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How sexual selection can drive the evolution of costly sperm ornamentation

Nature volume 533, pages 535538 (26 May 2016) | Download Citation

Abstract

Post-copulatory sexual selection (PSS), fuelled by female promiscuity, is credited with the rapid evolution of sperm quality traits across diverse taxa1. Yet, our understanding of the adaptive significance of sperm ornaments and the cryptic female preferences driving their evolution is extremely limited1,2. Here we review the evolutionary allometry of exaggerated sexual traits (for example, antlers, horns, tail feathers, mandibles and dewlaps), show that the giant sperm of some Drosophila species are possibly the most extreme ornaments3,4 in all of nature and demonstrate how their existence challenges theories explaining the intensity of sexual selection, mating-system evolution and the fundamental nature of sex differences5,6,7,8,9. We also combine quantitative genetic analyses of interacting sex-specific traits in D. melanogaster with comparative analyses of the condition dependence of male and female reproductive potential across species with varying ornament size to reveal complex dynamics that may underlie sperm-length evolution. Our results suggest that producing few gigantic sperm evolved by (1) Fisherian runaway selection mediated by genetic correlations between sperm length, the female preference for long sperm and female mating frequency, and (2) longer sperm increasing the indirect benefits to females. Our results also suggest that the developmental integration of sperm quality and quantity renders post-copulatory sexual selection on ejaculates unlikely to treat male–male competition and female choice as discrete processes.

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Acknowledgements

The authors thank B. Reil for technical assistance and S. Dorus for helpful comments on the manuscript. Financial support for this research was provided by the National Science Foundation (grants DEB-9806649 to S.P. and DEB-1145965 to S.P., S.L., M.K.M. and J.M.B.), the Swiss National Science Foundation (Fellowships PA00P3_134191 and PZ00P3_154767 to S.L.), the National University of Singapore (Overseas Postdoctoral Fellowship to N.P.) and a generous gift from Mike and Jane Weeden to Syracuse University.

Author information

Author notes

    • Stefan Lüpold
    •  & Scott Pitnick

    These authors contributed equally to this work.

Affiliations

  1. Center for Reproductive Evolution, Department of Biology, Syracuse University, 107 College Place, Syracuse, New York 13244-1270, USA

    • Stefan Lüpold
    • , Mollie K. Manier
    • , Nalini Puniamoorthy
    • , Christopher Schoff
    • , William T. Starmer
    • , Shannon H. Buckley Luepold
    • , John M. Belote
    •  & Scott Pitnick
  2. Department of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland

    • Stefan Lüpold
  3. Department of Biological Sciences, The George Washington University, 800 22nd St. NW, Suite 6000, Washington DC 20052, USA

    • Mollie K. Manier
  4. Department of Biological Sciences, National University of Singapore, 14 Science Drive, SG 117543, Singapore

    • Nalini Puniamoorthy

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Contributions

S.P. and S.L. conceived the research. S.P. and C.S. performed the reproductive potential experiments. S.P., C.S. and W.T.S. collected data for sperm and egg production allometry. S.L., S.P., M.K.M. and J.M.B. performed the male–female trait genetic covariance experiments. S.P., S.L., N.P. and S.H.B.L. performed the sperm length condition dependence experiment. S.L. and W.T.S. performed all statistical analyses. S.P. and S.L. wrote the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Scott Pitnick.

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https://doi.org/10.1038/nature18005

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