Abstract
Rapid and divergent evolution of male genital morphology is a conspicuous and general pattern across internally fertilizing animals. Rapid genital evolution is thought to be the result of sexual selection, and the role of natural selection in genital evolution remains controversial. However, natural and sexual selection are believed to act antagonistically on male genital form. We conducted an experimental evolution study to investigate the combined effects of natural and sexual selection on the genital-arch lobes of male Drosophila simulans. Replicate populations were forced to evolve under lifetime monogamy (relaxed sexual selection) or lifetime polyandry (elevated sexual selection) and two temperature regimes, 25°C (relaxed natural selection) or 27°C (elevated natural selection) in a fully factorial design. We found that natural and sexual selection plus their interaction caused genital evolution. Natural selection caused some aspects of genital form to evolve away from their sexually selected shape, whereas natural and sexual selection operated in the same direction for other shape components. Additionally, sexual and natural selection tended to favour larger genitals. Thus we find that the underlying selection driving genital evolution is complex, does not only involve sexual selection, and that natural selection and sexual selection do not always act antagonistically.
Highlights
The extreme diversity of male genital morphology across animals with internal fertilization is a conspicuous and general trend [1]
Evolution of RW3 was similar in that elevated natural selection in the absence of sexual selection (+N-S) caused genitals to evolve in the direction of the consensus shape and natural and sexual selection again appeared to be selecting genital shape in different directions
We have shown with a formal selection analysis of precopulatory sexual selection on male D. simulans, that sexual selection does not differ across temperatures (Ingleby et al unpublished) and male attractiveness is consistent across temperatures [35]
Summary
The extreme diversity of male genital morphology across animals with internal fertilization is a conspicuous and general trend [1]. Natural selection was invoked to explain male genital evolution, but the current consensus is that sexual selection is primarily responsible for this rapid, divergent evolution [1,2,3]. Compelling evidence for this comes from comparative work showing that genitals are more complex and evolve more rapidly in species with elevated post-copulatory sexual selection [3]. The combined influences of natural and sexual selection acting on genitalia have rarely been investigated empirically [6,17,18] and claims that natural selection acts on genital form remain extremely controversial [1,2,14,19]
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