Abstract
Study of parallel (or convergent) phenotypic evolution can provide important insights into processes driving sympatric, ecologically-mediated divergence and speciation, as ecotype pairs may provide a biological replicate of the underlying signals and mechanisms. Here, we provide evidence for a selective sweep creating an island of divergence associated with reproductive behavior in sockeye salmon (Oncorhynchus nerka), identifying a series of linked single nucleotide polymorphisms across a ~22,733 basepair region spanning the leucine-rich repeat-containing protein 9 gene exhibiting signatures of divergent selection associated with stream- and shore-spawning in both anadromous and resident forms across their pan-Pacific distribution. This divergence likely occurred ~3.8 Mya (95% HPD = 2.1–6.03 Mya), after sockeye separated from pink (O. gorbuscha) and chum (O. keta) salmon, but prior to the Pleistocene glaciations. Our results suggest recurrent evolution of reproductive ecotypes across the native range of O. nerka is at least partially associated with divergent selection of pre-existing genetic variation within or linked to this region. As sockeye salmon are unique among Pacific salmonids in their flexibility to spawn in lake-shore benthic environments, this region provides great promise for continued investigation of the genomic basis of O. nerka life history evolution, and, more broadly, for increasing our understanding of the heritable basis of adaptation of complex traits in novel environments.
Highlights
Understanding how and why populations diverge into new species or ecotypes are principal goals of evolutionary biology[1]
When similar environmental pressures and associated selective pressures occur in different populations within a species range, parallel evolution may lead to similar phenotypic changes[7, 8] that may have the same underlying genetic basis[9, 10]
In particular, exhibit tremendous life history and morphological variation, with the repeated parallel evolution of several morphologically and ecologically divergent ecotypes linked to migratory and spawning behaviour[24,25,26]
Summary
Understanding how and why populations diverge into new species or ecotypes are principal goals of evolutionary biology[1]. Studies of the genomic bases of local adaptation have been facilitated by the advent of high-throughput genotyping methods that allow for the identification and genotyping of thousands of genetic polymorphisms throughout the genome enabling population genomic and association studies in non-model organisms[14,15,16] Such data further allow for the investigation of the genetics of adaptation through divergence mapping, where large suites of markers are screened for signatures of divergent selection among ecologically distinct populations[17,18,19,20]. The key to this approach is that substitutions physically linked to a beneficial allele will ‘hitchhike’, creating a region of lower diversity of fixed alleles in a process known as a ‘selective sweep’[21, 22]. While it is possible that such divergence occurs due to philopatry or learned spawning habitat preferences, we predict there may be underlying genetic mechanisms behind ecotype divergence, potentially involving ‘speciation genes’[34]
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