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Genomics of a sexually selected sperm ornament and female preference in Drosophila

Nature Ecology & Evolution (2024)Cite this article

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Abstract

Our understanding of animal ornaments and the mating preferences driving their exaggeration is limited by knowledge of their genetics. Post-copulatory sexual selection is credited with the rapid evolution of female sperm-storage organ morphology and corresponding sperm quality traits across diverse taxa. In Drosophila, the mechanisms by which longer flagella convey an advantage in the competition among sperm for limited storage space in the female, and by which female sperm-storage organ morphology biases fertilization in favour of longer sperm have been resolved. However, the evolutionary genetics underlying this model post-copulatory ornament and preference system have remained elusive. Here we combined comparative analyses of 149 Drosophila species, a genome-wide association study in Drosophila melanogaster and molecular evolutionary analysis of ~9,400 genes to elucidate how sperm and female sperm-storage organ length co-evolved into one of nature’s most extreme ornaments and preferences. Our results reveal a diverse repertoire of pleiotropic genes linking sperm length and seminal receptacle length expression to central nervous system development and sensory biology. Sperm length development appears condition-dependent and is governed by conserved hormonal (insulin/insulin-like growth factor) and developmental (including Notch and Fruitless) pathways. Central developmental pathway genes, including Notch, also comprised the majority of a restricted set of genes contributing to both intraspecific and interspecific variation in sperm length. Our findings support ‘good genes’ models of female preference evolution.

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Fig. 1: Sperm length and female SR length have co-evolved across the drosophilid tree of life.
Fig. 2: Intraspecific phenotypic and genetic variation in sperm length and SR length are not correlated.
Fig. 3: Sperm length genes are biased towards expression in the CNS and sensory organs, as well as during the post-meiotic phase of spermatogenesis in the testes.
Fig. 4: Effect size distributions suggest different selective histories for genetic variants underlying sperm length and SR length expression.
Fig. 5: Correlated gene evolution with ornament and/or preference diversification reveals functionally relevant expression patterns.

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All data are available in the Supplementary Information accompanying this paper.

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Acknowledgements

We thank the National Drosophila Species Stock Center and the Artyom Kopp laboratory for providing fly cultures and technical support; E. Sedore and L. Pekowsky for assistance with Syracuse University’s OrangeGrid; B. Woolsey for graphic design assistance; S. Buel for technical assistance; and members of the Center for Reproductive Evolution for intellectual support. This research was funded by the National Science Foundation (grant nos. DEB-1811805 to S.P. and S.D.; DEB-1655840 to S.D. and S.P.; DEB-2011045 to R.A.G.; DEB-2030129, DEB-1839598 and DEB-1241253 to P.M.O.), the National Institutes of Health (grant no. R35GM147454 to Y.H.A.-B,), a Syracuse University Postdoctoral Fellowship (to S.D. and S.P.) and a generous gift from M. and J. Weeden to Syracuse University.

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Authors and Affiliations

  1. Center for Reproductive Evolution, Department of Biology, Syracuse University, Syracuse, NY, USA

    Zeeshan A. Syed, R. Antonio Gomez, Kirill Borziak, Amaar Asif, Abelard S. Cong, Peter Wengert, Caitlin McDonough-Goldstein, Yasir H. Ahmed-Braimah, Steve Dorus & Scott Pitnick

  2. Department of Entomology, Cornell University, Ithaca, NY, USA

    Patrick. M. O’Grady

  3. Department of Biology, Stanford University, Stanford, CA, USA

    Bernard Y. Kim & Dmitri A. Petrov

  4. Department of Biological Sciences, Virginia Tech, Blacksburg, VA, USA

    Anton Suvorov

  5. Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland

    Stefan Lüpold

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Contributions

Conceptualization: S.P., S.D., Z.A.S., D.A.P. Methodology: S.D., S.P., Z.A.S., K.B., R.A.G., B.Y.K. Investigation: Z.A.S., S.P., S.D., R.A.G., K.B., A.A., A.S.C., S.L., B.Y.K., P.M.O., P.W., Y.H.A.-B., C.M.-G. Funding acquisition: S.P., S.D., R.A.G., P.M.O., D.A.P. Project administration: S.P., S.D., P.M.O., B.Y.K. Supervision: S.P., S.D., Z.A.S., D.A.P. Writing—original draft: S.D., S.P., Z.A.S., R.A.G. Writing—review and editing: S.P., S.D., Z.A.S., R.A.G., S.L., B.Y.K., Y.H.A.-B.

Corresponding authors

Correspondence to Zeeshan A. Syed, Steve Dorus or Scott Pitnick.

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Nature Ecology and Evolution thanks Jacek Radwan, Murielle Ålund and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–10 and Table 1.

Reporting Summary

Supplementary Data 1

Sperm length, seminal receptacle length and body size data for 149 drosophilid species.

Supplementary Data 2

Sperm length and seminal receptacle length data for Drosophila Genetic Reference Panel lines.

Supplementary Data 3

Allelic information for genome-wide association study of sperm length and seminal receptacle length.

Supplementary Data 4

Gene information on significant sperm length and seminal receptacle length variants from genome-wide association studies.

Supplementary Data 5

Gene Ontology/Biological Process assessment for sperm and seminal receptacle length genome-wide association study.

Supplementary Data 6

Results of molecular evolutionary and network interaction analyses of significant sperm and/ or seminal receptacle length genes identified in Coevol analysis.

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Syed, Z.A., Gomez, R.A., Borziak, K. et al. Genomics of a sexually selected sperm ornament and female preference in Drosophila. Nat Ecol Evol (2024). https://doi.org/10.1038/s41559-024-02587-2

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