affiliations, gall induction and other types of domicile use, and different forms of social behaviour. Maximum parsimony analysis yielded forty-eight cladograms of length 316, and the strict consensus of these cladograms was well resolved. This phylogeny indicated that: (1) associations of thrips with their host plants tend to be evolutionarily conservative, with monophyletic groups of thrips on the host-plant genera Acacia, Casuarina and Geijera, (2) galling has evolved multiple times, on different host plants, (3) transitions in domicile use include changes between galling and living in holes or old galls, between living in glued phyllodes and living in old galls, and between leaf-feeding and galling, and (4) in three of five cases, inquiline lineages were not closely related to their host lineages and the evolution of inquilinism apparently involved a host-plant shift. However, in two cases, inquilines were very closely related to their gall-inducing hosts. Eusocial behaviour (involving soldier castes) has evolved in different lineages from those that exhibit communal behaviour (cooperation in building or defending domiciles), suggesting a lack of direct transition between the two social systems. This phylogeny serves as a framework for future molecular systematic studies, and future comparative analysis of ecology and behaviour in the Phlaeothripinae.
10. Chapman, TW; Crespi, B. (1998) High relatedness and inbreeding in two species of haplodiploid eusocial thrips (Insecta : Thysanoptera) revealed by microsatellite analysis.Behavioral Ecology and Sociobiology 43: 301-306 High relatedness and inbreeding in two species of haplodiploid eusocial thrips (Insecta : Thysanoptera) revealed by microsatellite analysis
social behavior; sib-mating; effective number of mates; soldier caste
Relatedness and inbreeding coefficients were estimated for Oncothrips tepperi and O, habrus, two species of eusocial gall-forming thrips, using data from two microsatellite loci. Relatedness between sets of individuals (sexes and castes) for O. tepperi ranged from 0.5 to 0.85 and for O, habrus estimates were centered around 0.5. Multiple mating in O. habrus was implicated in lowering relatedness within a gall. We estimated the inbreeding coefficient to be 0.38 for both species, the highest estimates known for eusocial insects. Our findings imply that high relatedness and inbreeding are important for the evolution and form of social behavior in Australian gall-forming Thysanoptera.
9.Crespi, B; Worobey, M. (1998) Comparative analysis of gall morphology in Australian gall thrips: The evolution of extended phenotypes.Evolution 52: 1686-1696 Comparative analysis of gall morphology in Australian gall thrips: The evolution of extended phenotypes
adaptation; extended phenotypes; gall morphology; gall thrips; phylogeny
We used a combination of morphometric, phylogenetic, and life-history information to analyze the evolution and possible adaptive significance of gall morphology in a clade of 24 species of gall-inducing thrips (Insecta: Thysanoptera) on Australian Acacia trees. Principal components analysis revealed that galls varied in morphology along two main axes, spherical versus elongate (PC1) and general size (PC2). A high degree of conservation of gall shape on an independently derived phylogeny of the insects and the presence of nine species of Acacia each bearing two or three morphologically disparate gall forms induced by different thrips species indicate that interspecific variation in gall form is determined predominantly by the insects. Character optimization of PC1 on the phylogeny of gall thrips suggested that the ancestral gall form was a simple roll or curl. The diversification of gall form involved four main processes: (1) the convergent evolution of relatively spherical galls in two clades; (2) the evolution of small elongate and hemispherical galls in one clade; (3) the evolution of a lobed interior in a species with a spherical gall and multiple within-gall generations; and (4) the evolution of intraspecific gall polymorphism in a clade of apparent sibling species. Comparative analyses indicated that gall sphericity was associated with the presence of physogastry (foundress hyperfecundity) and that small elongate and hemispherical forms may be associated with the presence of multiple generations in a gall and, perhaps, with the presence of soldier castes. The evolution of a lobed interior in one species, which greatly increases inner surface area, coincided with the evolution of multiple generations. In the clade with intraspecific gall polymorphism in some species, patterns of intraspecific variation mirror patterns of interspecific variation within the clade as a whole. This is the first study to analyze the evolution of gall size and shape in a phylogenetic context and to investigate the life-history correlates of evolutionary changes in gall form. Taken together, our findings indicate that the main selective pressures driving the evolution of gall form in Australian gall thrips on Acacia involve inner surface area to volume relationships, which change in concert with foundress fecundity and the number of within-gall generations.
