68. Guerra, VI; Haynes, G; Byrne, M; Hart, MW. (2021) Selection on genes associated with the evolution of divergent life histories: Gamete recognition or something else?Evol. Dev. 23: 423-438 Selection on genes associated with the evolution of divergent life histories: Gamete recognition or something else?
brooding; Cryptasterina hystera; Cryptasterina pentagona; RNA-seq; selection
Gamete compatibility, and fertilization success, is mediated by gamete-recognition genes (GRGs) that are expected to show genetic evidence of a response to sexual selection associated with mating system traits. Changes in the strength of sexual selection can arise from the resolution of sperm competition among males, sexual conflicts of interest between males and females, or other mechanisms of sexual selection. To assess these expectations, we compared patterns of episodic diversifying selection among genes expressed in the gonads of Cryptasterina pentagona and C. hystera, which recently speciated and have evolved different mating systems (gonochoric or hermaphroditic), modes of fertilization (outcrossing or selfing), and dispersal (planktonic larvae or internal brooding). Cryptasterina spp. inhabit the upper intertidal of the coast of Queensland and coral islands of the Great Barrier Reef. We found some evidence for positive selection on a GRG in the outcrossing C. pentagona, and we found evidence of loss of gene function in a GRG of the self-fertilizing C. hystera. The modification or loss of gene functionality may be evidence of relaxed selection on some aspects of gamete interaction in C. hystera. In addition to these genes involved in gamete interactions, we also found genes under selection linked to abiotic stress, chromosomal regulation, polyspermy, and egg-laying. We interpret those results as possible evidence that Cryptasterina spp. with different mating systems may have been adapting in divergent ways to oxidative stress or other factors associated with reproduction in the physiologically challenging environment of the high intertidal. Research Highlights Recent speciation between two sea stars was unlikely the result of selection on gamete-recognition genes annotated in this study. Instead, our results point to selection on genes linked to the intertidal environment and reproduction. DOI PubMed
67. Jackson, EW; Wilhelm, RC; Johnson, MR; Lutz, HL; Danforth, I; Gaydos, JK; Hart, MW; Hewson, I. (2021) Diversity of Sea Star-Associated Densoviruses and Transcribed Endogenous Viral Elements of Densovirus Origin.J. Virol. 95 Diversity of Sea Star-Associated Densoviruses and Transcribed Endogenous Viral Elements of Densovirus Origin
densovirus; parvovirus; sea star wasting disease; viral discovery; viral metagenomics; ssDNA viruses
A viral etiology of sea star wasting syndrome (SSWS) was originally explored with virus-sized material challenge experiments, field surveys, and metagenomics, leading to the conclusion that a densovirus is the predominant DNA virus associated with this syndrome and, thus, the most promising viral candidate pathogen. Single-stranded DNA viruses are, however, highly diverse and pervasive among eukaryotic organisms, which we hypothesize may confound the association between densoviruses and SSWS. To test this hypothesis and assess the association of densoviruses with SSWS, we compiled past metagenomic data with new metagenomic-derived viral genomes from sea stars collected from Antarctica, California, Washington, and Alaska. We used 179 publicly available sea star transcriptomes to complement our approaches for densovirus discovery. Lastly, we focus the study on sea star-associated densovirus (SSaDV), the first sea star densovirus discovered, by documenting its biogeography and putative tissue tropism. Transcriptomes contained only endogenized densovirus elements similar to the NS1 gene, while numerous extant densoviral genomes were recovered from viral metagenomes. SSaDV was associated with nearly all tested species from southern California to Alaska, and in contrast to previous work, we show that SSaDV is one genotype among a high diversity of densoviruses present in sea stars across the West Coast of the United States and globally that are commonly associated with grossly normal (i.e., healthy or asymptomatic) animals. The diversity and ubiquity of these viruses in sea stars confound the original hypothesis that one densovirus is the etiological agent of SSWS. IMPORTANCE The primary interest in sea star densoviruses, specifically SSaDV, has been their association with sea star wasting syndrome (SSWS), a disease that has decimated sea star populations across the West Coast of the United States since 2013. The association of SSaDV with SSWS was originally drawn from metagenomic analysis, which was further studied through field surveys using quantitative PCR (qPCR), with the conclusion that it was the most likely viral candidate in the metagenomic data based on its representation in symptomatic sea stars compared to asymptomatic sea stars. We reexamined the original metagenomic data with additional genomic data sets and found that SSaDV was 1 of 10 densoviruses present in the original data set and was no more represented in symptomatic sea stars than in asymptomatic sea stars. Instead, SSaDV appears to be a widespread, generalist virus that exists among a large diversity of densoviruses present in sea star populations. DOI PubMed
66. Guerra, V; Haynes, G; Byrne, M; Yasuda, N; Adachi, S; Nakamura, M; Nakachi, S; Hart, MW. (2019) Nonspecific expression of fertilization genes in the crown-of-thorns Acanthaster cf. solaris: Unexpected evidence of hermaphroditism in a coral reef predator.Mol. Ecol.Nonspecific expression of fertilization genes in the crown-of-thorns Acanthaster cf. solaris: Unexpected evidence of hermaphroditism in a coral reef predator
echinoderm Acanthaster; bindin; outbreaks; reproductive assurance; RNA-seq
The characterization of gene expression in gametes has advanced our understanding of the molecular basis for ecological variation in reproductive success and the evolution of reproductive isolation. These advances are especially significant for ecologically important keystone predators such as the coral-eating crown-of-thorns sea stars (COTS, Acanthaster) which are the most influential predator species in Indo-Pacific coral reef ecosystems and the focus of intensive management efforts. We used RNA-seq and transcriptome assemblies to characterize the expression of genes in mature COTS gonads. We described the sequence and domain organization of eight genes with sex-specific expression and well known functions in fertilization in other echinoderms. We found unexpected expression of genes in one ovary transcriptome that are characteristic of males and sperm, including genes that encode the sperm-specific guanylate cyclase receptor for an egg pheromone, and the sperm acrosomal protein bindin. In a reassembly of previously published RNA-seq data from COTS testes, we found a complementary pattern: strong expression of four genes that are otherwise well known to encode egg-specific fertilization proteins, including the egg receptor for bindin (EBR1) and the acrosome reaction-inducing substance in the egg coat (ARIS1, ARIS2, ARIS3). We also found histological evidence of both eggs and sperm developing in the same gonad in several COTS individuals from a parallel study. These results suggest the occurrence of hermaphrodites, and the potential for reproductive assurance via self-fertilization. Our findings have implications for management of COTS populations, especially in consideration of the large size and massive fecundity of these sea stars. DOI PubMed
65.Hart, MW; Wonham, MJ. (2019) Body size variation in the sexually dimorphic scaphopod Rhabdus rectius (Carpenter, 1864) (Dentaliida: Rhabdidae).Molluscan Res. 39: 205-213 Body size variation in the sexually dimorphic scaphopod Rhabdus rectius (Carpenter, 1864) (Dentaliida: Rhabdidae)
Sexual conflict; SSD; sex ratio; sperm competition; Naticidae
Male-biased sexual size dimorphism typically evolves via sexual selection for larger males that are favoured by choosy females or are more successful in mate competition with other males. Among marine invertebrates that broadcast their gametes into the ocean for fertilisation, this form of sexual size dimorphism is rare because such species lack direct interactions among males or between the sexes. However, the broadcast-spawning tusk shell Rhabdus rectius was recently reported to show strong male-biased sexual size dimorphism. That pattern might imply interesting and undiscovered sexual selection in this species. We found instead that the distribution of body size variation (weight, shell length) was similar between males and females of R. rectius, and mean sizes were not different between the sexes. However, we noted a male-biased sex ratio (similar to 1:1.3) in our large sample of individuals. Many live scaphopods (and several dead shells) showed partial or complete boreholes drilled by predatory gastropods. Boreholes were observed on males and females in similar proportions. We collected scaphopods along with multiple individuals of one likely scaphopod predator, the small moon snail Euspira pallida, and in the lab we observed successful attacks by moon snails on tusk shells. DOI
64. Morgan, CC; Hart, MW. (2019) Molecular evolution of mammalian genes with epistatic interactions in fertilization.BMC Evol. Biol. 19 Molecular evolution of mammalian genes with epistatic interactions in fertilization
Gamete recognition; Zona pellucida; Positive selection; Coevolution; Sexual selection; Innate immunity
BackgroundGenes that encode proteins associated with sperm competition, fertilization, and sexual conflicts of interest are often among the most rapidly evolving parts of animal genomes. One family of sperm-expressed genes (Zp3r, C4bpa) in the mammalian gene cluster called the regulator of complement activation (RCA) encodes proteins that bind eggs and mediate reproductive success, and are therefore expected to show high relative rates of nonsynonymous nucleotide substitution in response to sexual selection in comparison to other genes not involved in gamete binding at fertilization. We tested that working hypothesis by using phylogenetic models of codon evolution to identify episodes of diversifying positive selection. We used a comparative approach to quantify the evidence for episodic diversifying selection acting on RCA genes with known functions in fertilization (and sensitivity to sexual selection), and contrast them with other RCA genes in the same gene family that function in innate immunity (and are not sensitive to sexual selection).ResultsWe expected but did not find evidence for more episodes of positive selection on Zp3r in Glires (the rodents and lagomorphs) or on C4BPA in Primates, in comparison to other paralogous RCA genes in the same taxon, or in comparison to the same orthologous RCA gene in the other taxon. That result was not unique to RCA genes: we also found little evidence for more episodes of diversifying selection on genes that encode selective sperm-binding molecules in the egg coat or zona pellucida (Zp2, Zp3) in comparison to members of the same gene family that encode structural elements of the egg coat (Zp1, Zp4). Similarly, we found little evidence for episodic diversifying selection acting on two other recently discovered genes (Juno, Izumo1) that encode essential molecules for sperm-egg fusion.ConclusionsThese negative results help to illustrate the importance of a comparative context for this type of codon model analysis. The results may also point to other phylogenetic contexts in which the effects of selection acting on these fertilization proteins might be more readily discovered and documented in mammals and other taxa. DOI PubMed
63.Hart, MW; Stover, DA; Guerra, V; Mozaffari, SV; Ober, C; Mugal, CF; Kaj, I. (2018) Positive selection on human gamete-recognition genes.PeerJ 6 Positive selection on human gamete-recognition genes
Filization; Zona pellucida; Linkage disequilibrium; Epistasis; Balancing selection
Coevolution of genes that encode interacting proteins expressed on the surfaces of sperm and eggs can lead to variation in reproductive compatibility between mates and reproductive isolation between members of different species. Previous studies in mice and other mammals have focused in particular on evidence for positive or diversifying selection that shapes the evolution of genes that encode sperm-binding proteins expressed in the egg coat or zona pellucida (ZP). By fitting phylogenetic models of codon evolution to data from the 1000 Genomes Project, we identified candidate sites evolving under diversifying selection in the human genes ZP3 and ZP2. We also identified one candidate site under positive selection in C4BPA, which encodes a repetitive protein similar to the mouse protein ZP3R that is expressed in the sperm head and binds to the ZP at fertilization. Results from several additional analyses that applied population genetic models to the same data were consistent with the hypothesis of selection on those candidate sites leading to coevolution of sperm- and egg-expressed genes. By contrast, we found no candidate sites under selection in a fourth gene (ZP1) that encodes an egg coat structural protein not directly involved in sperm binding. Finally, we found that two of the candidate sites (in C4BPA and ZP2) were correlated with variation in family size and birth rate among Hutterite couples, and those two candidate sites were also in linkage disequilibrium in the same Hutterite study population. All of these lines of evidence are consistent with predictions from a previously proposed hypothesis of balancing selection on epistatic interactions between C4BPA and ZP3 at fertilization that lead to the evolution of co-adapted allele pairs. Such patterns also suggest specific molecular traits that may be associated with both natural reproductive variation and clinical infertility. DOI
62. Wonham, MJ; Hart, MW. (2018) El Nino Range Extensions of Pacific Sand Crab (Emerita analoga) in the Northeastern Pacific.Northwest Sci. 92 El Nino Range Extensions of Pacific Sand Crab (Emerita analoga) in the Northeastern Pacific
decapoda; parasites; Pacific Decadal Oscillation; climate change; citizen science
Many marine species are shifting poleward with global climate change, and many move on a shorter-term basis with periodic climate variations such as the El Nino Southern Oscillation (ENSO) and Pacific Decadal Oscillation (PDO). The Pacific sand crab Emerita analoga (Crustacea: Decapoda: Anomura: Hippidae) is a dominant member of the wave-exposed sandy beach macrofauna of California and Oregon. Its occasional records from Washington to Alaska have been taken to correspond to ENSO events. However, there are surprisingly few scientific or citizen-science records of its presence in this region. We report the first published record in over 30 years of E. analoga in British Columbia, and summarize historical published and unpublished records. Because this species is conspicuous and readily identifiable, we suggest the general absence of its published, institutional, and citizen-science records coincident with most historical ENSO events may be due to a lack of reporting. In California, E. analoga accumulates harmful algal bloom toxins, is consumed by crabs, fish, birds, and marine and terrestrial mammals, and serves as the intermediate host for a variety of parasites, including the peritonitis-inducing acanthocephalan implicated in sea otter mortalities. As coastal waters warm, we predict that E. analoga will colonize sandy beaches north of its current range, where it may serve as an abundant prey item and as a vector for the trophic transfer of toxins and parasites. Detecting changes in its abundance will require the continued observation and reporting of its records, which we encourage in academic, government, and citizen-science venues.
