Detecting genotypic changes associated with selective mortality at sea in Atlantic salmon: polygenic multilocus analysis surpasses genome scan

Bourret, Vincent; Dionne, Mélanie; Bernatchez, Louis

doi:10.1111/mec.12798

Cited by 63 publications

(101 citation statements)

References 52 publications

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“…Thus, the commonly held assumption that plasticity is the only reason for phenotypic differences in systems with weak population subdivision (such as marine species with planktonic dispersal) must be re-evaluated. Similar patterns have been found in recent studies of divergence that have sufficient resolution or design to detect such subtle genomic changes [39,45,46].…”

Section: Implications For Management and Beyondsupporting

confidence: 64%

“…Despite the emphasis on examples containing genes of major effect accounting for phenotypic variation in nature [38], quantitative traits are expected to involve many genes of minor effects; thus, subtle shifts in allele frequency should be the expected mechanism underlying polygenic selection. This has recently been demonstrated for salmon survival at sea [39] and coral thermal tolerance [40], but more strikingly with height in humans, where the cumulative total effects of identified outliers (univariate approach) only explain 5% of variation, as opposed to a polygenic approach that explained 45% of the phenotypic variation [41]. This demonstrates the inherent difficulty in detecting quantitative genetic differences with traditional outlier approaches.…”

Section: Causes Of Parallel Genetic Differences Despite Panmixiamentioning

confidence: 90%

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RAD Sequencing Highlights Polygenic Discrimination of Habitat Ecotypes in the Panmictic American Eel

et al. 2015

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The two primary ways that species respond to heterogeneous environments is through local adaptation and phenotypic plasticity. The American eel (Anguilla rostrata) presents a paradox; despite inhabiting drastically different environments [1], the species is panmictic [2, 3]. Spawning takes place only in the southern Sargasso Sea in the Atlantic Ocean [1]. Then, the planktonic larvae (leptocephali) disperse to rearing locations from Cuba to Greenland, and juveniles colonize either freshwater or brackish/saltwater habitats, where they spend 3-25 years before returning to the Sargasso Sea to spawn as a panmictic species. Depending on rearing habitat, individuals exhibit drastically different ecotypes [4-6]. In particular, individuals rearing in freshwater tend to grow slowly and mature older and are more likely to be female in comparison to individuals that rear in brackish/saltwater [4, 6]. The hypothesis that phenotypic plasticity alone can account for all of the differences was not supported by three independent controlled experiments [7-10]. Here, we present a genome-wide association study that demonstrates a polygenic basis that discriminates these habitat-specific ecotypes belonging to the same panmictic population. We found that 331 co-varying loci out of 42,424 initially considered were associated with the divergent ecotypes, allowing a reclassification of 89.6%. These 331 SNPs are associated with 101 genes that represent vascular and morphological development, calcium ion regulation, growth and transcription factors, and olfactory receptors. Our results are consistent with divergent natural selection of phenotypes and/or genotype-dependent habitat choice by individuals that results in these genetic differences between habitats, occurring every generation anew in this panmictic species.

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Section: Implications For Management and Beyondsupporting

confidence: 64%

Section: Causes Of Parallel Genetic Differences Despite Panmixiamentioning

confidence: 90%

RAD Sequencing Highlights Polygenic Discrimination of Habitat Ecotypes in the Panmictic American Eel

et al. 2015

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“…; Bourret et al . ) with changes in covarying alleles across populations. These methods can take into account interactions between loci of small phenotypic effect, typical of life history traits, and can reveal patterns of adaptive evolution beyond studies on individual loci (Hancock et al .…”

