Sperm<i>Bindin</i>Divergence under Sexual Selection and Concerted Evolution in Sea Stars

Patiño, Susana; Keever, Carson C.; Sunday, Jennifer M.; Popovic, Iva; Byrne, Maria; Hart, Michael W.

doi:10.1093/molbev/msw081

Cited by 13 publications

(28 citation statements)

References 81 publications

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“…) or at the level of vitelline layer binding and penetration (steps iii–iv) with the sperm protein bindin (Lessios ; Vacquier & Swanson ; Evans & Sherman ), as also shown recently for sea stars (Patiño et al . ). In Ophioderma longicauda , none of these proteins were found to evolve under positive selection.…”

Section: Discussionmentioning

confidence: 97%

“…Using domain prediction analyses, we did not detect any repetitive regions as found in sea stars (Patiño et al . ). It is therefore likely that the Ophioderma bindin sequences are incomplete, due to the difficulty of assembling repetitive regions using short read sequences.…”

Section: Discussionmentioning

confidence: 97%

“…Positive selection frequently targets these systems, as was shown for the bindin protein in sea urchins of the genus Strongylocentrotus, Paracentrotus , Heliocidaris and Echinometra (Lessios ), as well as in sea stars (Sunday & Hart ; Patiño et al . ), and for the egg receptor for sperm Obi1 (Hart ; Hart et al . ).…”

Section: Introductionmentioning

confidence: 99%

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Positive selection on sperm ion channels in a brooding brittle star: consequence of life‐history traits evolution

et al. 2017

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Closely related species are key models to investigate mechanisms leading to reproductive isolation and early stages of diversification, also at the genomic level. The brittle star cryptic species complex Ophioderma longicauda encompasses the sympatric broadcast-spawning species C3 and the internal brooding species C5. Here, we used de novo transcriptome sequencing and assembly in two closely related species displaying contrasting reproductive modes to compare their genetic diversity and to investigate the role of natural selection in reproductive isolation. We reconstructed 20 146 and 22 123 genes for C3 and C5, respectively, and characterized a set of 12 229 orthologs. Genetic diversity was 1.5-2 times higher in C3 compared to C5, confirming that species with low parental investment display higher levels of genetic diversity. Forty-eight genes were the targets of positive diversifying selection during the evolution of the two species. Notably, two genes (NHE and TetraKCNG) are sperm-specific ion channels involved in sperm motility. Ancestral sequence reconstructions show that natural selection targeted the two genes in the brooding species. This may result from an adaptation to the novel environmental conditions surrounding sperm in the brooding species, either directly affecting sperm or via an increase in male/female conflict. This phenomenon could have promoted prezygotic reproductive isolation between C3 and C5. Finally, the sperm receptors to egg chemoattractants differed between C3 and C5 in the ligand-binding region. We propose that mechanisms of species-specific gamete recognition in brittle stars occur during sperm chemotaxis (sperm attraction towards the eggs), contrary to other marine invertebrates where prezygotic barriers to interspecific hybridization typically occur before sperm-egg fusion.

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Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 97%

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Positive selection on sperm ion channels in a brooding brittle star: consequence of life‐history traits evolution

et al. 2017

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“…Our motivation for this study came from previous analyses of sperm-and egg-expressed genes with epistatic interactions at fertilization in sea stars, in which we found evidence of selection for amino acid differences between alleles from diverging conspecific populations (Sunday and Hart 2013) and from closely-related species (Popovic et al 2014;Patiño et al 2016), and strong effects of those amino acid differences on sperm-egg compatibility and fertilization rates in laboratory experiments (Hart et al 2014). Our goals in this study were similar: to identify specific sites under selection that could account for previously discovered LD between human C4BPA and ZP3 (Rohlfs, Swanson & Weir 2010), extend those analyses to include human ZP2, and identify possible phenotypic effects of those polymorphisms on reproductive success.…”

Section: Overviewmentioning

confidence: 99%

Peer Review #3 of "Positive selection on human gamete-recognition genes (v0.2)"

Turner¹

2018

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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 coadapted allele pairs. Such patterns also suggest specific molecular traits that may be associated with both natural reproductive variation and clinical infertility.

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“…Our motivation for this study came from previous analyses of sperm-and egg-expressed genes 152 with epistatic interactions at fertilization in sea stars, in which we found evidence of selection for 153 amino acid differences between alleles from diverging conspecific populations (Sunday and Hart 154 2013) and from closely-related species (Popovic et al 2014;Patiño et al 2016), and strong 155 effects of those amino acid differences on sperm-egg compatibility and fertilization rates in 156 laboratory experiments (Hart et al 2014). Our goals in this study were similar: to identify 157 specific sites under selection that could account for previously discovered LD between human 158 C4BPA and ZP3 (Rohlfs, Swanson & Weir 2010), extend those analyses to include human ZP2, 159 and identify possible phenotypic effects of those polymorphisms on reproductive success.…”

mentioning

confidence: 99%

Peer Review #1 of "Positive selection on human gamete-recognition genes (v0.1)"

2018

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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 coadapted allele pairs. Such patterns also suggest specific molecular traits that may be associated with both natural reproductive variation and clinical infertility. Abstract 12

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SpermBindinDivergence under Sexual Selection and Concerted Evolution in Sea Stars

Cited by 13 publications

References 81 publications

Positive selection on sperm ion channels in a brooding brittle star: consequence of life‐history traits evolution

Positive selection on sperm ion channels in a brooding brittle star: consequence of life‐history traits evolution

Peer Review #3 of "Positive selection on human gamete-recognition genes (v0.2)"

Peer Review #1 of "Positive selection on human gamete-recognition genes (v0.1)"

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