61.Hart, MW; Guerra, V. (2017) Finding genes and lineages under selection in speciation.Mol. Ecol. 26: 3587-3590 Finding genes and lineages under selection in speciation
echinoderm fertilization; positive selection; RNAseq; speciation
What are the genes and traits that respond to selection and cause prezygotic reproductive isolation between species? This question has been hard to answer because genomes are large, the targets of selection may be scattered across the genome (Sabeti et al., 2007) and different genes may respond to the same selective pressure in different populations (Scheinfeldt et al., 2012). In this issue of Molecular Ecology, Weber et al. (2017) use a clever comparative approach and leading-edge transcriptomic methods to identify the species and genes under positive selection for divergence between brittle stars (the echinoderm class Ophiuroidea) in the Ophioderma longicauda species complex. They found convincing evidence of positive or diversifying selection acting on two genes encoding ion channels that form part of the signal transduction cascade within the sperm in response to pheromones. Evidence for selection was concentrated in genes from one species (called C5, with internal fertilization and female parental care of brooded juveniles and not in the other species (called C3, with more conventional broadcast spawning and planktonic development of embryos and larvae). That analysis greatly extends the range of taxa, life history traits and molecules that are associated with positive selection in speciation. It also illustrates some of the current limitations on the application of RNAseq methods in the search for the targets of selection in nonmodel organisms like brittle stars. From both points of view, the new work by Weber et al. (2017) has important implications for our understanding of speciation in the ocean. DOI
60. Puritz, JB; Keever, CC; Addison, JA; Barbosa, SS; Byrne, M; Hart, MW; Grosberg, RK; Toonen, RJ. (2017) Life-history predicts past and present population connectivity in two sympatric sea stars.Ecol. Evol. 7: 3916-3930 Life-history predicts past and present population connectivity in two sympatric sea stars
gene flow; phylogeography; population genetics; population structure
Life-history traits, especially the mode and duration of larval development, are expected to strongly influence the population connectivity and phylogeography of marine species. Comparative analysis of sympatric, closely related species with differing life histories provides the opportunity to specifically investigate these mechanisms of evolution but have been equivocal in this regard. Here, we sample two sympatric sea stars across the same geographic range in temperate waters of Australia. Using a combination of mitochondrial DNA sequences, nuclear DNA sequences, and microsatellite genotypes, we show that the benthic-developing sea star, Parvulastra exigua, has lower levels of within- and among-population genetic diversity, more inferred genetic clusters, and higher levels of hierarchical and pairwise population structure than Meridiastra calcar, a species with planktonic development. While both species have populations that have diverged since the middle of the second glacial period of the Pleistocene, most P.exigua populations have origins after the last glacial maxima (LGM), whereas most M.calcar populations diverged long before the LGM. Our results indicate that phylogenetic patterns of these two species are consistent with predicted dispersal abilities; the benthic-developing P.exigua shows a pattern of extirpation during the LGM with subsequent recolonization, whereas the planktonic-developing M.calcar shows a pattern of persistence and isolation during the LGM with subsequent post-Pleistocene introgression. DOI
59. Patino, S; Keever, CC; Sunday, JM; Popovic, I; Byrne, M; Hart, MW. (2016) Sperm Bindin Divergence under Sexual Selection and Concerted Evolution in Sea Stars.Molecular Biology and Evolution 33: 1988-2001 Sperm Bindin Divergence under Sexual Selection and Concerted Evolution in Sea Stars
sexual selection; positive selection; gamete recognition; fertilization; speciation
Selection associated with competition among males or sexual conflict between mates can create positive selection for high rates of molecular evolution of gamete recognition genes and lead to reproductive isolation between species. We analyzed coding sequence and repetitive domain variation in the gene encoding the sperm acrosomal protein bindin in 13 diverse sea star species. We found that bindin has a conserved coding sequence domain structure in all 13 species, with several repeated motifs in a large central region that is similar among all sea stars in organization but highly divergent among genera in nucleotide and predicted amino acid sequence. More bindin codons and lineages showed positive selection for high relative rates of amino acid substitution in genera with gonochoric outcrossing adults (and greater expected strength of sexual selection) than in selfing hermaphrodites. That difference is consistent with the expectation that selfing (a highly derivedmating system) maymoderate the strength of sexual selection and limit the accumulation of bindin amino acid differences. The results implicate both positive selection on single codons and concerted evolution within the repetitive region in bindin divergence, and suggest that both single amino acid differences and repeat differences may affect sperm-egg binding and reproductive compatibility. DOI
58.Hart, MW. (2014) Models of Selection, Isolation, and Gene Flow in Speciation.Biological Bulletin 227: 133-145 Models of Selection, Isolation, and Gene Flow in Speciation
Many marine ecologists aspire to use genetic data to understand how selection and demographic history shape the evolution of diverging populations as they become reproductively isolated species. I propose combining two types of genetic analysis focused on this key early stage of the speciation process to identify the selective agents directly responsible for population divergence. Isolation-with-migration (IM) models can be used to characterize reproductive isolation between populations (low gene flow), while codon models can be used to characterize selection for population differences at the molecular level (especially positive selection for high rates of amino acid substitution). Accessible transcriptome sequencing methods can generate the large quantities of data needed for both types of analysis. I highlight recent examples (including our work on fertilization genes in sea stars) in which this confluence of interest, models, and data has led to taxonomically broad advances in understanding marine speciation at the molecular level. I also highlight new models that incorporate both demography and selection: simulations based on these theoretical advances suggest that polymorphisms shared among individuals (a key source of information in IM models) may lead to false-positive evidence of selection (in codon models), especially during the early stages of population divergence and speciation that are most in need of study. The false-positive problem may be resolved through a combination of model improvements plus experiments that document the phenotypic and fitness effects of specific polymorphisms for which codon models and IM models indicate selection and reproductive isolation (such as genes that mediate sperm-egg compatibility at fertilization). PubMed
57.Hart, MW; Sunday, JM; Popovic, I; Learning, KJ; Konrad, CM. (2014) INCIPIENT SPECIATION OF SEA STAR POPULATIONS BY ADAPTIVE GAMETE RECOGNITION COEVOLUTION.Evolution 68: 1294-1305 INCIPIENT SPECIATION OF SEA STAR POPULATIONS BY ADAPTIVE GAMETE RECOGNITION COEVOLUTION
bindin; coevolution; fertilization; sexual conflict; sexual selection
Reproductive isolationthe key event in speciationcan evolve when sexual conflict causes selection favoring different combinations of male and female adaptations in different populations. Likely targets of such selection include genes that encode proteins on the surfaces of sperm and eggs, but no previous study has demonstrated intraspecific coevolution of interacting gamete recognition genes under selection. Here, we show that selection drives coevolution between an egg receptor for sperm (OBi1) and a sperm acrosomal protein (bindin) in diverging populations of a sea star (Patiria miniata). We found positive selection on OBi1 in an exon encoding part of its predicted substrate-binding protein domain, the ligand for which is found in bindin. Gene flow was zero for the parts of bindin and OBi1 in which selection for high rates of amino acid substitution was detected; higher gene flow for other parts of the genome indicated selection against immigrant alleles at bindin and OBi1. Populations differed in allele frequencies at two key positively selected sites (one in each gene), and differences at those sites predicted fertilization rate variation among male-female pairs. These patterns suggest adaptively evolving loci that influence reproductive isolation between populations. DOI
56. Popovic, I; Marko, PB; Wares, JP; Hart, MW. (2014) Selection and demographic history shape the molecular evolution of the gamete compatibility protein bindin in Pisaster sea stars.Ecology and Evolution 4: 1567-1588 Selection and demographic history shape the molecular evolution of the gamete compatibility protein bindin in Pisaster sea stars
Bindin; concerted evolution; gamete recognition; positive selection; sexual conflict
Reproductive compatibility proteins have been shown to evolve rapidly under positive selection leading to reproductive isolation, despite the potential homogenizing effects of gene flow. This process has been implicated in both primary divergence among conspecific populations and reinforcement during secondary contact; however, these two selective regimes can be difficult to discriminate from each other. Here, we describe the gene that encodes the gamete compatibility protein bindin for three sea star species in the genus Pisaster. First, we compare the full-length bindin-coding sequence among all three species and analyze the evolutionary relationships between the repetitive domains of the variable second bindin exon. The comparison suggests that concerted evolution of repetitive domains has an effect on bindin divergence among species and bindin variation within species. Second, we characterize population variation in the second bindin exon of two species: We show that positive selection acts on bindin variation in Pisaster ochraceus but not in Pisaster brevispinus, which is consistent with higher polyspermy risk in P.ochraceus. Third, we show that there is no significant genetic differentiation among populations and no apparent effect of sympatry with congeners that would suggest selection based on reinforcement. Fourth, we combine bindin and cytochrome c oxidase 1 data in isolation-with-migration models to estimate gene flow parameter values and explore the historical demographic context of our positive selection results. Our findings suggest that positive selection on bindin divergence among P.ochraceus alleles can be accounted for in part by relatively recent northward population expansions that may be coupled with the potential homogenizing effects of concerted evolution. DOI
