Abstract

Genomic and genetic methods allow investigation of how frequently the same genes are used by different populations during adaptive evolution, yielding insights into the predictability of evolution at the genetic level. We estimated the probability of gene reuse in parallel and convergent phenotypic evolution in nature using data from published studies. The estimates are surprisingly high, with mean probabilities of 0.32 for genetic mapping studies and 0.55 for candidate gene studies. The probability declines with increasing age of the common ancestor of compared taxa, from about 0.8 for young nodes to 0.1–0.4 for the oldest nodes in our study. Probability of gene reuse is higher when populations begin from the same ancestor (genetic parallelism) than when they begin from divergent ancestors (genetic convergence). Our estimates are broadly consistent with genomic estimates of gene reuse during repeated adaptation to similar environments, but most genomic studies lack data on phenotypic traits affected. Frequent reuse of the same genes during repeated phenotypic evolution suggests that strong biases and constraints affect adaptive evolution, resulting in changes at a relatively small subset of available genes. Declines in the probability of gene reuse with increasing age suggest that these biases diverge with time.

Highlights

  • Parallel and convergent evolution of traits in independent populations inhabiting similar environments (‘repeated phenotypic evolution’) implicates natural selection [1,2,3,4]

  • Some genes might contribute to adaptation more often than others because they have more standing genetic variation, higher mutation rates, larger effect sizes, more numerous beneficial mutations, fewer pleiotropic constraints, particular linkage relationships, or because they are involved in particular epistatic interactions with the genetic background [5 –12]

  • Results are plotted separately for measurements based on genetic cross methods and candidate gene methods

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Summary

Introduction

Parallel and convergent evolution of traits in independent populations inhabiting similar environments (‘repeated phenotypic evolution’) implicates natural selection [1,2,3,4]. Some genes might contribute to adaptation more often than others because they have more standing genetic variation, higher mutation rates, larger effect sizes, more numerous beneficial mutations, fewer pleiotropic constraints, particular linkage relationships, or because they are involved in particular epistatic interactions with the genetic background [5 –12]. Knowledge of these underlying effects and constraints might allow us to predict genetic evolution [5,8,9]. Instances of parallel and convergent phenotypic evolution provide an opportunity to measure the predictability of genetic changes underlying adaptation

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