Gene swamping alters evolution during range expansions in the protist Tetrahymena thermophila

Abstract

At species’ range edges, individuals often face novel environmental conditions that may limit range expansion until populations adapt. The potential to adapt depends on genetic variation upon which selection can act. However, populations at species’ range edges are often genetically depauperate. One mechanism increasing genetic variation is reshuffling existing variation through sex. Sex, however, can potentially limit adaptation by breaking up existing beneficial allele combinations (recombination load). The gene swamping hypothesis predicts this is specifically the case when populations expand along an abiotic gradient and asymmetric dispersal leads to numerous maladapted dispersers from the range core swamping the range edge. We used the ciliate Tetrahymena thermophila as a model for testing the gene swamping hypothesis. We performed replicated range expansions in landscapes with or without a pH-gradient, while simultaneously manipulating the occurrence of gene flow and sexual versus asexual reproduction. We show that sex accelerated evolution of local adaptation in the absence of gene flow, but hindered it in the presence of gene flow. However, sex affected adaptation independently of the pH-gradient, indicating that both abiotic gradients and the biotic gradient in population density lead to gene swamping. Overall, our results show that gene swamping alters adaptation in life-history strategies.