Abstract

BackgroundExamples of rapid evolution are common in nature but difficult to account for with the standard population genetic model of adaptation. Instead, selection from the standing genetic variation permits rapid adaptation via soft sweeps or polygenic adaptation. Empirical evidence of this process in nature is currently limited but accumulating.ResultsWe provide genome-wide analyses of rapid evolution in Fundulus heteroclitus populations subjected to recently elevated temperatures due to coastal power station thermal effluents using 5449 SNPs across two effluent-affected and four reference populations. Bayesian and multivariate analyses of population genomic structure reveal a substantial portion of genetic variation that is most parsimoniously explained by selection at the site of thermal effluents. An FST outlier approach in conjunction with additional conservative requirements identify significant allele frequency differentiation that exceeds neutral expectations among exposed and closely related reference populations. Genomic variation patterns near these candidate loci reveal that individuals living near thermal effluents have rapidly evolved from the standing genetic variation through small allele frequency changes at many loci in a pattern consistent with polygenic selection on the standing genetic variation.ConclusionsWhile the ultimate trajectory of selection in these populations is unknown and we survey only a minority of genomic loci, our findings suggest that polygenic models of adaptation may play important roles in large, natural populations experiencing recent selection due to environmental changes that cause broad physiological impacts.

Highlights

  • Examples of rapid evolution are common in nature but difficult to account for with the standard population genetic model of adaptation

  • Functional genomic and phenotypic evidence suggestive of adaptation in natural Fundulus heteroclitus populations exposed to thermal effluents

  • F. heteroclitus populations were sampled in two “triads” [51], each consisting of a single thermal effluent (TE) site bordered on either side along the coast by a reference site (Fig. 1)

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Summary

Introduction

Examples of rapid evolution are common in nature but difficult to account for with the standard population genetic model of adaptation. Fixation of each adaptive allele leads to a strong selective signature among genomic variants in linkage disequilibrium with the causative mutation, producing a “hard sweep” [2] This model has provided a detailed set of predictions that form the basis of many empirical tests for selection [3, 4] and has been supported by population genetic examinations of candidate genes, where the genotype to phenotype map for known adaptive traits is well characterized [5, 6]. Examples of rapid phenotypic evolution abound in both the laboratory and in nature and can occur over time scales as short as tens

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