15. 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
14.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
13. 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
12. 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
11.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
10.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
9.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
8.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
6.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
5. 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
4. 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
3.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
2. 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