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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.

SUBMITTER: Moerman F

PROVIDER: S-EPMC7336843 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Populations that expand their range can undergo rapid evolutionary adaptation of life-history traits, dispersal behaviour and adaptation to the local environment. Such adaptation may be aided or hindered by sexual reproduction, depending on the context. However, few empirical and experimental studies have investigated the genetic basis of adaptive evolution during range expansions. Even less attention has been given to the question how sexual reproduction may modulate such adaptive evolution during range expansions. We here studied genomic adaptation during experimental range expansions of the protist Tetrahymena thermophila in landscapes with a uniform environment or a pH gradient. Specifically, we investigated two aspects of genomic adaptation during range expansion. First, we investigated adaptive genetic change in terms of the underlying numbers of allele frequency changes from standing genetic variation and de novo variants. We focused on how sexual reproduction may alter this adaptive genetic change. Second, we identified genes subject to selection caused by the expanding range itself, and directional selection due to the presence or absence of the pH gradient. We focused this analysis on alleles with large frequency changes that occurred in parallel in more than one population to identify the most likely candidate targets of selection. We found that sexual reproduction altered adaptive genetic change both in terms of de novo variants and standing genetic variation. However, sexual reproduction affected allele frequency changes in standing genetic variation only in the absence of long-distance gene flow. Adaptation to the range expansion affected genes involved in cell divisions and DNA repair, whereas adaptation to the pH gradient additionally affected genes involved in ion balance and oxidoreductase reactions. These genetic changes may result from selection on growth and adaptation to low pH. In the absence of gene flow, sexual reproduction may have aided genetic adaptation. Gene flow may have swamped expanding populations with maladapted alleles, thus reducing the extent of evolutionary adaptation during range expansion. Sexual reproduction also altered the genetic basis of adaptation in our evolving populations via de novo variants, possibly by purging deleterious mutations or by revealing fitness benefits of rare genetic variants.

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

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