Population genomics perspectives on convergent adaptation

Abstract

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'.

Keywords: adaptation; convergence; convergent adaptation; information theory; population genomics.

Figure 1.

Allele frequency trajectories (red) at a single locus for two or more populations. (a) The allele was standing in the ancestor of three populations where it was fixed in populations 1 and 3 but lost in population 2. This case of incomplete lineage sorting (ILS) may falsely resemble independent mutations in populations 1 and 3, but may still be convergent adaptation if selection for the allele occurred twice independently (e.g. onsets of selection marked by blue triangles). (b) The beneficial allele was standing in the ancestral population of our present-day populations. Selection started when the ancestral allele frequency was x_1A and increased in frequency such that it was at x_2A when the populations split. Then, it continued to increase in both daughter populations to fixation. (c) The beneficial allele arose in a single present-day population and spread via introgression into the other population. The allele was at frequency x₁ at the onset of selection and migrated into the recipient population at frequency p where it also increased in frequency to fixation.

Figure 2.

Patterns generated under scenarios of convergent adaptation and not truly convergent (i.e. not independent) adaptation. (a) Haplotypic diversity in the ancestral population is shown. Each line represents an individual chromosome. (b) The four scenarios considered are depicted with yellow stars representing mutations at the beneficial locus, and red lines on the phylogenies when selection occurred. The scenarios are: (i) independent mutations, (ii) independent selection on ancestral standing variation, (iii) introgression, and (iv) selection in the ancestral population. (c) Panels for each of the four scenarios contain a cartoon representation of the haplotypic patterns surrounding the beneficial allele (black dot) in the two selected populations after fixation and a gene tree relating the populations at the beneficial allele. Pink regions in the haplotypes represent new mutations. (d) Within- and between-population conacestry coefficients for the four scenarios are shown as a function of recombination distance from the beneficial allele. Both gene trees and coancestry coefficients were derived from simulations briefly outlined in appendix Ab.