55. Sunday, JM; Popovic, I; Palen, WJ; Foreman, MGG; Hart, MW. (2014) Ocean circulation model predicts high genetic structure observed in a long-lived pelagic developer.Molecular Ecology 23: 5036-5047 Ocean circulation model predicts high genetic structure observed in a long-lived pelagic developer
larval dispersal; marine connectivity; oceanographic circulation model; population genetics
Understanding the movement of genes and individuals across marine seascapes is a long-standing challenge in marine ecology and can inform our understanding of local adaptation, the persistence and movement of populations, and the spatial scale of effective management. Patterns of gene flow in the ocean are often inferred based on population genetic analyses coupled with knowledge of species' dispersive life histories. However, genetic structure is the result of time-integrated processes and may not capture present-day connectivity between populations. Here, we use a high-resolution oceanographic circulation model to predict larval dispersal along the complex coastline of western Canada that includes the transition between two well-studied zoogeographic provinces. We simulate dispersal in a benthic sea star with a 6-10week pelagic larval phase and test predictions of this model against previously observed genetic structure including a strong phylogeographic break within the zoogeographical transition zone. We also test predictions with new genetic sampling in a site within the phylogeographic break. We find that the coupled genetic and circulation model predicts the high degree of genetic structure observed in this species, despite its long pelagic duration. High genetic structure on this complex coastline can thus be explained through ocean circulation patterns, which tend to retain passive larvae within 20-50km of their parents, suggesting a necessity for close-knit design of Marine Protected Area networks. DOI PubMed
54.Hart, MW. (2013) Structure and evolution of the sea star egg receptor for sperm bindin.Molecular Ecology 22: 2143-2156 Structure and evolution of the sea star egg receptor for sperm bindin
POSITIVE DARWINIAN SELECTION; GAMETE-RECOGNITION; PHYLOGENETIC ANALYSIS; MAXIMUM-LIKELIHOOD; GENETIC ALGORITHM; NEXT-GENERATION; PROTEIN; URCHINS; LYSIN; POPULATION
Selection on coevolving sperm- and egg-recognition molecules is a potent engine of population divergence leading to reproductive isolation and speciation. The study of receptorligand pairs can reveal co-evolution of male- and female-expressed genes or differences between their evolution in response to selective factors such as sperm competition and sexual conflict. Phylogeographical studies of these patterns have been limited by targeted gene methods that favour short protein-coding sequences amplifiable by PCR. Here, I use high-throughput transcriptomic methods to characterize the structure and divergence of full-length coding sequences for the gene encoding the protein component of a large complex egg surface glycopeptide receptor for the sperm acrosomal protein bindin from the sea star Patiria miniata. I used a simple but effective method for resolving nucleotide polymorphisms into haplotypes for phylogeny-based analyses of selection. The protein domain organization of sea star egg bindin receptor (EBR1) was similar to sea urchins and included a pair of protein-recognition domains plus a series of tandem repeat domains of two types. Two populations separated by a well-characterized phylogeographical break included lineages of EBR1 alleles under positive selection at several codons (similar to selection on sperm bindin in the same populations). However, these populations shared the same alleles that were under selection for amino acid differences at multiple codons (unlike the pattern of selection for population divergence in sperm bindin). The significance of positively selected EBR1 domains and alleles could be tested in functional analyses of fertilization rates associated with EBR1 (and bindin) polymorphisms. DOI
53.Hart, MW; Foster, A. (2013) Highly expressed genes in gonads of the bat star Patiria miniata: gene ontology, expression differences, and gamete recognition loci.Invertebrate Biology 132: 241-250 Highly expressed genes in gonads of the bat star Patiria miniata: gene ontology, expression differences, and gamete recognition loci
URCHIN EGG RECEPTOR; SEA-URCHIN; REPRODUCTIVE PROTEINS; POSITIVE SELECTION; NEXT-GENERATION; SEQUENCING DATA; SPERM BINDIN; EVOLUTION; FERTILIZATION; TRANSCRIPTOME
Evolutionary analysis of mating systems in broadcast-spawning marine animals and plants has focused on sperm- and egg-surface proteins and glycopeptides that mediate reproductive interactions at different stages of gamete recognition. Improved understanding of the ecology and evolution of such interactions depends on extending our knowledge to multiple genes expressed in both sperm and eggs of diverse taxonomic groups with different modes of fertilization. Here, we use readily accessible next-generation sequencing methods and desktop bioinformatics to characterize the repertoire of highly expressed genes in testes and ovaries of the asterinid sea star Patiria miniata, including gene ontology annotations for male- and female-expressed molecules, and descriptions of two genes that encode egg-surface molecules involved in fertilization that have not previously been studied in sea stars. The results are used to contrast expression differences between the testis and ovary, and to develop hypotheses of gamete-specific expression. We also explore differences in ovary gene expression among multiple females from northern and southern populations that show nucleotide differentiation at many non-expressed loci and at a gamete recognition locus. DOI
52. Sunday, JM; Hart, MW. (2013) Sea star populations diverge by positive selection at a sperm-egg compatibility locus.Ecology and Evolution 3: 640-654 Sea star populations diverge by positive selection at a sperm-egg compatibility locus
GENETIC DIFFERENTIATION MEASURE; GAMETE-RECOGNITION; RAPID EVOLUTION; SEXUAL CONFLICT; STRONGYLOCENTROTUS-FRANCISCANUS; CHARACTER DISPLACEMENT; REPRODUCTIVE PROTEINS; PHYLOGENETIC ANALYSIS; DARWINIAN SELECTION; GENUS ECHINOMETRA
Fertilization proteins of marine broadcast spawning species often show signals of positive selection. Among geographically isolated populations, positive selection within populations can lead to differences between them, and may result in reproductive isolation upon secondary contact. Here, we test for positive selection in the reproductive compatibility locus, bindin, in two populations of a sea star on either side of a phylogeographic break. We find evidence for positive selection at codon sites in both populations, which are under neutral or purifying selection in the reciprocal population. The signal of positive selection is stronger and more robust in the population where effective population size is larger and bindin diversity is greater. In addition, we find high variation in coding sequence length caused by large indels at two repetitive domains within the gene, with greater length diversity in the larger population. These findings provide evidence of population-divergent positive selection in a fertilization compatibility locus, and suggest that sexual selection can lead to reproductive divergence between conspecific marine populations. DOI
51.Hart, MW. (2012) New sea urchin phylogeography reveals latitudinal shifts associated with speciation.Molecular Ecology 21: 26-27 New sea urchin phylogeography reveals latitudinal shifts associated with speciation
allopatry; echinoderms; ecological speciation; hybridization; phylogeography
Where do new species arise? When do they form and how do they diverge from a common ancestor? A new comprehensive study of Arbacia sea urchins provides surprising answers to these questions. By combining mtDNA phylogeographic markers with a nuclear locus (encoding the sperm acrosomal protein bindin) known to be susceptible to high rates of adaptive codon evolution, Lessios (2012) show that new species and lineages arose relatively recently, most often in association with latitudinal shifts between the temperate zones and the tropics, and in one case, in association with a significant geological barrier to gene flow (the rise of the Isthmus of Panama). In addition to the where and when of Arbacia speciation, these new data resolve an important question about whoArbacia species are by revealing extensive allele sharing at both loci between a pair of broadly sympatric nominal species (that should perhaps be considered a single taxon). HowArbacia diverge from each other is less easily resolved: there is no evidence for reinforcement (via selection on bindin) as an important source of divergence between nominal species, and there are few other data to decide among the alternative hypotheses to explain Arbacia speciation. DOI
50.Hart, MW. (2012) NEXT-GENERATION STUDIES OF MATING SYSTEM EVOLUTION.Evolution 66: 1675-1680 NEXT-GENERATION STUDIES OF MATING SYSTEM EVOLUTION
ARIS; asterosap; bindin; fertilization; guanylate cyclase; lysin
The specificity of mate selection can vary from wantonly indiscriminate to extraordinarily choosy, and depends in large part on molecules expressed on the surfaces of sperm and eggs. Understanding the evolution of this specificity of gamete recognition leads to important insights into the evolution of reproductive isolation and speciation. One productive area of research has focused on genes that encode gamete recognition proteins in broadcast-spawning marine invertebrates. These gene products are relatively accessible to biochemical and cellular analyses of expression and function, and they mediate almost all of the elements of mate selection and specificity between males and females of such species. However, genetic analyses of their evolution are currently limited to a few combinations of molecules and taxa, and may miss the broader view of adaptive responses to selection on mating specificity across many genes and many types of mating systems. A transcriptomic study shows how next-generation sequencing methods and analyses could relatively easily broaden such studies to more clades, deepen those studies to include more of the interacting molecular parts that mediate gamete recognition, and eventually lead to a more complete understanding of the molecular basis for mating system variation and its evolutionary response to selection. DOI
49.Hart, MW; Popovic, I; Emlet, RB. (2012) LOW RATES OF BINDIN CODON EVOLUTION IN LECITHOTROPHIC HELIOCIDARIS SEA URCHINS.Evolution 66: 1709-1721 LOW RATES OF BINDIN CODON EVOLUTION IN LECITHOTROPHIC HELIOCIDARIS SEA URCHINS
Bindin; fertilization; polyspermy; sexual selection
