Evolution of sexual cooperation from sexual conflict

Edited by James J. Bull, The University of Texas at Austin, Austin, TX, and approved September 22, 2019 (received for review March 11, 2019)
October 14, 2019
116 (46) 23225-23231

Significance

The past 50 y have seen much research on sexual selection. However, in many species, displays between the sexes continue long after pair formation, even if pairs have been together for years. As shown experimentally, such displays result in cooperation between the sexes, whereby displays by one partner affect investment into the brood by the other. How one gets to this cooperative outcome is not understood. We show such outcomes evolve if a novel display exploits a preexisting sensory bias that raises receiver investment. Once established, displays are maintained because they are required to stimulate the partner optimally. The pair bond is strengthened, and displays between the sexes accumulate over evolutionary time, even in the absence of sexual selection.

Abstract

In many species that form pair bonds, males display to their mate after pair formation. These displays elevate the female’s investment into the brood. This is a form of cooperation because without the display, female investment is reduced to levels that are suboptimal for both sexes. The presence of such displays is paradoxical as in their absence the male should be able to invest extra resources directly into offspring, to the benefit of both sexes. We consider that the origin of these displays lies in the exploitation of preexisting perceptual biases which increase female investment beyond that which is optimal for her, initially resulting in a sexual conflict. We use a combined population genetic and quantitative genetic model to show how this conflict becomes resolved into sexual cooperation. A cooperative outcome is most likely when perceptual biases are under selection pressures in other contexts (e.g., detection of predators, prey, or conspecifics), but this is not required. Cooperation between pair members can regularly evolve even when this provides no net advantage to the pair and when the display itself reduces a male’s contributions to raising the brood. The findings account for many interactions between the sexes that have been difficult to explain in the context of sexual selection.

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Data Availability

Data deposition: An interactive file is available at https://powers.shinyapps.io/pqreadr/, and C code is archived on Dryad.

Acknowledgments

We would like to thank and remember Alexander Kenan, who made valuable contributions to the development of this project while he was an undergraduate at University of North Carolina. We thank Nan Lyu, Carlos Servan, David Wheatcroft, Haven Wiley, and Justin Yeh for discussion. This project was funded in part by the National Science Foundation Grant DEB-0919018 to M.R.S. and the Norwegian Research Council’s Center of Excellence project SFF-III 223257 to R.L.

Supporting Information

Appendix (PDF)

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 116 | No. 46
November 12, 2019
PubMed: 31611370

Classifications

Data Availability

Data deposition: An interactive file is available at https://powers.shinyapps.io/pqreadr/, and C code is archived on Dryad.

Submission history

Published online: October 14, 2019
Published in issue: November 12, 2019

Keywords

  1. cooperation
  2. differential allocation
  3. sensory bias
  4. sexual conflict
  5. sexual stimulation

Acknowledgments

We would like to thank and remember Alexander Kenan, who made valuable contributions to the development of this project while he was an undergraduate at University of North Carolina. We thank Nan Lyu, Carlos Servan, David Wheatcroft, Haven Wiley, and Justin Yeh for discussion. This project was funded in part by the National Science Foundation Grant DEB-0919018 to M.R.S. and the Norwegian Research Council’s Center of Excellence project SFF-III 223257 to R.L.

Notes

This article is a PNAS Direct Submission.
See Commentary on page 22899.

Authors

Affiliations

Maria R. Servedio1
Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599;
John M. Powers1
Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599;
Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92617;
Russell Lande
Center for Biodiversity Dynamics, Norwegian University of Science and Technology, N-7491 Trondheim, Norway;
Department of Ecology and Evolution, University of Chicago, Chicago, IL 60637

Notes

2
To whom correspondence may be addressed. Email: [email protected].
Author contributions: M.R.S., R.L., and T.D.P. designed research; M.R.S., J.M.P., R.L., and T.D.P. performed research; and M.R.S., J.M.P., R.L., and T.D.P. wrote the paper.
1
M.R.S. and J.M.P. contributed equally to this work.

Competing Interests

The authors declare no competing interest.

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    Evolution of sexual cooperation from sexual conflict
    Proceedings of the National Academy of Sciences
    • Vol. 116
    • No. 46
    • pp. 22885-23363

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