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.
Highlights
A long-standing goal of evolutionary biology is to understand the interacting roles of selective and demographic processes in shaping patterns of genetic diversity among populations, and how that can lead to the evolution of distinct species
2012); and identifying barrier genes that maintain species boundaries among already diverged species during secondary contact (e.g., Won et al 2005; Maroja et al 2009; Pinho and Hey 2010). Both themes of research have made major advances in understanding the roles played by disruptive selection during ecological speciation (Schluter 2001; Rundle and Nosil 2005; Schluter 2009; Via 2009), the frequency and nature of sexual conflict (Rice and Holland 1997; Chapman et al 2003; Tomaiuolo et al 2007; Crespi and Nosil 2013) and sexual selection (Maan and Seehausen 2011) in genetic divergence, and the evolutionary conditions that increase the potential for reinforcement (Maroja et al 2009; Pinho and Hey 2010)
I characterized the gene coding for bindin for all three sea star species in the genus Pisaster and analyzed its molecular evolution within and between species
Summary
A long-standing goal of evolutionary biology is to understand the interacting roles of selective and demographic processes in shaping patterns of genetic diversity among populations, and how that can lead to the evolution of distinct species. Both themes of research have made major advances in understanding the roles played by disruptive selection during ecological speciation (Schluter 2001; Rundle and Nosil 2005; Schluter 2009; Via 2009), the frequency and nature of sexual conflict (Rice and Holland 1997; Chapman et al 2003; Tomaiuolo et al.2007; Crespi and Nosil 2013) and sexual selection (Maan and Seehausen 2011) in genetic divergence, and the evolutionary conditions that increase the potential for reinforcement (Maroja et al 2009; Pinho and Hey 2010) Among these developments, genome-scale generation sequencing and traditional genetic analyses have characterized genomic signatures of the origins of lineage sorting in parts of the genome specific to ‘barrier’ or ‘speciation’ loci, where relative reductions in gene flow may reflect differences among populations in the relative fitness of immigrant alleles specific to those loci (Turner et al 2005; Nosil et al 2009; Via 2012; Nosil and Feder 2012; Ellegren 2013). A more complete understanding of the interaction between migration, genetic drift and selection at specific loci can provide important perspectives on the evolutionary processes that promote local adaptation and population-level divergence (Coyne and Orr 2004; Maroja et al 2009; Pinho and Hey 2010; Feder and Nosil 2010)
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