Life-history variables including egg size affect the evolutionary response to sexual selection in broadcast-spawning sea urchins and other marine animals. Such responses include high or low rates of codon evolution at gamete recognition loci that encode sperm- and egg-surface peptides. Strong positive selection on such loci affects intraspecific mating success and interspecific reproductive divergence (and may play a role in speciation). Here, we analyze adaptive codon evolution in the sperm acrosomal protein bindin from a brooding sea urchin (Heliocidaris bajulus, with large eggs and nonfeeding or lecithotrophic larval development) and compare our results to previously published data for two closely related congeners. Purifying selection and low relative rates of bindin nonsynonymous substitution in H. bajulus were significantly different from selectively neutral bindin evolution in H. erythrogramma despite similar large egg size in those two species, but were similar to the background rate of nonsynonymous bindin substitution for other closely related sea urchins (including H. tuberculata, all with small egg size and feeding planktonic larval development). Bindin evolution is not driven by egg size variation among Heliocidaris species, but may be more consistent with an alternative mechanism based on the effects of high or low spatial density of conspecific mates. DOI
48. Marko, PB; Hart, MW. (2012) Retrospective coalescent methods and the reconstruction of metapopulation histories in the sea.Evolutionary Ecology 26: 291-315 Retrospective coalescent methods and the reconstruction of metapopulation histories in the sea
Connectivity; Extinction; F-ST; Island model; Gene flow; Marine ecology; Mitochondrial DNA; Population genetics; Recolonization
Phylogeographic analyses are a key interface between ecological and evolutionary ways of knowing because such analyses integrate the cumulative effects of demographic (ecological) processes over geological (evolutionary) time scales. Newly developed coalescent methods allow evolutionary ecologists to overcome some limitations associated with inferring population history from classic methods such as Wright's F (ST). Here we briefly contrast classic and coalescent methods for looking backward in time through a population genetic lens, focusing on the key advantages of the isolation-with-migration (IM) class of coalescent methods for distinguishing ancient connectedness from actual recurrent contemporary gene flow as causes of genetic similarity or differentiation among populations. Making this critical distinction can lead to the discovery of otherwise obscured histories underlying conventional patterns of spatial variation. We illustrate the importance of these insights using analyses of Pacific fishes, snails, and sea stars in which population sizes and divergence times are more important than rates of contemporary gene flow as determinants of population genetic differentiation. We then extend the IM method to genetic data from two model metapopulation species (California abalone, Australian damselfish). The analyses show the potential use of non-equilibrium IM methods for differentiating among metapopulation models that make different predictions about population parameters and have different implications for the design of marine protected areas and other conservation goals. At face value, the results largely rule out classic metapopulation dynamics (dominated by extinction and colonization rather than connectivity via ongoing recurrent gene flow) but, at the same time, do not strongly support a modern marine metapopulation dynamic (ecologically significant connectivity between demes). However, the results also highlight the need for much more data (i.e., loci) sampled on different spatial scales in order to determine whether metapopulation dynamics might exist on smaller scales than are typically sampled by most phylogeographers and landscape geneticists. DOI
46.Hart, MW. (2011) THE SPECIES CONCEPT AS AN EMERGENT PROPERTY OF POPULATION BIOLOGY.Evolution 65 THE SPECIES CONCEPT AS AN EMERGENT PROPERTY OF POPULATION BIOLOGY
Metapopulation lineage; speciation; species delimitation; unified species concept
Resurgent interest in the genetics of population divergence and speciation coincides with recent critical evaluation of species concepts and proposals for species delimitation. An important result of these parallel trends is a slight but important conceptual shift in focus away from species diagnoses based on prior species concepts or definitions, and toward analyses of the processes acting on lineages of metapopulations that eventually lead to differences recognizable as species taxa. An advantage of this approach is that it identifies quantitative metapopulation differences in continuous variables, rather than discrete entities that do or do not conform to a prior species concept, and species taxa are recognized as an emergent property of population-level processes. The tension between species concepts and diagnosis versus emergent recognition of species taxa is at least as old as Darwin, and is unlikely to be resolved soon in favor of either view, because the products of both approaches (discrete utilitarian taxon names for species, process-based understanding of the origins of differentiated metapopulations) continue to have important applications. DOI
45.Hart, MW; Abt, CHJ; Emlet, RB. (2011) Molecular phylogeny of echinometrid sea urchins: more species of Heliocidaris with derived modes of reproduction.Invertebrate Biology 130: 175-185 Molecular phylogeny of echinometrid sea urchins: more species of Heliocidaris with derived modes of reproduction
Pachycentrotus; bindin; COI; 16S
Pachechinus bajulus is an endemic Australian sea urchin with an unusual mode of brooded larval development. We used mitochondrial and nuclear gene sequences to estimate the phylogenetic relationships among Pachechinus and other Echinometridae, including well-studied species of Heliocidaris with planktonic development. We found strong evidence for the planktotrophic species Heliocidaris tuberculata as the sister group to a clade of three closely related species in which development is known (Heliocidaris erythrogramma, P. bajulus) or suspected (Pachechinus australiae) to be lecithotrophic. Clade support values and likelihood ratio tests rejected monophyly of Heliocidaris species. The sister group to H. erythrogramma is most likely the two Pachechinus species. We resolve the paraphyly problem by reassigning the Pachechinus species to the genus Heliocidaris (the senior synonym), which has six extant species including Heliocidaris australiae and Heliocidaris bajulus. The phylogeny has potentially important implications for comparative studies of developmental morphology and genetics that have assumed a close sister-group relationship between H. erythrogramma and H. tuberculata, and highlights the need for such data from H. bajulus and other Heliocidaris species. DOI
44. Marko, PB; Hart, MW. (2011) The complex analytical landscape of gene flow inference.Trends in Ecology & Evolution 26: 448-456 The complex analytical landscape of gene flow inference
Gene flow estimation is essential for characterizing local adaptation, speciation potential and connectivity among threatened populations. New model-based population genetic methods can resolve complex demographic histories, but many studies in fields such as landscape genetics continue to rely on simple rules of thumb focused on gene flow to explain patterns of spatial differentiation. Here, we show how methods that use gene genealogies can reveal cryptic demographic histories and provide better estimates of gene flow with other parameters that contribute to genetic variation across landscapes and seascapes. We advocate for the expanded use and development of methods that consider spatial differentiation as the product of multiple forces interacting over time, and caution against a routine reliance on post-hoc gene flow interpretations. DOI
43. Sunday, JM; Crim, RN; Harley, CDG; Hart, MW. (2011) Quantifying Rates of Evolutionary Adaptation in Response to Ocean Acidification.PLOS One 6 Quantifying Rates of Evolutionary Adaptation in Response to Ocean Acidification
The global acidification of the earth's oceans is predicted to impact biodiversity via physiological effects impacting growth, survival, reproduction, and immunology, leading to changes in species abundances and global distributions. However, the degree to which these changes will play out critically depends on the evolutionary rate at which populations will respond to natural selection imposed by ocean acidification, which remains largely unquantified. Here we measure the potential for an evolutionary response to ocean acidification in larval development rate in two coastal invertebrates using a full-factorial breeding design. We show that the sea urchin species Strongylocentrotus franciscanus has vastly greater levels of phenotypic and genetic variation for larval size in future CO(2) conditions compared to the mussel species Mytilus trossulus. Using these measures we demonstrate that S. franciscanus may have faster evolutionary responses within 50 years of the onset of predicted year-2100 CO(2) conditions despite having lower population turnover rates. Our comparisons suggest that information on genetic variation, phenotypic variation, and key demographic parameters, may lend valuable insight into relative evolutionary potentials across a large number of species. DOI
41.Hart, MW; Marko, PB. (2010) It's About Time: Divergence, Demography, and the Evolution of Developmental Modes in Marine Invertebrates.Integrative and Comparative Biology 50: 643-661 It's About Time: Divergence, Demography, and the Evolution of Developmental Modes in Marine Invertebrates
Differences in larval developmental mode are predicted to affect ecological and evolutionary processes ranging from gene flow and population bottlenecks to rates of population recovery from anthropogenic disturbance and capacity for local adaptation. The most powerful tests of these predictions use comparisons among species to ask how phylogeographic patterns are correlated with the evolution and loss of prolonged planktonic larval development. An important and largely untested assumption of these studies is that interspecific differences in population genetic structure are mainly caused by differences in dispersal and gene flow (rather than by differences in divergence times among populations or changes in effective population sizes), and that species with similar patterns of spatial genetic variation have similar underlying temporal demographic histories. Teasing apart these temporal and spatial patterns is important for understanding the causes and consequences of evolutionary changes in larval developmental mode. New analytical methods that use the coalescent history of allelic diversity can reveal these temporal patterns, test the strength of traditional population-genetic explanations for variation in spatial structure based on differences in dispersal, and identify strongly supported alternative explanations for spatial structure based on demographic history rather than on gene flow alone. We briefly review some of these recent analytical developments, and show their potential for refining ideas about the correspondence between the evolution of larval developmental mode, population demographic history, and spatial genetic variation. DOI
40. McGovern, TM; Keever, CC; Saski, CA; Hart, MW; Marko, PB. (2010) Divergence genetics analysis reveals historical population genetic processes leading to contrasting phylogeographic patterns in co-distributed species.Molecular Ecology 19: 5043-5060 Divergence genetics analysis reveals historical population genetic processes leading to contrasting phylogeographic patterns in co-distributed species
