Abstract
BackgroundOne of the big remaining challenges in evolutionary biology is to understand the evolution and maintenance of meiotic recombination. As recombination breaks down successful genotypes, it should be selected for only under very limited conditions. Yet, recombination is very common and phylogenetically widespread. The Red Queen Hypothesis is one of the most prominent hypotheses for the adaptive value of recombination and sexual reproduction. The Red Queen Hypothesis predicts an advantage of recombination for hosts that are coevolving with their parasites. We tested predictions of the hypothesis with experimental coevolution using the red flour beetle, Tribolium castaneum, and its microsporidian parasite, Nosema whitei.ResultsBy measuring recombination directly in the individuals under selection, we found that recombination in the host population was increased after 11 generations of coevolution. Detailed insights into genotypic and phenotypic changes occurring during the coevolution experiment furthermore helped us to reconstruct the coevolutionary dynamics that were associated with this increase in recombination frequency. As coevolved lines maintained higher genetic diversity than control lines, and because there was no evidence for heterozygote advantage or for a plastic response of recombination to infection, the observed increase in recombination most likely represented an adaptive host response under Red Queen dynamics.ConclusionsThis study provides direct, experimental evidence for an increase in recombination frequency under host-parasite coevolution in an obligatory outcrossing species. Combined with earlier results, the Red Queen process is the most likely explanation for this observation.
Highlights
One of the big remaining challenges in evolutionary biology is to understand the evolution and maintenance of meiotic recombination
One hypothesis for the adaptive value of recombination, the Red Queen Hypothesis [2,3,4], suggests that parasites play an important role in maintaining non-zero recombination rates in their hosts
The evolution and maintenance of recombination rate is rarely directly addressed, as most tests deal with the question of what favours sexual over asexual reproduction [20,21], without considering how parasitism may change recombination rate within a sexual host population itself
Summary
One of the big remaining challenges in evolutionary biology is to understand the evolution and maintenance of meiotic recombination. Direct experimental support for a change in recombination rate compatible with the Red Queen Hypothesis in obligatory outcrossing species has so far only been reported in one of our earlier studies using Tribolium castaneum as the host and Nosema whitei as its parasite [29]. This finding could not be confirmed in a follow-up study [30], yet post-hoc checks suggested that the extant genetic variation in the hosts probably was too small to sustain an adaptive response This finding could not be confirmed in a follow-up study [30], yet post-hoc checks suggested that the extant genetic variation in the hosts probably was too small to sustain an adaptive response (unpubl. data)
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