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The development, evaluation, and illustration of a timeline procedure for testing the role of sperm competition in the evolution of sexual traits using paternity data

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Abstract

The empirical study of the role of sperm competition in the evolution of sexual traits has historically been problematic through the inability either to measure sperm competition levels directly in the present or to reconstruct changes in the evolutionary past. Here, we develop and test a procedure based on paternity data that potentially permits both. For our pilot study, we use the rate of change of the seminal protein gene SEMG2 for catarrhine primates published by Dorus et al. (Nat Genet 36:1326–1329, 2004). From their data, Dorus et al. proposed a two-part hypothesis: (1) sperm competition plays a role in the evolution of the SEMG2 gene and (2) higher levels of sperm competition generate more positive selection for change in SEMG2 than lower levels. Dorus et al. were limited, however, by being able to use only proxy measures of sperm competition and only seven “recent” segments of catarrhine primate phylogeny. Here, we develop a “timeline procedure” that permits the Dorus hypothesis to be tested using data from across the whole of catarrhine phylogeny. Our analysis supports part (1) of the Dorus hypothesis but questions part (2), suggesting instead that changes in level of sperm competition have a more powerful influence on the rate of evolution of traits than the level of sperm competition itself. We conclude that the timeline procedure developed here could be a valuable investigative tool in the role of sperm competition in the evolution of sexual traits measured over evolutionary time such as SEMG2.

Significance statement

The empirical study of the role of sperm competition in the evolution of sexual traits has historically been problematic through the inability to measure sperm competition levels directly in the present and to reconstruct changes in the evolutionary past. Here, we test a “timeline procedure” based on paternity data that potentially permits both. For our pilot study, we use the rate of change of the seminal protein gene SEMG2 for catarrhine primates published by Dorus et al. (Nat Genet 36:1326–1329, 2004). Whereas Dorus et al. were limited to using proxy measures for only “recent” segments of catarrhine primate phylogeny, our method permits direct measures of sperm competition to be applied across the whole of Catarrhine phylogeny. We conclude that this new procedure could be valuable for investigation of the role of sperm competition in the evolution of a wide range of sexual traits.

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Acknowledgments

We thank Holger Herlyn for many helpful suggestions for the improvement of our manuscript. We also thank an anonymous reviewer for an extensive and detailed review of our original submission. It was an example of constructive reviewing at its best, and our paper is stronger and better organized as a result.

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Correspondence to Todd K. Shackelford.

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The authors declare that they have no conflicts of interest.

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As all data for catarrhines used here are from published studies by other authors, the protocol and procedures did not require review and approval by the IACUC or other institutional ethics committees overseeing the use of humans or other animals in research in either the USA or the UK. The study also adhered to the American Society of Primatologists Principles for the Ethical Treatment of Non-Human Primates.

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All data generated or analyzed for this study are included in this published article and its supplementary information file.

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Communicated by E. Huchard

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Baker, R.R., Shackelford, T.K. The development, evaluation, and illustration of a timeline procedure for testing the role of sperm competition in the evolution of sexual traits using paternity data. Behav Ecol Sociobiol 74, 106 (2020). https://doi.org/10.1007/s00265-020-02889-y

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  • DOI: https://doi.org/10.1007/s00265-020-02889-y

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