Dataset Information

The Linked Selection Signature of Rapid Adaptation in Temporal Genomic Data.

ABSTRACT: The majority of empirical population genetic studies have tried to understand the evolutionary processes that have shaped genetic variation in a single sample taken from a present-day population. However, genomic data collected over tens of generations in both natural and laboratory populations are increasingly used to find selected loci underpinning adaptation over these short timescales. Although these studies have been quite successful in detecting selection on large-effect loci, the fitness differences between individuals are often polygenic, such that selection leads to allele frequency changes that are difficult to distinguish from genetic drift. However, one promising signal comes from polygenic selection's effect on neutral sites that become stochastically associated with the genetic backgrounds that lead to fitness differences between individuals. Previous theoretical work has established that the random associations between a neutral allele and heritable fitness backgrounds act to reduce the effective population size experienced by this neutral allele. These associations perturb neutral allele frequency trajectories, creating autocovariance in the allele frequency changes across generations. Here, we show how temporal genomic data allow us to measure the temporal autocovariance in allele frequency changes and characterize the genome-wide impact of polygenic selection. We develop expressions for these temporal autocovariances, showing that their magnitude is determined by the level of additive genetic variation, recombination, and linkage disequilibria in a region. Furthermore, by using analytic expressions for the temporal variances and autocovariances in allele frequency, we demonstrate that one can estimate the additive genetic variation for fitness and the drift-effective population size from temporal genomic data. We also show how the proportion of total variation in allele frequency change due to linked selection can be estimated from temporal data. Overall, we demonstrate that temporal genomic data offer opportunities to identify the role of linked selection on genome-wide diversity over short timescales, and can help bridge population genetic and quantitative genetic studies of adaptation.

SUBMITTER: Buffalo V

PROVIDER: S-EPMC6827383 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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The Linked Selection Signature of Rapid Adaptation in Temporal Genomic Data.

Buffalo Vince V Coop Graham G

Genetics 20190926 3

The majority of empirical population genetic studies have tried to understand the evolutionary processes that have shaped genetic variation in a single sample taken from a present-day population. However, genomic data collected over tens of generations in both natural and laboratory populations are increasingly used to find selected loci underpinning adaptation over these short timescales. Although these studies have been quite successful in detecting selection on large-effect loci, the fitness ...[more]

PMID: 31558582

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Project description:Despite evolutionary biology's obsession with natural selection, few studies have evaluated multi-generational series of patterns of selection on a genome-wide scale in natural populations. Here, we report on a nine-year population-genomic survey of the microcrustacean Daphnia pulex. The genome-sequences of > 800 isolates provide insights into patterns of selection that cannot be obtained from long-term molecular-evolution studies, including the pervasiveness of near quasi-neutrality across the genome (mean net selection coefficients near zero, but with significant temporal variance about the mean, and little evidence of positive covariance of selection across time intervals), the preponderance of weak negative selection operating on minor alleles, and a genome-wide distribution of numerous small linkage islands of observable selection influencing levels of nucleotide diversity. These results suggest that fluctuating selection is a major determinant of standing levels of variation in natural populations, challenge the conventional paradigm for interpreting patterns of nucleotide diversity and divergence, and motivate the need for the development of new theoretical expressions for the interpretation of population-genomic data.SignificanceExcept for mono/oligogenic traits known in advance to be under strong selection, there is little information on genome-wide patterns of temporal dynamics of allele-frequency changes in well-defined and unmanipulated natural populations. A multi-year survey of a population of the microcrustacean Daphnia pulex provides insight into these matters. Genome-wide analysis of > 800 genetic isolates demonstrates that temporal variation in selection intensity is a major determinant of levels of nucleotide polymorphism and divergence. Most nucleotide sites experience fluctuating selection with mean selection coefficients near zero, with little covariance in the strength of selection across time intervals, and with selection distributed across large numbers of genomic islands of linked sites. These results raise challenges for the conventional interpretation of measures of nucleotide diversity and divergence as indicators of effective population sizes and intensities of positive/negative selection.

Dataset Information

The Linked Selection Signature of Rapid Adaptation in Temporal Genomic Data.

Publications

The Linked Selection Signature of Rapid Adaptation in Temporal Genomic Data.

Similar Datasets

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