ancestral polymorphism; biogeography; coalescence; divergence time; gene flow; glaciation; larval development; pseudo-congruence; vicariance
Coalescent samplers are computational time machines for inferring the historical demographic genetic processes that have given rise to observable patterns of spatial genetic variation among contemporary populations. We have used traditional characterizations of population structure and coalescent-based inferences about demographic processes to reconstruct the population histories of two co-distributed marine species, the frilled dog whelk, Nucella lamellosa, and the bat star, Patiria miniata. Analyses of population structure were consistent with previous work in both species except that additional samples of N. lamellosa showed a larger regional genetic break on Vancouver Island (VI) rather than between the southern Alexander Archipelago as in P. miniata. Our understanding of the causes, rather than just the patterns, of spatial genetic variation was dramatically improved by coalescent analyses that emphasized variation in population divergence times. Overall, gene flow was greater in bat stars (planktonic development) than snails (benthic development) but spatially homogeneous within species. In both species, these large phylogeographic breaks corresponded to relatively ancient divergence times between populations rather than regionally restricted gene flow. Although only N. lamellosa shows a large break on VI, population separation times on VI are congruent between species, suggesting a similar response to late Pleistocene ice sheet expansion. The absence of a phylogeographic break in P. miniata on VI can be attributed to greater gene flow and larger effective population size in this species. Such insights put the relative significance of gene flow into a more comprehensive historical biogeographic context and have important implications for conservation and landscape genetic studies that emphasize the role of contemporary gene flow and connectivity in shaping patterns of population differentiation. DOI
39.Hart, MW; Grosberg, RK. (2009) Caterpillars did not evolve from onychophorans by hybridogenesis.Proceedings of the National Academy of Sciences of the United States of America 106: 19906-19909 Caterpillars did not evolve from onychophorans by hybridogenesis
MARINE-INVERTEBRATES; LIFE-CYCLES; GENOME; LARVAE; EVOLUTION; ADAPTATION; ORIGINS
The evolution and loss of distinctive larval forms in animal life cycles have produced complex patterns of similarity and difference among life-history stages and major animal lineages. One example of this similarity is the morphological forms of Onychophora (velvet worms) and the caterpillar-like larvae of some insects. Williamson [(2009) Proc Natl Acad Sci USA 106: 15786-15790] has made the astonishing and unfounded claim that the ancestors of the velvet worms directly gave rise to insect caterpillars via hybridization and that evidence of this ancient "larval transfer'' could be found in comparisons among the genomes of extant onychophorans, insects with larvae, and insects without larvae. Williamson has made a series of predictions arising from his hypothesis and urged genomicists to test them. Here, we use data already in the literature to show these predictions to be false. Hybridogenesis between distantly related animals does not explain patterns of morphological and life-history evolution in general, and the genes and genomes of animals provide strong evidence against hybridization or larval transfer between a velvet worm and an insect in particular. DOI
38. Keever, CC; Sunday, J; Puritz, JB; Addison, JA; Toonen, RJ; Grosberg, RK; Hart, MW. (2009) DISCORDANT DISTRIBUTION OF POPULATIONS AND GENETIC VARIATION IN A SEA STAR WITH HIGH DISPERSAL POTENTIAL.Evolution 63: 3214-3227 DISCORDANT DISTRIBUTION OF POPULATIONS AND GENETIC VARIATION IN A SEA STAR WITH HIGH DISPERSAL POTENTIAL
LIFE-HISTORY; MAXIMUM-LIKELIHOOD; LARVAL DISPERSAL; MARINE FISH; CONTRASTING PATTERNS; INTEGRATED SOFTWARE; SEQUENCE ALIGNMENT; STATISTICAL TESTS; BRITISH-COLUMBIA; SPECIES COMPLEX
Patiria miniata, a broadcast-spawning sea star species with high dispersal potential, has a geographic range in the intertidal zone of the northeast Pacific Ocean from Alaska to California that is characterized by a large range gap in Washington and Oregon. We analyzed spatial genetic variation across the P. miniata range using multilocus sequence data (mtDNA, nuclear introns) and multilocus genotype data (microsatellites). We found a strong phylogeographic break at Queen Charlotte Sound in British Columbia that was not in the location predicted by the geographical distribution of the populations. However, this population genetic discontinuity does correspond to previously described phylogeographic breaks in other species. Northern populations from Alaska and Haida Gwaii were strongly differentiated from all southern populations from Vancouver Island and California. Populations from Vancouver Island and California were undifferentiated with evidence of high gene flow or very recent separation across the range disjunction between them. The surprising and discordant spatial distribution of populations and alleles suggests that historical vicariance (possibly caused by glaciations) and contemporary dispersal barriers (possibly caused by oceanographic conditions) both shape population genetic structure in this species. DOI
36. Patino, S; Aagaard, JE; MacCoss, MJ; Swanson, WJ; Hart, MW. (2009) Bindin from a sea star.Evolution & Development 11: 376-381 Bindin from a sea star
URCHIN SPERM BINDIN; ADAPTIVE EVOLUTION; REPRODUCTIVE PROTEINS; MOLECULAR EVOLUTION; POSITIVE SELECTION; DIVERGENCE TIMES; RAPID EVOLUTION; EGG RECEPTOR; RECOGNITION; SPECIATION
The genetic basis for the evolution of development includes genes that encode proteins expressed on the surfaces of sperm and eggs. Previous studies of the sperm acrosomal protein bindin have helped to characterize the adaptive evolution of gamete compatibility and speciation in sea urchins. The absence of evidence for bindin expression in taxa other than the Echinoidea has limited such studies to sea urchins, and led to the suggestion that bindin might be a sea urchin-specific molecule. Here we characterize the gene that encodes bindin in a broadcast-spawning asterinid sea star (Patiria miniata). We describe the sequence and domain structure of a full-length bindin cDNA and its single intron. In comparison with sea urchins, P. miniata bindin is larger but the two molecules share several general features of their domain structure and some sequence features of two domains. Our results extend the known evolutionary history of bindin from the Mesozoic (among the crown group sea urchins) into the early Paleozoic (and the common ancestor of eleutherozoans), and present new opportunities for understanding the role of bindin molecular evolution in sexual selection, life history evolution, and speciation among sea stars. DOI
35. Sunday, J; Raeburn, L; Stewart, H; Hart, MW. (2009) Allelic inheritance in naturally occurring parthenogenetic offspring of the gonochoric sea star Patiria miniata.Invertebrate Biology 128: 276-282 Allelic inheritance in naturally occurring parthenogenetic offspring of the gonochoric sea star Patiria miniata
POLAR BODY EXTRUSION; ARTIFICIAL PARTHENOGENESIS; EGGS; OOCYTES; REPRODUCTION; ACTIVATION; EVOLUTION; LARVAL; 1-METHYLADENINE; HYBRIDIZATION
In laboratory studies of fertilization using the gonochoric broadcast-spawning asterinid sea star Patiria miniata, we found many cases in which some mature eggs spawned by females formed cleavage-stage embryos and feeding bipinnaria larvae without fertilization by sperm. Segregation of maternal microsatellite alleles among the parthenogenetic offspring of known heterozygous females was consistent with several specific modes of asexual reproduction, including polar body suppression. Cryptic outcrossing by sperm contamination was ruled out by the failure to observe non-maternal alleles. The potential for asexual reproduction by the normally outcrossing members of P. miniata may suggest a shared propensity for asexuality among asterinid species from several clades in which isolated adults can produce offspring without outcrossing. DOI
33. Keever, CC; Hart, MW. (2008) Something for nothing? Reconstruction of ancestral character states in asterinid sea star development.Evolution & Development 10: 62-73 Something for nothing? Reconstruction of ancestral character states in asterinid sea star development
Traits from early development mapped onto phylogenetic trees can potentially offer insight into the evolutionary history of development by inferring the states of those characters among ancestors at nodes in the phylogeny. A key and often-overlooked aspect of such mapping is the underlying model of character evolution. Without a well-supported and realistic model ("nothing"), character mapping of ancestral traits onto phylogenetic trees might often return results ("something") that lack a sound basis. Here we reconsider a challenging case study in this area of evolutionary developmental biology: the inference of ancestral states for ecological and morphological characters in the reproduction and larval development of asterinid sea stars. We apply improved analytical methods to an expanded set of asterinid phylogenetic data and developmental character states. This analysis shows that the new methods might generally offer some independent insight into choice of a model of character evolution, but that in the specific case of asterinid sea stars the quantitative features of the model (especially the relative probabilities of different directions of change) have an important effect on the results. We suggest caution in applying ancestral state reconstructions in the absence of an independently corroborated model of character evolution, and highlight the need for such modeling in evolutionary developmental biology.
32. Keever, CC; Sunday, J; Wood, C; Byrne, M; Hart, MW. (2008) Discovery and Cross-Amplification of Microsatellite Polymorphisms in Asterinid Sea Stars.Biological Bulletin 215: 164-172 Discovery and Cross-Amplification of Microsatellite Polymorphisms in Asterinid Sea Stars
Variation in tandem repeats of two- to six-base nucleotide motifs (microsatellites) can be used to obtain inexpensive and highly informative multi-locus data on population geneticsWe developed and tested a large set of cross-amplifiable sea star (Asterinidae) microsatellite markers from a mixed pool of genomic DNA from eight species. We describe cloned sequences, primers, and PCR conditions, and characterize population-level variation for some species and markers. A few clones containing microsatellites showed considerable similarity to sequences (including genes of known function) in other sea stars and in sea urchins (from the Strongylocentrotus purpuratus complete genome). The pooled genomic DNA method was an efficient way to sample microsatellites from many species: we cloned 2-10 microsatellites from each of eight species, and most could be cross-amplified in 1-7 other species. At 12 loci in two species, we found 1-10 alleles per microsatellite, with a broad range of inbreeding coefficients. Measures of polymorphism were negatively correlated with the extent of cross-amplification.
