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Genomic release-recapture experiment in the wild reveals within-generation polygenic selection in stickleback fish.

ABSTRACT: How rapidly natural selection sorts genome-wide standing genetic variation during adaptation remains largely unstudied experimentally. Here, we present a genomic release-recapture experiment using paired threespine stickleback fish populations adapted to selectively different lake and stream habitats. First, we use pooled whole-genome sequence data from the original populations to identify hundreds of candidate genome regions likely under divergent selection between these habitats. Next, we generate F2 hybrids from the same lake-stream population pair in the laboratory and release thousands of juveniles into a natural stream habitat. Comparing the individuals surviving one year of stream selection to a reference sample of F2 hybrids allows us to detect frequency shifts across the candidate regions toward the genetic variants typical of the stream population-an experimental outcome consistent with polygenic directional selection. Our study reveals that adaptation in nature can be detected as a genome-wide signal over just a single generation.

SUBMITTER: Laurentino TG

PROVIDER: S-EPMC7174299 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Genomic release-recapture experiment in the wild reveals within-generation polygenic selection in stickleback fish.

Laurentino Telma G TG Moser Dario D Roesti Marius M Ammann Matthias M Frey Anja A Ronco Fabrizia F Kueng Benjamin B Berner Daniel D

Nature communications 20200421 1

How rapidly natural selection sorts genome-wide standing genetic variation during adaptation remains largely unstudied experimentally. Here, we present a genomic release-recapture experiment using paired threespine stickleback fish populations adapted to selectively different lake and stream habitats. First, we use pooled whole-genome sequence data from the original populations to identify hundreds of candidate genome regions likely under divergent selection between these habitats. Next, we gene ...[more]

PMID: 32317640

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Project description:Changing environments, whether through natural or anthropogenic causes, can lead to the loss of some selective pressures ('relaxed selection') and possibly even the reinstatement of selective agents not encountered for many generations ('reversed selection'). We examined the outcome of relaxed and reversed selection in the adaptive radiation of the threespine stickleback fish, Gasterostues aculeatus L., in which isolated populations encounter a variety of predation regimes. Oceanic stickleback, which represent the ancestral founders of the freshwater radiation, encounter many piscivorous fish. Derived, freshwater populations, on the other hand, vary with respect to the presence of predators. Some populations encounter native salmonids, whereas others have not experienced predation by large fish in thousands of generations (relax-selected populations). Some relax-selected populations have had sport fish, including rainbow trout, Oncorhynchus mykiss, introduced within the past several decades (reverse-selected). We examined the behavioural responses of stickleback from three populations of each type to simulated attacks by trout and birds to determine whether relaxed and reversed selection has led to divergence in behaviour, and whether this divergence was predator specific. Fish from trout-free populations showed weak responses to trout, as predicted, but these responses were similar to those of oceanic (ancestral) populations. Fish from populations that co-occur with trout, whether native or introduced, showed elevated antipredator responses, indicating that in freshwater, trout predation selects for enhanced antipredator responses, which can evolve extremely rapidly. Comparison of laboratory-reared and wild-caught individuals suggests a combination of learned and genetic components to this variation. Responses to a model bird flyover were weakly linked to predation environment, indicating that the loss of predation by trout may partially influence the evolution of responses to birds. Our results reject the hypothesis that the consistent presence of predatory birds has been sufficient to maintain responses to piscivorous fish under periods of relaxed selection.

Project description:BackgroundArtificial selection on quantitative traits using breeding values and selection indices in commercial livestock breeding populations causes changes in allele frequency over time at hundreds or thousands of causal loci and the surrounding genomic regions. In population genetics, this type of selection is called polygenic selection. Researchers and managers of pig breeding programs are motivated to understand the genetic basis of phenotypic diversity across genetic lines, breeds, and populations using selection mapping analyses. Here, we applied generation proxy selection mapping (GPSM), a genome-wide association analysis of single nucleotide polymorphism (SNP) genotypes (38,294-46,458 markers) of birth date, in four pig populations (15,457, 15,772, 16,595 and 8447 pigs per population) to identify loci responding to artificial selection over a period of five to ten years. Gene-drop simulation analyses were conducted to provide context for the GPSM results. Selected loci within and across each population of pigs were compared in the context of swine breeding objectives.ResultsThe GPSM identified 49 to 854 loci as under selection (Q-values less than 0.10) across 15 subsets of pigs based on combinations of populations. The number of significant associations increased when data were pooled across populations. In addition, several significant associations were identified in more than one population. These results indicate concurrent selection objectives, similar genetic architectures, and shared causal variants responding to selection across these pig populations. Negligible error rates (less than or equal to 0.02%) of false-positive associations were found when testing GPSM on gene-drop simulated genotypes, suggesting that GPSM distinguishes selection from random genetic drift in actual pig populations.ConclusionsThis work confirms the efficacy and the negligible error rates of the GPSM method in detecting selected loci in commercial pig populations. Our results suggest shared selection objectives and genetic architectures across swine populations. The identified polygenic selection highlights loci that are important to swine production.

Project description:BackgroundLong-term selection experiments are a powerful tool to understand the genetic background of complex traits. The longest of such experiments has been conducted in the Research Institute for Farm Animal Biology (FBN), generating extreme mouse lines with increased fertility, body mass, protein mass and endurance. For >140 generations, these lines have been maintained alongside an unselected control line, representing a valuable resource for understanding the genetic basis of polygenic traits. However, their history and genomes have not been reported in a comprehensive manner yet. Therefore, the aim of this study is to provide a summary of the breeding history and phenotypic traits of these lines along with their genomic characteristics. We further attempt to decipher the effects of the observed line-specific patterns of genetic variation on each of the selected traits.ResultsOver the course of >140 generations, selection on the control line has given rise to two extremely fertile lines (>20 pups per litter each), two giant growth lines (one lean, one obese) and one long-distance running line. Whole genome sequencing analysis on 25 animals per line revealed line-specific patterns of genetic variation among lines, as well as high levels of homozygosity within lines. This high degree of distinctiveness results from the combined effects of long-term continuous selection, genetic drift, population bottleneck and isolation. Detection of line-specific patterns of genetic differentiation and structural variation revealed multiple candidate genes behind the improvement of the selected traits.ConclusionsThe genomes of the Dummerstorf trait-selected mouse lines display distinct patterns of genomic variation harbouring multiple trait-relevant genes. Low levels of within-line genetic diversity indicate that many of the beneficial alleles have arrived to fixation alongside with neutral alleles. This study represents the first step in deciphering the influence of selection and neutral evolutionary forces on the genomes of these extreme mouse lines and depicts the genetic complexity underlying polygenic traits.

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Genomic release-recapture experiment in the wild reveals within-generation polygenic selection in stickleback fish.

Publications

Genomic release-recapture experiment in the wild reveals within-generation polygenic selection in stickleback fish.

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