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Higher rates of sex evolve in spatially heterogeneous environments

Abstract

The evolution and maintenance of sexual reproduction has puzzled biologists for decades1,2. Although this field is rich in hypotheses3,4,5, experimental evidence is scarce. Some important experiments have demonstrated differences in evolutionary rates between sexual and asexual populations6,7,8; other experiments have documented evolutionary changes in phenomena related to genetic mixing, such as recombination9,10 and selfing11. However, direct experiments of the evolution of sex within populations are extremely rare (but see ref. 12). Here we use the rotifer, Brachionus calyciflorus, which is capable of both sexual and asexual reproduction, to test recent theory13,14,15 predicting that there is more opportunity for sex to evolve in spatially heterogeneous environments. Replicated experimental populations of rotifers were maintained in homogeneous environments, composed of either high- or low-quality food habitats, or in heterogeneous environments that consisted of a mix of the two habitats. For populations maintained in either type of homogeneous environment, the rate of sex evolves rapidly towards zero. In contrast, higher rates of sex evolve in populations experiencing spatially heterogeneous environments. The data indicate that the higher level of sex observed under heterogeneity is not due to sex being less costly or selection against sex being less efficient; rather sex is sufficiently advantageous in heterogeneous environments to overwhelm its inherent costs2. Counter to some alternative theories16,17 for the evolution of sex, there is no evidence that genetic drift plays any part in the evolution of sex in these populations.

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Figure 1: Fitness in alternative environments.
Figure 2: Evolution of the propensity for sex in Brachionus calyciflorus populations from spatially heterogeneous and spatially homogeneous environments measured in a common environment.
Figure 3: In situ measure of the rate of sex in Brachionus calyciflorus populations from spatially heterogeneous and spatially homogeneous environments measured as the fraction of sexually derived offspring (resting eggs) of total offspring.

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Acknowledgements

We thank C. Kearns and N. G. Hairston Jr for providing the sediment with resting eggs from which the Brachionus cultures were established. This research was funded by the Volkswagen Foundation to L.B. (I/83 517) and the Natural Sciences and Engineering Research Council (Canada) to A.F.A.

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L.B. and A.F.A. conceived and designed the study, L.B. performed experiments, L.B. and A.F.A. discussed and analysed the results, and shared the writing of the paper.

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Correspondence to Lutz Becks.

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The authors declare no competing financial interests.

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Becks, L., Agrawal, A. Higher rates of sex evolve in spatially heterogeneous environments. Nature 468, 89–92 (2010). https://doi.org/10.1038/nature09449

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