31. Sunday, J; Raeburn, L; Hart, MW. (2008) Emerging infectious disease in sea stars: castrating ciliate parasites in Patiria miniata.Diseases of Aquatic Organisms 81: 173-176 Emerging infectious disease in sea stars: castrating ciliate parasites in Patiria miniata
scuticociliate; Asterias amurensis; biocontrol; sperm
Orchitophrya stellarum is a holotrich ciliate that facultatively parasitizes and castrates male asteriid sea stars. We discovered a morphologically similar ciliate in testes of an asterinid sea star, the northeastern Pacific bat star Patiria miniata (Brandt, 1835). This parasite may represent a threat to Canadian populations of this iconic sea star. Confirmation that the parasite is O. stellarum would indicate a considerable host range expansion, and suggest that O. stellarum is a generalist sea star pathogen. DOI
30. Cassista, MC; Hart, MW. (2007) Spatial and temporal genetic homogeneity in the Arctic surfclam (Mactromeris polynyma).Marine Biology 152: 569-579 Spatial and temporal genetic homogeneity in the Arctic surfclam (Mactromeris polynyma)
Commercially harvested marine bivalve populations show a broad range of population-genetic patterns that may be driven by planktonic larval dispersal (gene flow) or by historical (genetic drift) and ecological processes (selection). We characterized microsatellite genetic variation among populations and year classes of the commercially harvested Arctic surfclam, Mactromeris polynyma, in order to test the relative significance of gene flow and drift on three spatial scales: within commercially harvested populations in the northwest Atlantic; among Atlantic populations; and between the Atlantic and Pacific oceans. We found small nonsignificant genetic subdivision among eight populations from the northwest Atlantic (F (ST) = 0.002). All of these Atlantic populations were highly significantly differentiated from a northeast Pacific population (F (ST) = 0.087); all populations showed high inbreeding coefficients (F (IS) = 0.432). We tested one likely source of heterozygote deficits by aging individual clams and exploring genetic variation among age classes within populations (a temporal Wahlund effect). Populations showed strikingly different patterns of age structure, but we found little differentiation among age classes. In one case, we were able to analyze genetic diversity between age classes older or younger than the advent of intensive commercial harvesting. The results generally suggest spatially broad and temporally persistent genetic homogeneity of these bivalves. We discuss the implications of the results for the biology and management of surfclam populations. DOI
29. Harper, FM; Addison, JA; Hart, MW. (2007) Introgression versus immigration in hybridizing high-dispersal echinoderms.Evolution 61: 2410-2418 Introgression versus immigration in hybridizing high-dispersal echinoderms
echinoderm asterias; fertilization; gene flow; larval dispersal; phylogeography; speciation; Strongylocentrotus; trans-Arctic interchange
Phylogeographic studies designed to estimate rates and patterns of genetic differentiation within species often reveal unexpected and graphically striking cases of allele or haplotype sharing between species (introgression) via hybridization and backcrossing. Does introgression between species significantly influence population genetic structure relative to more conventional sources of differentiation (drift) and similarity (dispersal) among populations within species ? Here we use mtDNA sequences from four species in two genera of sea urchins and sea stars to quantify the relative magnitude of gene flow across oceans and across species boundaries in the context of the trans-Arctic interchange of marine organisms between the Pacific and Atlantic oceans. In spite of the much smaller distances between sympatric congeners, rates of gene flow between sympatric species via heterospecific gamete interactions were small and significantly lower than gene flow across oceans via dispersal of planktonic larvae. We conclude that, in these cases at least, larvae are more effective than gametes as vectors of gene flow. DOI
28. Harper, FM; Hart, MW. (2007) Morphological and phylogenetic evidence for hybridization and introgression in a sea star secondary contact zone.Invertebrate Biology 126: 373-384 Morphological and phylogenetic evidence for hybridization and introgression in a sea star secondary contact zone
phylogeography; Asterias; mtDNA; statistical parsimony
Glacial cycles and other climatic events have been widely invoked as factors promoting divergence, secondary contact, and hybridization between populations of terrestrial organisms, but the origin and fate of secondary contact in the sea is much less well understood. We studied the distribution of morphological and genetic variation in a northwest Atlantic zone of secondary contact between congeneric sea stars of Asterias that probably separated after the Pliocene as part of the trans-Arctic interchange. These species have similar reproductive biology and can hybridize in the laboratory. However, multivariate analysis of morphological traits scored from sea stars inside and outside the zone of secondary contact clearly indicated two clusters of phenotypes that corresponded to the two taxonomic species. A quantitative analysis of this clustering pattern did not support the hypothesis of a third grouping that might correspond to intermediate hybrid phenotypes. Known F-1 hybrids from laboratory matings grouped with one of the two taxonomic species. However, a survey of mtDNA sequence variation clearly indicated that similar to 13% of individuals of one species (Asterias forbesi) are descendants of hybridization events that resulted in introgression of haplotypes of Asterias rubens into populations of A. forbesi. We conclude that morphological phenotypes are inadequate to identify hybrids of Asterias and their descendants, and that hybridization and introgression might be common in this secondary contact zone. DOI
27.Hart, MW; Sunday, J. (2007) Things fall apart: biological species form unconnected parsimony networks.Biology Letters 3: 509-512 Things fall apart: biological species form unconnected parsimony networks
phylogenetic species; phylogeography; Astraptes; Cypraeidae
The generality of operational species definitions is limited by problematic definitions of between-species divergence. A recent phylogenetic species concept based on a simple objective measure of statistically significant genetic differentiation uses between-species application of statistical parsimony networks that are typically used for population genetic analysis within species. Here we review recent phylogeographic studies and reanalyse several mtDNA barcoding studies using this method. We found that (i) alignments of DNA sequences typically fall apart into a separate subnetwork for each Linnean species ( but with a higher rate of true positives for mtDNA data) and (ii) DNA sequences from single species typically stick together in a single haplotype network. Departures from these patterns are usually consistent with hybridization or cryptic species diversity. DOI
26.Hart, MW; Keever, CC; Dartnall, AJ; Byrne, M. (2006) Morphological and genetic variation indicate cryptic species within Lamarck's little sea star, Parvulastra (=Patiriella) exigua.Biol Bull 210: 158-167 Morphological and genetic variation indicate cryptic species within Lamarck's little sea star, Parvulastra (=Patiriella) exigua
The asterinid sea star Parvulastra exigua (Lamarck) is a common member of temperate intertidal marine communities from geographically widespread sites around the southern hemisphere. Individuals from Australian populations lay benthic egg masses (through orally directed gonopores) from which nonplanktonic offspring hatch and metamorphose without a dispersing planktonic larval phase. Scattered reports in the taxonomic literature refer to a similar form in southern Africa with aborally directed gonopores (and possibly broadcast spawning of planktonic eggs and larvae); such differences would be consistent with cryptic species variation. Surveys of morphology and mtDNA sequences have revealed cryptic species diversity in other asterinid genera. Here we summarize the taxonomic history of Lamarck's "Asterie exigue" and survey morphological variation (the location of the gonopores) for evidence that some P. exigua populations include cryptic species with a different mode of reproduction. We found strong evidence for multiple species in the form of two phenotypes and modes of reproduction (oral and aboral gonopore locations) in populations from southern Africa and islands in the Atlantic and Indian oceans. Both modes of reproduction have broad geographic ranges. These results are consistent with previously published genetic data that indicate multiple species in African and island (but not Australian) populations.
25. Addison, JA; Hart, MW. (2005) Colonization, dispersal, and hybridization influence phylogeography of North Atlantic sea urchins (Strongylocentrotus droebachiensis).Evolution 59: 532-543 Colonization, dispersal, and hybridization influence phylogeography of North Atlantic sea urchins (Strongylocentrotus droebachiensis)
coalescent analysis; cytochrome c oxidase subunit 1; Echinoidea; introgression; microsatellites; mitochondrial DNA; range expansion
We used frequency-based and coalescent-based phylogeographic analysis of sea urchin (Strongylocentrolus droebachiensis) mitochondrial DNA (mtDNA) sequences and previously published microsatellite data to understand the relative influence of colonization and gene flow from older (north Pacific) and younger (northeast Atlantic) sea urchin populations on genetic variation in the northwest Atlantic. We found strong evidence of survival of northwestern Atlantic populations in local Pleistocene glacial refugia: most haplotypes were the same as or closely related to Pacific haplotypes, with deep gene genealogies that reflect divergence times within the northwestern Atlantic that are much older than the last glacial maximum. We detected gene flow across the North Atlantic in the form of haplotypes shared with or recently descended from European populations. We also found evidence of significant introgression of haplotypes from a closely related species (S. pallidus). The relative magnitude of gene flow estimated by coalescent methods (and the effective population size differences among oceanic regions) depended on the genetic marker used. In general, we found very small effective population size in the northeastern Atlantic and high trans-Arctic gene flow between the Pacific and northwestern Atlantic. Both analyses suggested significant back-migration to the Pacific. However, microsatellites more strongly reflected older Pacific migration (with similar effective population sizes across the Arctic), whereas mtDNA sequences appeared to be more sensitive to recent trans-Atlantic dispersal (with larger differences in effective population size). These differences across marker types might have several biological or methodological causes, and they suggest caution in interpretation of the results from a single locus or class of markers.
24. Addison, JA; Hart, MW. (2005) Spawning, copulation and inbreeding coefficients in marine invertebrates.Biology Letters 1: 450-453 Spawning, copulation and inbreeding coefficients in marine invertebrates
F-IS; Wahlund effect; fertilization; population genetics
Patterns of population genetic variation have frequently been understood as consequences of life history covariates such as dispersal ability and breeding systems (e.g. selfing). For example, marine invertebrates show enormous variation in life history traits that are correlated with the extent of gene flow between populations and the magnitude of differentiation among populations at neutral genetic markers (F-ST). Here we document an unexpected correlation between marine invertebrate life histories and deviation from Hardy-Weinberg equilibrium (non-zero values of F-IS, the inbreeding coefficient). F-IS values were significantly higher in studies of species with free-spawned planktonic sperm than in studies of species that copulate or have some form of direct sperm transfer to females or benthic egg masses. This result was robust to several different analytical approaches. We note several mechanisms that might contribute to this pattern, and appeal for more studies and ideas that might help to explain our observations.
23. Cassista, MC; Hart, MW. (2005) Isolation and characterization of new microsatellite markers in the surfclam Mactromeris polynyma.Molecular Ecology Notes 5: 218-219 Isolation and characterization of new microsatellite markers in the surfclam Mactromeris polynyma
age structure; bivalve; fishery; inbreeding; population structure; Spisula spp.
We describe primers and amplification conditions for seven microsatellite loci that were developed and characterized in the commercially harvested surfclam Mactromeris polynyma. Five of these loci were polymorphic: we found 6 to 23 alleles per locus among 100 individuals from one population in Nova Scotia, with some large heterozygote deficits that may reflect unrecognized temporal genetic variation. We are using these markers to investigate temporal and spatial genetic structure in this species.
22. Harper, FM; Hart, MW. (2005) Gamete compatibility and sperm competition affect paternity and hybridization between sympatric Asterias sea stars.Biol Bull 209: 113-126 Gamete compatibility and sperm competition affect paternity and hybridization between sympatric Asterias sea stars
Gamete interactions may strongly influence speciation and hybridization in sympatric broadcast-spawning marine invertebrates. We examined the role of gamete compatibility in species integrity using cross-fertilization studies between sympatric Asterias sea stars from a secondary contact zone in the northwest Atlantic. In crosses between single males and single females, gametes of both species were compatible and produced viable, fertile hybrid offspring, but with considerable variation in the receptivity of eggs to heterospecific sperm. Differential compatibility of heterospecific gametes was detected in sperm competition studies in which we used a nuclear DNA marker to assign paternity to larval offspring. Several families showed conspecific sperm precedence in A. forbesi eggs, and one family showed competitive superiority of A. forbesi sperm fertilizing A. rubens eggs. Gametic interactions are an important component of prezygotic reproductive isolation in sympatric Asterias. The interaction between gametes of these closely related sea stars is consistent with the function of gamete recognition systems that are known to mediate fertilization success and speciation in other marine invertebrates.
