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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.

SUBMITTER: Popovic I

PROVIDER: S-EPMC4063459 | biostudies-literature | 2014 May

REPOSITORIES: biostudies-literature

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

Popovic Iva I Marko Peter B PB Wares John P JP Hart Michael W MW

Ecology and evolution 20140331 9

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 se ...[more]

PMID: 24967076

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Project description:Disease emergence occurs within the context of ecological communities, and disease driven declines in host populations can lead to complex direct and indirect ecological effects. Varying effects of a single disease among multiple susceptible hosts could benefit relatively resistant species. Beginning in 2013, an outbreak of sea star wasting disease (SSWD) led to population declines of many sea star species along the west coast of North America. Through field surveys and laboratory experiments, we investigated how and why the relative abundances of two co-occurring sea star species, Evasterias troschelii and Pisaster ochraceus, shifted during the ongoing wasting epidemic in Burrard Inlet, British Columbia, Canada. We hypothesized that Evasterias is competitively inferior to Pisaster but more resistant to SSWD. Thus, we predicted that SSWD-induced declines of Pisaster could mitigate the negative effects of SSWD on Evasterias, as the latter would experience competitive release. We document shifts in sea star abundance from 2008-2017: Pisaster abundance and mean size declined during the outbreak, while Evasterias abundance increased from relatively rare to numerically dominant within the intertidal. When exposed to symptomatic sea stars, Pisaster and Evasterias both showed signs of SSWD, but transmission and susceptibility was lower in Evasterias. Despite diet overlap documented in our field surveys, Evasterias was not outcompeted by Pisaster in laboratory trails conducted with the relatively small Pisaster available after the outbreak. Interference competition with larger Pisaster, or prey exploitation by Pisaster during the summer when Evasterias is primarily subtidal, may explain the rarity of Evasterias prior to Pisaster declines. Our results suggest that indirect effects mediated by competition can mask some of the direct effects of disease outbreaks, and the combination of direct and indirect effects will determine the restructuring of a community after disturbance.

Dataset Information

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

Publications

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

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