Section: Introductionmentioning

confidence: 99%

Integration of Random Forest with population‐based outlier analyses provides insight on the genomic basis and evolution of run timing in Chinook salmon (Oncorhynchus tshawytscha)

et al. 2015

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Anadromous Chinook salmon populations vary in the period of river entry at the initiation of adult freshwater migration, facilitating optimal arrival at natal spawning. Run timing is a polygenic trait that shows evidence of rapid parallel evolution in some lineages, signifying a key role for this phenotype in the ecological divergence between populations. Studying the genetic basis of local adaptation in quantitative traits is often impractical in wild populations. Therefore, we used a novel approach, Random Forest, to detect markers linked to run timing across 14 populations from contrasting environments in the Columbia River and Puget Sound, USA. The approach permits detection of loci of small effect on the phenotype. Divergence between populations at these loci was then examined using both principle component analysis and FST outlier analyses, to determine whether shared genetic changes resulted in similar phenotypes across different lineages. Sequencing of 9107 RAD markers in 414 individuals identified 33 predictor loci explaining 79.2% of trait variance. Discriminant analysis of principal components of the predictors revealed both shared and unique evolutionary pathways in the trait across different lineages, characterized by minor allele frequency changes. However, genome mapping of predictor loci also identified positional overlap with two genomic outlier regions, consistent with selection on loci of large effect. Therefore, the results suggest selective sweeps on few loci and minor changes in loci that were detected by this study. Use of a polygenic framework has provided initial insight into how divergence in a trait has occurred in the wild.

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“…Using a natural ‘differential mortality’ experiment, Bourret et al . () compared allelic and genotypic frequencies between juveniles (smolts) and adults (grilses) in two regional genetic groups, across 2 years. This natural experiment estimates the contemporary allelic response to unknown selective forces that smolts encounter during their year at sea (Fig.…”

Section: The Contemporary Response To Selectionmentioning

confidence: 99%

“…The findings of Bourret et al . () are consistent with polygenic selection on a quantitative trait of smolts during their first year at sea, and it will be interesting for future studies to identify the quantitative trait under selection. Their results make a compelling argument that single‐locus approaches may be limiting our ability to detect parallel signatures of selection.…”

Section: Looking Forwardmentioning

confidence: 99%

Genome scans for the contemporary response to selection in quantitative traits

Lotterhos

Schaal

2014

Molecular Ecology

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Genome scans have been an important approach for discovering historical signatures of selection in both model and nonmodel species. An exciting new experimental design for genome scans is to measure the change in allele frequency before and after contemporary selection within a generation, from a single population. The most widely-used methods, however, have two major limitations: they are based on testing one locus at a time, and they only have power to uncover loci that have evolved under relatively strong selection. On the other hand, complex quantitative traits are common in nature and are caused by several loci of small effect. Selection on a quantitative trait at the phenotypic level is predicted to be accompanied by subtle allele frequency changes in many loci that covary (a polygenic soft sweep), rather than a large, single-effect allele (a selective sweep). In this issue of Molecular Ecology, Bourret et al. (2014) measure the contemporary response to natural selection across the genome in multiple cohorts of Atlantic salmon during their first year at sea. They introduce a multilocus framework based on groups of markers that covary in their genotypic distribution. While the traditional, singlelocus approach did not find evidence for repeated patterns of selection, the multivariate approach found that a group of covarying SNPs was selected for in different cohorts at one site. Their multilocus framework has potential to be a more fruitful approach for uncovering the genomic basis of adaptation in quantitative traits, although caution should be applied as the framework has yet to be validated with simulated data.

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Detecting genotypic changes associated with selective mortality at sea in Atlantic salmon: polygenic multilocus analysis surpasses genome scan

Cited by 63 publications

References 52 publications

RAD Sequencing Highlights Polygenic Discrimination of Habitat Ecotypes in the Panmictic American Eel

RAD Sequencing Highlights Polygenic Discrimination of Habitat Ecotypes in the Panmictic American Eel

Integration of Random Forest with population‐based outlier analyses provides insight on the genomic basis and evolution of run timing in Chinook salmon (Oncorhynchus tshawytscha)

Genome scans for the contemporary response to selection in quantitative traits

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