8.Crespi, BJ; Carmean, DA; Mound, LA; Worobey, M; Morris, D. (1998) Phylogenetics of social behavior in Australian gall-forming thrips: Evidence from mitochondrial DNA sequence, adult morphology and behavior, and gall morphology.Molecular Phylogenetics and Evolution 9: 163-180 Phylogenetics of social behavior in Australian gall-forming thrips: Evidence from mitochondrial DNA sequence, adult morphology and behavior, and gall morphology
Six species of Australian gall-forming thrips (Insecta: Thysanoptera) on Acacia exhibit soldier castes, individuals with reduced wings and enlarged forelegs that defend their gall against interspecific invaders. We used data from two mitochondrial genes (cytochrome oxidase I and 16S rDNA), adult morphology and behavior, and gall morphology to infer a phylogeny for Acacia gall-forming thrips with and without soldiers, and we used this phylogeny to evaluate hypotheses concerning soldier evolution. Phylogenies inferred from each data set analyzed separately yielded large numbers of most-parsimonious trees and weak support for most nodes. However, when analyzed together the data sets complemented and reinforced one another in such a way as to yield a well-resolved phylogeny. Our phylogeny implies that soldiers originated once or twice early in the history of this clade, that soldiers were lost once or twice, and that soldiers evolved from winged dispersers rather than from non-soldier within-gall reproductive offspring of foundresses. The phylogeny also provides evidence for long-term morphological stasis, an ancient split between eastern and western gall thrips species, and a high degree of conservatism in host-plant affiliations. (C) 1998 Academic Press.
7. Mound, LA; Crespi, BJ; Tucker, A. (1998) Polymorphism and kleptoparasitism in thrips (Thysanoptera : Phlaeothripidae) from woody galls on Casuarina trees.Australian Journal of Entomology 37: 8-16 Polymorphism and kleptoparasitism in thrips (Thysanoptera : Phlaeothripidae) from woody galls on Casuarina trees
behavioural polymorphism; gall induction; genitalic dimorphism
Two species of Iotatubothrips are now known, both inducing woody stem galls on Casuarina trees In Australia, and the single known species in each of Phallothrips and Thaumatothrips kleptoparasitise these galls. All four species of thrips vary remarkably in body form, in association with wing and behavioural polymorphisms, In particular, the previously unknown macropterae of Phallothrips houstoni are strikingly different in body form from the apterae of this species. The weakly armed macropterae invade Iotatubothrips galls, isolate themselves individually within a small, self-built enclosure, and produce a brood of highly armed apterae that then leaves the enclosure and usurps the gall. In contrast, macropterae of Thaumatothrips froggatti are well armed and heavily sclerotised, and apparently do not isolate themselves within a gall subsequent to invading it. One of the two species of Iotatubothrips is here newly described as Iotatubothrips kranzae. It is remarkable because the male genitalia are about 55% longer in macropterae than micropterae, and are longer than in any other thysanopteran. This is the first recorded instance of genitalic dimorphism within a Thysanoptera species. This species is from Western Australia on Casuarina obesa, whereas the previously known species, Iotatubothrips crozieri, is from eastern Australia on Casuarina cristata and Casuarina pauper. In contrast, no significant morphological differences were detected between the eastern and western populations of the Phallothrips and Thaumatothrips species on these tree species. All four thrips species exhibit unusually high intrapopulation variation within all morphs, and this may be related to fluctuations in within-gall density and, for the kleptoparasites, deterioration of feeding conditions in older galls.
6. Sandoval, C; Carmean, DA; Crespi, BJ. (1998) Molecular phylogenetics of sexual and parthenogenetic Timema walking-sticks.Proceedings of the Royal Society B-Biological Sciences 265: 589-595 Molecular phylogenetics of sexual and parthenogenetic Timema walking-sticks
parthenogenesis; speciation; walking-sticks
We inferred a phylogeny for the walking-stick genus Timema (Insecta: Phasmatoptera) using mitochondrial DNA sequence, and we used the phylogeny to infer temporal patterns of speciation and the evolutionary history of parthenogenesis. Maximum parsimony, neighbour-joining and maximum-likelihood analyses of 660 base pairs (bp) of cytochrome oxidase I (COT) yielded phylogenies that were well resolved and topologically identical or very similar. Application of an insect molecular clock for COI suggests that the genus originated in southern California, northern Mexico or Arizona about 20 million years ago and underwent a burst of speciation 1.5-3 million years ago during the uplifts of the Sierra Nevada, Coast, and Transverse Ranges. The phylogeny indicates that the three parthenogenetic lineages of Timema have arisen independently and are each closely related to morphologically indistinguishable or similar sexual species. Each of the three lineages exhibits an allopatric or parapatric, and more northerly, distribution with regard to their closest sexual relative. COI divergence levels between each of the three parthenogens and their closest sexual relative suggest ancient origins of parthenogenesis, 1.5-3 million years ago, that may coincide with the extensive glaciation that formed the North American ice sheets.ResearchGate DOI
5.Crespi, BJ; Carmean, DA; Chapman, TW. (1997) Ecology and evolution of galling thrips and their allies.Annual Review of Entomology 42: 51-71 Ecology and evolution of galling thrips and their allies
galls; behavior; tritrophic interactions; sociality
About 300 species of thrips belonging to 57 genera are known to form galls. Galls are caused by feeding, usually by one or more adults, on actively growing plant tissue. Most thrips genera with galling capabilities exploit multiple plant families, but there are several possible cases of thrips tracking the speciations of their host-plants. Gall morphology in thrips reflects insect phylogenetic relationships rather than those of plants. Galling species and their nongalling allies on Acacia in Australia exhibit a range of complex social behavior, including soldier castes, pleometrosis (i.e. joint colony founding), group foraging, and group defense, that is directly related to the nature of their domiciles. Galling thrips, by virtue of their haplodiploid genetic system and their ecological relationships with plants and natural enemies, are useful for analyzing a wide range of ecological, evolutionary, and behavioral questions.
