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Arrest of sex-specific adaptation during the evolution of sexual dimorphism in Drosophila

Abstract

Sexually antagonistic selection arises when a trait expressed in both sexes (a shared trait) is selected towards different, sex-specific optima. Sex-discordant selection causes different alleles to be favoured in each sex (intralocus sexual conflict). A key parameter responsible for generating this conflict is the intersexual genetic correlation (rMF), which determines the degree to which heritable genetic variation for the shared trait produces a similar phenotype in both sexes. A strong, positive rMF interferes with adaptation when there is sex-discordant selection. In principle, the rMF can evolve in response to sex-discordant selection: the faster it declines, the faster the resolution of intralocus sexual conflict. Here, we use Drosophila melanogaster to quantify the time scale over which a strong, positive rMF impedes a response to sex-discordant selection for a canonical quantitative trait (body size) with an exceptionally long (250 generations) selection experiment for a complex multicellular organism. We found that, compared with rapid and substantial evolution under sex-concordant selection, a high rMF arrested sex-specific adaptation for 100 generations in females and a minimum of 250 generations in males. Our study demonstrates that a high rMF can lead to a protracted period of adaptive stalemate during the evolution of sexual dimorphism.

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Fig. 1: Male and female body size over time.
Fig. 2: Sexual dimorphism over time.
Fig. 3: Body size change in response to long-term selection.
Fig. 4: Changes in male and female body size.

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Acknowledgements

Funding during the early part of this study was provided by the NSF (DEB-0128780 and DEB-0410112) and NIH (1R01HD057974-01). Canisius College provided funding during the later parts of the study. We thank A. Pischedda, P. Miller and numerous undergraduate researchers at UCSB and Canisius College for assistance with the body size assays, and U. Frieberg and A. Pischedda for comments on earlier drafts of the manuscript.

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The idea for this study originated from discussions between A.D.S. and W.R.R. A.D.S conducted the experiments. A.D.S. and W.R.R. conducted the data analyses and drafted the manuscript.

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Correspondence to Andrew D. Stewart.

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Stewart, A.D., Rice, W.R. Arrest of sex-specific adaptation during the evolution of sexual dimorphism in Drosophila. Nat Ecol Evol 2, 1507–1513 (2018). https://doi.org/10.1038/s41559-018-0613-4

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