Radical environmental change that provokes population decline can impose constraints on the sources of genetic variation that may enable evolutionary rescue. Adaptive toxicant resistance has rapidly evolved in Gulf killifish (Fundulus grandis) that occupy polluted habitats. We show that resistance scales with pollution level and negatively correlates with inducibility of aryl hydrocarbon receptor (AHR) signaling. Loci with the strongest signatures of recent selection harbor genes regulating AHR signaling. Two of these loci introgressed recently (18 to 34 generations ago) from Atlantic killifish (F. heteroclitus). One introgressed locus contains a deletion in AHR that confers a large adaptive advantage [selection coefficient (s) = 0.8]. Given the limited migration of killifish, recent adaptive introgression was likely mediated by human-assisted transport. We suggest that interspecies connectivity may be an important source of adaptive variation during extreme environmental change.
Geographically separated populations can convergently adapt to the same selection pressure. Convergent evolution at the level of a gene may arise via three distinct modes. The selected alleles can (1) have multiple independent mutational origins, (2) be shared due to shared ancestral standing variation, or (3) spread throughout subpopulations via gene flow. We present a model-based, statistical approach that utilizes genomic data to detect cases of convergent adaptation at the genetic level, identify the loci involved and distinguish among these modes. To understand the impact of convergent positive selection on neutral diversity at linked loci, we make use of the fact that hitchhiking can be modeled as an increase in the variance in neutral allele frequencies around a selected site within a population. We build on coalescent theory to show how shared hitchhiking events between subpopulations act to increase covariance in allele frequencies between subpopulations at loci near the selected site, and extend this theory under different models of migration and selection on the same standing variation. We incorporate this hitchhiking effect into a multivariate normal model of allele frequencies that also accounts for population structure. Based on this theory, we present a composite-likelihood-based approach that utilizes genomic data to identify loci involved in convergence, and distinguishes among alternate modes of convergent adaptation. We illustrate our method on genome-wide polymorphism data from two distinct cases of convergent adaptation. First, we investigate the adaptation for copper toxicity tolerance in two populations of the common yellow monkey flower, We show that selection has occurred on an allele that has been standing in these populations prior to the onset of copper mining in this region. Lastly, we apply our method to data from four populations of the killifish,, that show very rapid convergent adaptation for tolerance to industrial pollutants. Here, we identify a single locus at which both independent mutation events and selection on an allele shared via gene flow, either slightly before or during selection, play a role in adaptation across the species' range.
1Geographically separated populations can convergently adapt to the same selection pressure. Convergent 2 evolution at the level of a gene may arise via three distinct modes. The selected alleles can (1) have 3 multiple independent mutational origins, (2) be shared due to shared ancestral standing variation, or (3) 4 spread throughout subpopulations via gene flow. We present a model-based, statistical approach that utilizes 5 genomic data to detect cases of convergent adaptation at the genetic level, identify the loci involved and 6 distinguish among these modes. To understand the impact of convergent positive selection on neutral 7 diversity at linked loci, we make use of the fact that hitchhiking can be modeled as an increase in the 8 variance in neutral allele frequencies around a selected site within a population. We build on coalescent 9 theory to show how shared hitchhiking events between subpopulations act to increase covariance in allele 10 frequencies between subpopulations at loci near the selected site, and extend this theory under different 11 models of migration and selection on the same standing variation. We incorporate this hitchhiking effect 12 into a multivariate normal model of allele frequencies that also accounts for population structure. Based 13 on this theory, we present a composite-likelihood-based approach that utilizes genomic data to identify loci 14 involved in convergence, and distinguishes among alternate modes of convergent adaptation. We illustrate 15 our method on genome-wide polymorphism data from two distinct cases of convergent adaptation. First, we 16 investigate the adaptation for copper toxicity tolerance in two populations of the common yellow monkey 17 flower, Mimulus guttatus. We show that selection has occurred on an allele that has been standing in these 18 populations prior to the onset of copper mining in this region. Lastly, we apply our method to data from four
Convergent adaptation is the independent evolution of similar traits conferring a fitness advantage in two or more lineages. Cases of convergent adaptation inform our ideas about the ecological and molecular basis of adaptation. In judging the degree to which putative cases of convergent adaptation provide an independent replication of the process of adaptation, it is necessary to establish the degree to which the evolutionary change is unexpected under null models and to show that selection has repeatedly, independently driven these changes. Here, we discuss the issues that arise from these questions particularly for closely related populations, where gene flow and standing variation add additional layers of complexity. We outline a conceptual framework to guide intuition as to the extent to which evolutionary change represents the independent gain of information owing to selection and show that this is a measure of how surprised we should be by convergence. Additionally, we summarize the ways population and quantitative genetics and genomics may help us address questions related to convergent adaptation, as well as open new questions and avenues of research. This article is part of the theme issue ‘Convergent evolution in the genomics era: new insights and directions’.
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