4.Crespi, BJ; Vanderkist, BA. (1997) Fluctuating asymmetry in vestigial and functional traits of a haplodiploid insect.Heredity 79: 624-630 Fluctuating asymmetry in vestigial and functional traits of a haplodiploid insect
fluctuating asymmetry; haplodiploidy; vestigial traits
If natural selection on fluctuating asymmetry (FA) is common and related to trait functionality, then vestigial traits should show elevated FA. Moreover, if FA increases with heterozygosity, then haploid males of haplodiploid taxa should exhibit higher FA than diploid females. We measured fluctuating asymmetry of functional traits (fore femora of soldier morphs and disperser morphs, and wings of dispersers) and a vestigial trait (wings of soldiers) in the eusocial haplodiploid gall thrips Oncothrips tepperi (Insecta: Thysanoptera). Wing FA, but not femur FA, was substantially and significantly higher in soldiers than in dispersers in both sexes. Patterns of intersexual variation in FA were complex: for wings, female soldiers had higher FA than male soldiers but male dispersers had higher FA than female dispersers, and for femora, males and females did not differ in FA in either morph. Our results suggest that vestigial traits exhibit higher FA because of relaxation of selection for functionality, and that haploidy does not necessarily lead to increased FA in males of haplodiploid taxa.
3.Crespi, B; Carmean, D; Vawter, L; VonDohlen, C. (1996) Molecular phylogenetics of Thysanoptera.Systematic Entomology 21: 79-87 Molecular phylogenetics of Thysanoptera
Analyses of morphological data on the higher-level phylogenetics of Thysanoptera have suggested two alternative hypotheses: (1) sister-taxon status of the monophyletic suborders Terebrantia and Tubulifera, and (2) paraphyly of Terebrantia with respect to Tubulifera. Analyses of nucleotide sequence data from the mitochondrial gene cytochrome oxidase I and the nuclear gene 18S rDNA using maximum parsimony, neighbour joining, and maximum likelihood provide strong support for the hypothesis of a sister-taxon relationship between the Terebrantia and Tubulifera. These data resolve this long-standing controversy in thysanopteran phylogenetics and provide a framework for further studies of higher-level relationships in this order.
2. Mound, LA; Crespi, BJ; Kranz, B. (1996) Gall-inducing Thysanoptera (Phlaeothripidae) on Acacia phyllodes in Australia: Host-plant relations and keys to genera and species.Invertebrate Taxonomy 10: 1171-1198 Gall-inducing Thysanoptera (Phlaeothripidae) on Acacia phyllodes in Australia: Host-plant relations and keys to genera and species
The available biological information on the association, unique to Australia, between gall-inducing thrips and the phyllodes of Acacia species is summarised. Identification keys to the three genera and 21 gall-inducing species involved are presented, together with descriptions of nine new species (Kladothrips harpophyllae, Kladothrips maslini, Kladothrips xiphius, Oncothrips morrisi, Oncothrips schwarzi, Oncothrips sterni, Oncothrips torus, Onychothrips pilbara and Onychothrips zygus).
1. Carmean, D; Crespi, BJ. (1995) Do long branches attract flies?Nature 373: 666 Do long branches attract flies?
Strepsiptera and Diptera group together in phylogenetic analysis as an artefact resulting from the high substitution rates in their 18S rDNA sequences. The grouping is an excellent example of long-branch attraction resulting from the violation of the molecular clock for this gene. Website DOI