21.Hart, MW; Podolsky, RD. (2005) Mitochondrial DNA phylogeny and rates of larval evolution in Macrophiothrix brittlestars.Molecular Phylogenetics and Evolution 34: 438-447 Mitochondrial DNA phylogeny and rates of larval evolution in Macrophiothrix brittlestars
echinoderm ophiuroid; brittlestar; facultative feeding; pluteus; mode of development; life-history transition; mitochondrial DNA
Phylogenetic analysis has led to significant insights into the evolution of early life-history stages of marine invertebrates. Although echinoderms have been a major focus, developmental and phylogenetic information are relatively poor for ophiuroids, the most species-rich echinoderm class. We used DNA sequences from two mitochondrial genes to develop a phylogenetic hypothesis for 14 brittlestar species in the genus Macrophiothrix (Family Ophiotrichidae). Species are similar in adult form and ecology, but have diverse egg sizes and modes of larval development. In particular, two species have rare larval forms with characteristics that are intermediate between more common modes of feeding and non-feeding development. We use the phylogeny to address whether intermediate larval forms are rare because the evolution of a simplified morphology is rapid once food is no longer required for development. In support of this hypothesis, branch lengths for intermediate forms were short relative to those for species with highly derived non-feeding forms. The absolute rarity of such forms makes robust tests of the hypothesis difficult. (C) 2004 Elsevier Inc. All rights reserved.
19. Henry, LA; Hart, M. (2005) Regeneration from injury and resource allocation in sponges and corals - A review.International Review of Hydrobiology 90: 125-158 Regeneration from injury and resource allocation in sponges and corals - A review
disturbance; wound; repair; life history; trade-off
The ability of bottom-dwelling marine epifauna to regenerate injured or lost body parts is critical to the survival of individuals from disturbances that inflict wounds. Numerous studies on marine sponges (Phlyum Porifera) and corals (of the orders Scleractinia and Alcyonacea) suggest that regeneration is limited by many intrinsic (individual-dependent) and extrinsic (environment-dependent) factors, and that other fife history processes may compete with regeneration for energetic and cellular resources. We review how intrinsic (size, age, morphology, genotype) and extrinsic (wound characteristics, water temperature, food availability, sedimentation, disturbance history, selection) factors limit regeneration in sponges and corals. We then review the evidence for impaired somatic growth and sexual reproduction, and altered outcomes of interactions (anti-predator defenses, competitive abilities, self- and non-self recognition abilities) with other organisms in regenerating sponges and corals. We demonstrate that smaller, older sponges and corals of decreasing morphological complexities tend to regenerate less well than others, and that regeneration can be modulated by genotype. Large wounds with small perimeters inflicted away from areas where resources are located tend to be regenerated less well than others, as are injuries inflicted when food is limited and when the animal has been previously or recently injured. We also demonstrate that regeneration strongly impairs somatic growth, reduces aspects of sexual reproduction, and decreases the ability for sponges and corals to defend themselves against predators, to compete, and to recognize conspecifics. Effects of limited regeneration and impaired life histories may manifest themselves in higher levels of biological assembly e.g., reduced accretion of epifaunal biomass, reduced recruitment and altered biotic associations, and thus affect marine community and ecosystem recovery from disturbances.
17. Addison, JA; Hart, MW. (2004) Analysis of population genetic structure of the green sea urchin (Strongylocentrotus droebachiensis) using microsatellites.Marine Biology 144: 243-251 Analysis of population genetic structure of the green sea urchin (Strongylocentrotus droebachiensis) using microsatellites
We measured within- and among-population genetic variation in the green sea urchin (Strongylocentrotus droebachiensis) at 11 sites in the north Atlantic and northeast Pacific by using four-locus microsatellite genotypes. We found no differentiation among populations from Atlantic Canada, but strong differentiation across the north Atlantic and between the Atlantic and Pacific samples. High inbreeding coefficients at three loci are consistent with high variance in reproductive success. One population that was recently decimated by disease was strongly differentiated from some others, but there was little differentiation otherwise among populations in Atlantic Canada. On a larger scale, populations in Atlantic Canada were more similar to a population from the north Pacific than to populations in the northwest Atlantic. Differentiation among populations at this large spatial scale is consistent with biogeographical hypotheses of: (1) Pleistocene population reduction and isolation in the northeast Atlantic, but (2) extinction in the northwest Atlantic followed by extensive recolonization from the Pacific. In contrast to other recent studies of trans-Atlantic organisms, we found no evidence of extensive gene flow across the north Atlantic.
16.Hart, MW; Johnson, SL; Addison, JA; Byrne, M. (2004) Strong character incongruence and character choice in phylogeny of sea stairs of the Asterinidae.Invertebrate Biology 123: 343-356 Strong character incongruence and character choice in phylogeny of sea stairs of the Asterinidae
total evidence; modes of development; life history; mtDNA; Asteroidea
Historically, characters from early animal development have been a potentially rich source of phylogenetic information, but many traits associated with the gametes and larval stages of animals with complex life cycles are widely suspected to have evolved frequent convergent similarities. Such convergences will confound true phylogenetic relationships. We compared phylogenetic inferences based on early life history traits with those from mitochondrial DNA sequences for sea stars in the genera Asterina, Cryptasterina, and Patiriella (Valvatida: Asterinidae). Analysis of these two character sets produced phylogenetics that shared few clades. We quantified the degree of homoplasy in each character set when mapped onto the phylogeny inferred from the alternative characters. The incongruence between early life history and nucleotide characters implies more homoplasy in the -life-history character set. We suggest that the early life history traits in this case are most likely to be misleading as phylogenetic characters because simple adaptive models predict convergence in early life histories. We show that adding early life history characters may slightly improve a phylogeny based on nucleotide sequences, but adding nucleotide characters may be critically important to improving inferences from phylogenies based on early life history characters.
15. Byrne, M; Hart, MW; Cerra, A; Cisternas, P. (2003) Reproduction and larval morphology of broadcasting and viviparous species in the Cryptasterina species complex.Biological Bulletin 205: 285-294 Reproduction and larval morphology of broadcasting and viviparous species in the Cryptasterina species complex
The Cryptasterina group of asterinid sea stars in Australasia comprises cryptic species with derived life histories. C. pentagona and C. hystera have planktonic and intragonadal larvae, respectively. C. pentagona has the gonochoric, free-spawning mode of reproduction with a planktonic lecithotrophic brachiolaria larva. C. hystera is hermaphroditic with an intragonadal lecithotrophic brachiolaria, and the juveniles emerge through the gonopore. Both species have large lipid-rich buoyant eggs and well-developed brachiolariae. Early juveniles are sustained by maternal nutrients for several weeks while the digestive tract develops. C. hystera was reared in vitro through metamorphosis. Its brachiolariae exhibited the benthic exploration and settlement behavior typical of planktonic larvae, and they attached to the substratum with their brachiolar complex. These behaviors are unlikely to be used in the intragonadal environment. The presence of a buoyant egg and functional brachiolaria larva would not be expected in an intragonadal brooder and indicate the potential for life-history reversal to a planktonic existence. Life-history traits of species in the Cryptasterina group are compared with those of other asterinids in the genus Patiriella with viviparous development. Modifications of life-history traits and pathways associated with evolution of viviparity in the Asterinidae are assessed, and the presence of convergent adaptations and clade-specific features associated with this unusual mode of parental care are examined.
13.Hart, MW; Byrne, M; Johnson, SL. (2003) Patiriella pseudoexigua (Asteroidea : Asterinidae): a cryptic species complex revealed by molecular and embryological analyses.Journal of the Marine Biological Association of the United Kingdom 83: 1109-1116 Patiriella pseudoexigua (Asteroidea : Asterinidae): a cryptic species complex revealed by molecular and embryological analyses
Cryptic lineages were identified within a morphologically uniform group of sea stars distributed from Australia to Japan. Among eight populations, all of which have been referred to Patiriella pseudoexigua, we found seven unique mitochondrial DNA sequences clustered into four distinct lineages. These four lineages formed a monophyletic group in which sister clades were separated by small genetic distances but could be differentiated from each other on the basis of reproductive differences. The four lineages thus appear to be separate but very closely related species. Examination of reproduction in several Queensland populations revealed that one population (Statue Bay) consisted of hermaphroditic intragonadal brooders with live-born offspring while other populations (Townsville., Bowen, Airlie Beach) consisted of dioecious free-spawners with a planktonic larva. The brooded larvae front central Queensland populations closely resembled brooded embryos and larvae of a Japanese lineage, while the planktonic larvae from northern Queensland were similar to the original description of planktonic larvae from a Taiwan population. However, each of the viviparous lineages was more closely related to a lineage with planktonic larval development than the viviparous lineages were to each other. Patiriella pseudoexigua thus comprises at least four species with different reproductive phenotypes in which viviparous brooding appears to have evolved in parallel. Based on previous taxonomic work we propose the following names for these four lineages: the dioecious free-spawner front northern Queensland (including the P. pseudoexigua type locality) is P. pseudoexigua sensu stricto; the viviparous brooder from central Queensland is undescribed and here referred to as Patiriella sp. nov: the dioecious free-spawner from Taiwan is temporarily referred to as Patiriella sp. (a senior name for this species may be P. pentagonus); and the hermaphrodite brooder from,japan should be raised to specific status and referred to by the new combination P. pacifica.
12. Addison, JA; Hart, MW. (2002) Characterization of microsatellite loci in sea urchins (Strongylocentrotus spp.).Molecular Ecology Notes 2: 493-494 Characterization of microsatellite loci in sea urchins (Strongylocentrotus spp.)
echinoderm; microsatellite; primers; sea urchin; Strongylocentrotus spp.
We present six dinucleotide repeats that were developed and characterized in Strongylocentrotus droebachiensis and also tested in S. purpuratus. Four of these loci are polymorphic in S. droebachiensis (13-20 alleles, N = 100) and five are polymorphic in S. purpuratus (5-12 alleles, N = 10). We are currently using these markers to investigate the population substructure of shallow water populations of S. droebachiensis in the north Atlantic.
11.Hart, MW. (2002) Life history evolution and comparative developmental biology of echinoderms.Evolution & Development 4: 62-71 Life history evolution and comparative developmental biology of echinoderms
Evolutionary biologists studying life history variation have used echinoderms in experimental, laboratory, and field studies of life history evolution. This focus on echinoderms grew originally from the tradition of comparative embryology, in which echinoderms were central. The tools for obtaining and manipulating echinoderm gametes and larvae were taken directly from comparative embryological research. In addition, the comparative embryologists employed a diverse array of echinoderms, not a few model species, and this diversity has led to a broad understanding of the development, function, and evolution of echinoderm larvae. As a result, this branch of life history evolution has deep roots in comparative developmental biology of echinoderms. Here two main aspects of this relationship are reviewed. The first is a broad range of studies of fertilization biology, dispersal, population genetics, functional morphology, and asexual reproduction in which developmental biologists might take a keen interest because of the historical origins of this research in echinoderm comparative embryology. The second is a similarly broad variety of topics in life history research in which evolutionary biologists require techniques or data from developmental biology in order to make progress on understanding patterns of life history variation among echinoderm species and higher taxa. Both sets of topics provide opportunities for interaction and collaboration.
