Patterns of speciation and parallel genetic evolution under adaptation from standing variation

Abstract

When isolated populations adapt to novel environments, they may do so using the same or different alleles. Use of the same alleles - parallel genetic evolution - is increasingly likely if populations have shared ancestral standing genetic variation. Here, we investigate the conditions under which populations undergo parallel genetic evolution from standing variation and the associated implications for speciation via environment-specific hybrid fitness. Using computer simulations, we find that populations adapting to identical environments tend to fix the same alleles from standing variation unless there is a deficient or excess amount of variation in the founding population. We also find that the degree of parallel genetic adaptation decreases faster-than-linearly as selection deviates from fully parallel toward divergent. This rapid decrease in parallelism occurs because seemingly small environmental differences among populations correspond to steep reductions in the fraction of alleles that are mutually beneficial. Lastly, we show that adaptation from standing variation reduces the phenotypic segregation variance of hybrids under both parallel and divergent selection. Under parallel selection, parental populations fix the same alleles which do not segregate in hybrids. In addition, adaptation from standing variation proceeds via a greater number of alleles with individually smaller effects than when adaptation is from new mutation - this further reduces segregation variance even under divergent selection. This reduced segregation variance improves mean hybrid fitness when parents adapt to similar environments but reduces mean hybrid fitness under divergent adaptation. Therefore adaptation from standing variation forestalls speciation via parallel selection and promotes speciation via divergent selection.