The phoenix hypothesis of speciation

Abstract

Genetic divergence among allopatric populations builds reproductive isolation over time. This process is accelerated when populations face a changing environment that allows large-effect mutational differences to accumulate, but abrupt change also places populations at risk of extinction. Here we use simulations of Fisher's geometric model with explicit population dynamics to explore the genetic changes that occur in the face of environmental changes. Because evolutionary rescue leads to the fixation of mutations whose phenotypic effects are larger on average compared with populations not at risk of extinction, these mutations are thus more likely to lead to reproductive isolation. We refer to the formation of new species from the ashes of populations in decline as the phoenix hypothesis of speciation. The phoenix hypothesis predicts more substantial hybrid fitness breakdown among populations surviving a higher extinction risk. The hypothesis was supported when many loci underlie adaptation. With only a small number of potential rescue mutations, however, mutations that fixed in different populations were more likely to be identical, with such parallel changes reducing isolation. Consequently, reproductive isolation builds fastest in populations subject to an intermediate extinction risk, given a limited number of mutations available for adaptation.