10. Grosberg, RK; Hart, MW. (2000) Mate selection and the evolution of highly polymorphic self/nonself recognition genes.Science 289: 2111-2114 Mate selection and the evolution of highly polymorphic self/nonself recognition genes
Multicellular organisms use the products of highly polymorphic genes to distinguish self from conspecific nonself cells or tissues. These allorecognition polymorphisms may regulate somatic interactions between hosts and pathogens or between competitors (to avoid various forms of parasitism), as well as reproductive interactions between mates or between gametes (to avoid inbreeding). In both cases, rare alleles may be advantageous, but it remains unclear which mechanism maintains the genetic polymorphism for specificity in self/nonself recognition. Contrary to earlier reports, we show that mate selection cannot be a strong force maintaining allorecognition polymorphism in two colonial marine invertebrates. Instead, the regulation of intraspecific competitive interactions appears to promote the evolution of polymorphisms in these species.
9.Hart, M. (2000) Phylogenetic analyses of mode of larval development.Seminars in Cell & Developmental Biology 11: 411-418 Phylogenetic analyses of mode of larval development
ancestral state reconstruction; maximum likelihood; parallelism; phylogeny; species selection
Phylogenies based on morphological or molecular characters have been used to provide an evolutionary context for analysis of larval evolution. Studies of gastropods, bivalves, tunicates, sea stars, sea urchins, and polychaetes have revealed massive parallel evolution of similar larval forms. Some of these studies were designed to test, and have rejected, the species selection hypothesis for evolutionary trends in the frequency of derived larvae or life history traits. However; the lack of well supported models of larval character evolution leave some doubt about the quality of inferences of larval evolution from phylogenies of living taxa. Better models based on maximum likelihood methods and known prior probabilities of larval character state changes will improve our understanding of the history of larval evolution.
8.Hart, MW; Grosberg, RK. (1999) Kin interactions in a colonial hydrozoan (Hydractinia symbiolongicarpus): Population structure on a mobile landscape.Evolution 53: 793-805 Kin interactions in a colonial hydrozoan (Hydractinia symbiolongicarpus): Population structure on a mobile landscape
allorecognition; genetic polymorphism; Hydractinia symbiolongicarpus; Hydrozoa; population structure; RAPDs
Many sessile colonial organisms intensively compete with conspecifics for growing space. This competition can result in either cooperative fusion or aggressive rejection between colonies, and some species have evolved highly polymorphic genetic systems that mediate the outcome of these interactions. Here we demonstrate the potential for interactions among close kin as the basis for the evolutionary maintenance of a genetically polymorphic allorecognition system in the colonial hydroid Hydractinia symbiolongicarpus, which lives on gastropod shells occupied by hermit crabs. Fusion between hydroids in the laboratory is restricted mainly to encounters between full siblings, whereas other encounters result in aggressive rejection. Natural selection acting on the costs or benefits of fusion between colonies could be responsible for the present maintenance of such a highly specific behavioral response, but only if encounters between fusible colonies still occur in contemporary populations. The large size of these hydroid populations and the mobility of the crabs should limit the potential for interactions among closely related hydroids on the same shell. However, RAPD polymorphisms among a large sample of hydroids from a population off the coast of Massachusetts indicate that genetically similar colonies are often found together on the same shell. Some genetic distances between colonies on the same shell were low relative to genetic distances between colonies on different shells or genetic distances between known full siblings from laboratory matings. We conservatively estimate that 2-18% of co-occurring colonies may be full sibling pairs. These observations suggest that encounters between genetically similar hydroids are common, despite the mobile nature of their habitat, and these encounters may provide frequent opportunities for natural selection to influence the evolution of cooperative and agonistic behaviors and their polymorphic genetic basis.
6.Hart, MW; Byrne, M; Smith, MJ. (1997) Molecular phylogenetic analysis of life-history evolution in Asterinid starfish.Evolution 51: 1848-1861 Molecular phylogenetic analysis of life-history evolution in Asterinid starfish
Asterinidae; Asterina; COI; egg size; hermaphroditism; larval development; Oreaster; Patiriella; Pisaster; planktotrophy; tRNA; viviparity
We analyzed phylogenetic relationships among 12 nominal species of starfish in the genera Patiriella and Asterina (Order Valvatida, Family Asterinidae), based on complete sequences for a mitochondrial protein coding gene (cytochrome oxidase subunit I) and five mitochondrial transfer RNA genes (alanine, leucine, asparagine, glutamine, and proline) (1923 bp total). The resulting phylogeny was used to test a series of hypotheses about the evolution of life-history traits. (1) A complex, feeding, planktonic larva is probably ancestral for these starfish, but this is not the most parsimonious reconstruction of ancestral larval states, (2) The feeding larval form was lost at least four times among these species, and three of these losses occurred among members of a single clade. (3) Small adult size evolved before both cases of hermaphroditism and viviparous brooding, but viviparity was not always preceded by an inter mediate form of external brooding, (4) An ordered transformation series from feeding planktonic development to viviparous brooding has been predicted for starfish, but we could not find an example of this transformation series. (5) Viviparity evolved recently (< 2 Mya). (6) Both species selection and transformation of lineages may have contributed to the accumulation of species with nonfeeding development among these starfish. (7) Neither Asterina nor Patiriella are monophyletic genera. Larval forms and Life-history traits of these starfish have evolved freely under no obvious constraints, contrary to the widely assumed evolutionary conservatism of early development. DOI PubMed
5.Hart, MW. (1996) Deconstructing suspension feeders by analysis of film and video.Invertebrate Biology 115: 185-190 Deconstructing suspension feeders by analysis of film and video
cilia; larva; behavior; echinoderms; bryozoans
Technological advances in illuminating, imaging, and recording the movements of small organisms now make it possible to analyze feeding behaviors that were previously misunderstood (e. g., suspension feeding). Presentations in this symposium include some of the best examples of the use of modern videomicroscopy to study suspension feeding, and other examples are found in the recent literature. However, video recordings often do not provide direct demonstration of feeding mechanisms (or other behaviors). Instead, video recordings provide data with which to test hypotheses about feeding. The presentation and interpretation of such data require a forthright accounting of their strengths and limitations. This accounting helps to dispel the common misconception that direct observation of behavior should provide direct insight into feeding mechanisms. I illustrate the usefulness of this accounting with a well-known example of suspension feeding: capture of small particles by reversal of ciliary beat in ciliated bands of some small echinoderms, hemichordates, and lophophorates.
4.Hart, MW. (1996) Evolutionary loss of larval feeding: Development, form and function in a facultatively feeding larva, Brisaster latifrons.Evolution 50: 174-187 Evolutionary loss of larval feeding: Development, form and function in a facultatively feeding larva, Brisaster latifrons
Brisaster latifrons; Echinoidea; egg size; facultative feeding; larval feeding; mode of development; Spatangoida
Species with large eggs and nonfeeding larvae have evolved many times from ancestors with smaller eggs and feeding larvae in numerous groups of aquatic invertebrates and amphibians. This change in reproductive allocation and larval form is often accompanied by dramatic changes in development. Little is known of this transformation because the intermediate form (a facultatively feeding larva) is rare. Knowledge of facultatively feeding larvae may help explain the conditions under which nonfeeding larvae evolve. Two hypotheses concerning the evolutionary loss of larval feeding are as follows: (1) large eggs evolve before modifications in larval development, and (2) the intermediate form (facultatively feeding larva) is evolutionarily short-lived. I show that larvae of a heart urchin, Brisaster latifrons, are capable of feeding but do not require food to complete larval development. Food for larvae appears to have little effect on larval growth and development. The development, form, and suspension feeding mechanism of these larvae are similar to those of obligate-feeding larvae of other echinoids. Feeding rates of Brisaster larvae are similar to cooccurring, obligate-feeding echinoid larvae but are low relative to the large size of Brisaster larvae. The comparison shows that in Brisaster large egg size, independence from larval food, and relatively low feeding rate have evolved before the heterochronies and modified developmental mechanisms common in nonfeeding echinoid larvae. If it is general, the result suggests that hypotheses concerning the origin of nonfeeding larval development should be based on ecological factors that affect natural selection for large eggs, rather than on the evolution of heterochronies and developmental novelties in particular clades. I also discuss alternative hypotheses concerning the evolutionary persistence of facultative larval feeding as a reproductive strategy. These hypotheses could be tested against a phylogenetic hypothesis.
3.Hart, MW. (1996) Variation in suspension feeding rates among larvae of some temperate, eastern Pacific echinoderms.Invertebrate Biology 115: 30-45 Variation in suspension feeding rates among larvae of some temperate, eastern Pacific echinoderms
echinoderm larval morphology; cilia
Larvae of many echinoderms and other benthic marine invertebrates depend on ciliary suspension feeding for growth and development, but some larvae may be superior feeding devices (with consequences for variation in growth, size, and fitness). I measured differences in feeding performance among larvae of 9 echinoderm species from 4 taxonomic classes (Asteroidea, Ophiuroidea, Holothuroidea, Echinoidea). Maximum clearance rates (relative to size of the feeding structure) of some larvae were much higher than the rates of others, indicating substantial variation in feeding capabilities among larvae of similar size. In order to interpret these differences in feeding capability, I also give some preliminary data on larval form, development, and organic content. Although incomplete in several respects, these data do not indicate a simple relation between larval feeding and growth. This surprising result indicates that functional morphology is not always the most appropriate perspective from which to examine variation in growth and development of planktonic larvae.
1.Hart, MW. (1996) Deconstructing suspension feeders by analysis of film and video.Invertebr. Biol. 115: 185-190 Deconstructing suspension feeders by analysis of film and video
cilia; larva; behavior; echinoderms; bryozoans
Technological advances in illuminating, imaging, and recording the movements of small organisms now make it possible to analyze feeding behaviors that were previously misunderstood (e. g., suspension feeding). Presentations in this symposium include some of the best examples of the use of modern videomicroscopy to study suspension feeding, and other examples are found in the recent literature. However, video recordings often do not provide direct demonstration of feeding mechanisms (or other behaviors). Instead, video recordings provide data with which to test hypotheses about feeding. The presentation and interpretation of such data require a forthright accounting of their strengths and limitations. This accounting helps to dispel the common misconception that direct observation of behavior should provide direct insight into feeding mechanisms. I illustrate the usefulness of this accounting with a well-known example of suspension feeding: capture of small particles by reversal of ciliary beat in ciliated bands of some small echinoderms, hemichordates, and lophophorates. DOI