Global adaptation complicates the interpretation of genome scans for local adaptation

Abstract

Spatially varying selection promotes variance in allele frequencies, increasing genetic differentiation between the demes of a metapopulation. For that reason, outliers in the genome‐wide distribution of summary statistics measuring genetic differentiation, such as F _ST , are often interpreted as evidence for alleles that contribute to local adaptation. However, theoretical studies have shown that in spatially structured populations the spread of beneficial mutations with spatially uniform fitness effects can also induce transient genetic differentiation. In recent years, numerous empirical studies have suggested that such species‐wide, or global, adaptation makes a substantial contribution to molecular evolution. In this perspective, we discuss how commonly such global adaptation may influence the genome‐wide distribution of F _ST and generate genetic differentiation patterns, which could be mistaken for local adaptation. To illustrate this, we use forward‐in‐time population genetic simulations assuming parameters for the rate and strength of beneficial mutations consistent with estimates from natural populations. We demonstrate that the spread of globally beneficial mutations in parapatric populations may frequently generate F _ST outliers, which could be misinterpreted as evidence for local adaptation. The spread of beneficial mutations causes selective sweeps at flanking sites, so in some cases, the effects of global versus local adaptation may be distinguished by examining patterns of nucleotide diversity within and between populations in addition to F _ST . However, when local adaptation has been only recently established, it may be much more difficult to distinguish from global adaptation, due to less accumulation of linkage disequilibrium at flanking sites. Through our discussion, we conclude that a large fraction of F _ST outliers that are presumed to arise from local adaptation may instead be due to global adaptation.