Selection and demographic history shape the molecular evolution of the gamete compatibility protein bindin in Pisaster sea stars

Abstract

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.

Ocean circulation model predicts high genetic structure observed in a long‐lived pelagic developer

“…However, our results suggest that this structure may alternatively be caused by historical processes (such as vicariance) and maintained by oceanographic effects on passive dispersal alone (Hilbish 1996). By contrast, additional mechanisms are required to explain the lack of genetic structure in taxa with similar dispersal potentials in the same region, for example the sea star Pisaster ochraceus (Harley et al 2006;Popovic et al 2014), dispersing snails (Kyle & Boulding 2000;Marko 2004), chitons with dispersive larvae (Kelly & Eernisse 2007), intertidal copepods (Edmands 2001) and other dispersing species (Kelly & Palumbi 2010). The relatively low connectivity generated by our oceanographic model suggests that the lack of genetic structure in other taxa is more likely attributable to historical processes such as relatively recent range expansions, or to large effective population sizes that limit the rate of lineage sorting through genetic drift.…”

“…; Popovic et al . ), dispersing snails (Kyle & Boulding ; Marko ), chitons with dispersive larvae (Kelly & Eernisse ), intertidal copepods (Edmands ) and other dispersing species (Kelly & Palumbi ). The relatively low connectivity generated by our oceanographic model suggests that the lack of genetic structure in other taxa is more likely attributable to historical processes such as relatively recent range expansions, or to large effective population sizes that limit the rate of lineage sorting through genetic drift.…”

Comparative genomics reveals divergent thermal selection in warm‐ and cold‐tolerant marine mussels

“…In turn, such methods may underestimate adaptive fixation if current polymorphism is maintained by polygenic selection or soft selective sweeps (Messer & Petrov, 2013;Storz & Wheat, 2010). Furthermore, because signatures of selection cannot be specified to individual codons, methods based on pooled polymorphism statistics are likely to miss selective targets if adaptive evolution is constrained to small gene regions, such as protein binding domains in long conserved proteins (e.g., Hart, Sunday, Popovic, Learning, & Konrad, 2014;Popovic, Marko, Wares, & Hart, 2014).…”

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

“…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.…”