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An ancient selective sweep linked to reproductive life history evolution in sockeye salmon.

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.

SUBMITTER: Veale AJ

PROVIDER: S-EPMC5431894 | biostudies-literature | 2017 May

REPOSITORIES: biostudies-literature

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An ancient selective sweep linked to reproductive life history evolution in sockeye salmon.

Veale Andrew J AJ Russello Michael A MA

Scientific reports 20170511 1

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 ~22,73 ...[more]

PMID: 28496186

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Project description:Human-mediated habitat fragmentation in freshwater ecosystems can negatively impact genetic diversity, demography, and life history of native biota, while disrupting the behavior of species that are dependent on spatial connectivity to complete their life cycles. In the Alouette River system (British Columbia, Canada), dam construction in 1928 impacted passage of anadromous sockeye salmon (Oncorhynchus nerka), with the last records of migrants occurring in the 1930s. Since that time, O. nerka persisted as a resident population in Alouette Reservoir until experimental water releases beginning in 2005 created conditions for migration; two years later, returning migrants were observed for the first time in ~70 years, raising important basic and applied questions regarding life-history variation and population structure in this system. Here, we investigated the genetic distinctiveness and population history of Alouette Reservoir O. nerka using genome-wide SNP data (n = 7,709 loci) collected for resident and migrant individuals, as well as for neighboring anadromous sockeye salmon and resident kokanee populations within the Fraser River drainage (n = 312 individuals). Bayesian clustering and principal components analyses based on neutral loci revealed five distinct clusters, largely associated with geography, and clearly demonstrated that Alouette Reservoir resident and migrant individuals are genetically distinct from other O. nerka populations in the Fraser River drainage. At a finer level, there was no clear evidence for differentiation between Alouette Reservoir residents and migrants; although we detected eight high-confidence outlier loci, they all mapped to sex chromosomes suggesting that differences were likely due to uneven sex ratios rather than life history. Taken together, these data suggest that contemporary Alouette Reservoir O. nerka represents a landlocked sockeye salmon population, constituting the first reported instance of deep-water spawning behavior associated with this life-history form. This finding punctuates the need for reassessment of conservation status and supports ongoing fisheries management activities in Alouette Reservoir.

Project description:Evaluations of human impacts on Earth's ecosystems often ignore evolutionary changes in response to altered selective regimes. Freshwater habitats for Snake River fall Chinook salmon (SRFCS), a threatened species in the US, have been dramatically changed by hydropower development and other watershed modifications. Associated biological changes include a shift in juvenile life history: Historically essentially 100% of juveniles migrated to sea as subyearlings, but a substantial fraction have migrated as yearlings in recent years. In contemplating future management actions for this species should major Snake River dams ever be removed (as many have proposed), it will be important to understand whether evolution is at least partially responsible for this life-history change. We hypothesized that if this trait is genetically based, parents who migrated to sea as subyearlings should produce faster-growing offspring that would be more likely to reach a size threshold to migrate to sea in their first year. We tested this with phenotypic data for over 2,600 juvenile SRFCS that were genetically matched to parents of hatchery and natural origin. Three lines of evidence supported our hypothesis: (i) the animal model estimated substantial heritability for juvenile growth rate for three consecutive cohorts; (ii) linear modeling showed an association between juvenile life history of parents and offspring growth rate; and (iii) faster-growing juveniles migrated at greater speeds, as expected if they were more likely to be heading to sea. Surprisingly, we also found that parents reared a full year in a hatchery produced the fastest growing offspring of all-apparently an example of cross-generational plasticity associated with artificial propagation. We suggest that SRFCS is an example of a potentially large class of species that can be considered to be "anthro-evolutionary"-signifying those whose evolutionary trajectories have been profoundly shaped by altered selective regimes in human-dominated landscapes.

Dataset Information

An ancient selective sweep linked to reproductive life history evolution in sockeye salmon.

Publications

An ancient selective sweep linked to reproductive life history evolution in sockeye salmon.

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