Male mating displays can evolve from exploitative origins to cooperative endings

October 28, 2019
116 (46) 22899-22900
Research Article
Evolution of sexual cooperation from sexual conflict
Maria R. Servedio, John M. Powers [...] Trevor D. Price
Animal mating displays provide some of nature’s most dramatic and curious spectacles. Ring doves (Streptopelia risoria) are a case in point (Fig. 1). According to Cheng (ref. 1, p. 2), “When a male ring dove courts a female, he starts with majestic bowing and cooing (bow coo) interspersed with strutting directed toward the female… At some point the male … stops cooing and turns to chasing, strutting, and bow cooing; this … causes the female to flee. The male then resumes nest cooing, and the ritual repeats itself.”
Fig. 1.
A pair of ring doves (S. risoria) crossing. Image courtesy of Todd Petit (photographer).
What could explain such elaborate mating behavior? Evolutionary biologists have been puzzling over this question since Darwin (2, 3). Many striking examples of mating displays, including the large male antlers of red deer Cervus elaphas (4), the deafening calls of male common toads Bufo bufo (5), and the bright red male dewlaps of Carolina anole lizards Anolis carolinensis (6), have evolved by sexual selection, which is driven by an association between the trait display and mating success (7).
Species like the ring doves, however, are pair bonded and effectively offer no variation in the number of mates a male can have each season. This excludes sexual selection as an explanation for their exaggerated mating displays. Instead, male displays appear to stimulate female investment in reproduction (8). From an adaptive evolutionary standpoint, this is unexpected since a male’s efforts would be better spent contributing resources directly to his offspring and the female would be better off ignoring such displays if her investment in the brood is already optimal. When a male displays to a receptive female, the stimulation may cause her to overinvest in the offspring, imposing an immediate benefit to the male and future cost to the female. This is a form of sexual conflict, in which traits favored in one sex harm the other (9). In PNAS, Servedio et al. (10) show that evolution can result in male displays that stimulate receptive females to invest optimally in their offspring; that is, evolution can convert sexual conflict into cooperation. Some have speculated that this reversal is logically impossible (11), but Servedio et al. (10) prove otherwise.
Following convention, when sexes have conflicting interests, a male display trait that arises in a population with receptive females will spread initially, which stimulates the females to overinvest in their offspring. This, in turn, favors the evolution of females who ignore the male display. If the display is at all costly, it will then disappear from the population after which a new male display may arise, repeating the cycle and maintaining sexual conflict in perpetuity. Servedio et al. (10) reconsider this dynamic by formulating a mathematical genetic model that recursively tracks the joint evolution of male display, female responsiveness, and constitutive female investment in reproduction. Consistent with convention, they verify that cycles driven by continual sexual conflict will evolve if costly female investment is coupled with large additional investments when she responds to the male display. However, the analyses revealed a heterodox prediction when male displays simulate moderate added female investment. In that scenario, evolution breaks from the initial sexual conflict not by eliminating female responsiveness to male displays but rather by lowering the level of constitutive female reproductive investment. The result is that the male display is now essential for a female to optimize the amount she invests in her brood, which benefits both mates—a decidedly cooperative interaction.
Beyond merely proving that pair-bonded species can escape the evolutionary snare of sexual conflict, Servedio et al. (10) are able to delineate the conditions under which conflict or cooperation (or neither one) is expected to evolve. Their analyses show that sexual cooperation should evolve over a broad range of conditions, which include survival costs for male display and female reproductive investment. Showing that a wide range of theoretical conditions are consistent with evolutionary transitions from sexual conflict to sexual cooperation need not imply that those transitions occur frequently in the wild. The latter depends entirely on how often conditions compatible with sexual cooperation occur in nature, which is ultimately an empirical question. Theoretical studies like Servedio et al. (10) are especially useful to empirical evolutionary biologists, not only because they present well-reasoned hypotheses that experimentalists can use to interpret their hard-earned observations but also because they provide guidance for rational experimental designs that facilitate efficient and informative studies about the evolutionary causes of mating displays.
Sexual stimulation can often be traced back to preexisting perceptual biases that evolved in species because they offer advantages outside the context of mating, such as detection of enemies or resources (12, 13). A male display that subsequently exploits an established sensory bias can cause a receptive female to increase her investment in reproduction. This benefits the male partner. Servedio et al. (10) show that including the external benefits to receptive females in their model further broadens the theoretical scope under which females remain receptive to male displays and achieve optimal levels of reproductive investment when stimulated. They also conjecture that this evolutionary path to sexual cooperation could set the stage for female self-stimulation. Perhaps this could explain the final act of the ring dove mating ritual. From Cheng (ref. 1, p. 2), after his solo display “the male allows the female to join in a nest cooing duet. The duet lasts for a day or two, then the female assumes solo cooing while the male perches nearby or actively procures nesting materials and constructs a nest by giving the nesting materials to the female to tuck beneath her chest as she crouches low while nest cooing.”

Acknowledgments

I thank H. Watts for helpful suggestions.

References

1
M.-F. Cheng, The role of vocal self-stimulation in female responses to males: Implications for state-reading. Horm. Behav. 53, 1–10 (2008).
2
C. Darwin, On the Origin of Species by Means of Natural Selection (Murray, 1859).
3
C. Darwin, The Descent of Man, and Selection in Relation to Sex (Murray, 1871).
4
T. H. Clutton-Brock, F. E. Guinness, S. D. Albon, Red Deer: Behavior and Ecology of Two Sexes (University of Chicago Press, 1982).
5
J. Höglund, J. G. M. Robertson, Chorusing behaviour, a density-dependent alternative mating strategy in male common toads (Bufo bufo). Ethology 79, 324–332 (1988).
6
W. R. Sigmund, Female preference for Anolis carolinensis males as a function of dewlap color and background coloration. J. Herpetol. 17, 137–143 (1983).
7
M. B. Andersson, Sexual Selection (Princeton University Press, 1994).
8
D. S. Lehrman, M. Friedman, Auditory stimulation of ovarian activity in the ring dove (Streptopelia risoria). Anim. Behav. 17, 494–497 (1969).
9
G. A. Parker, “Sexual selection and sexual conflict” in Sexual Selection and Reproductive Competition in Insects, M. S. Blum, N. A. Blum, Eds. (Academic Press, 1979), pp. 123–166.
10
M. R. Servedio, J. M. Powers, R. Lande, T. D. Price, Evolution of sexual cooperation from sexual conflict. Proc. Natl. Acad. Sci. U.S.A. 116, 23225–23231 (2019).
11
G. A. Arnquist, L. Rowe, Sexual Conflict (Princeton University Press, 2005).
12
M. J. Ryan, Sexual selection, sensory systems and sensory exploitation. Oxf. Surv. Evol. Biol. 7, 157–195 (1990).
13
M. J. Ryan, M. E. Cummings, Perceptual biases and mate choice. Annu. Rev. Ecol. Evol. Syst. 44, 437–459 (2013).

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Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 116 | No. 46
November 12, 2019
PubMed: 31659042

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Submission history

Published online: October 28, 2019
Published in issue: November 12, 2019

Acknowledgments

I thank H. Watts for helpful suggestions.

Notes

See companion article on page 23225.

Authors

Affiliations

Richard Gomulkiewicz1 [email protected]
School of Biological Sciences, Washington State University, Pullman, WA 99164

Notes

Author contributions: R.G. wrote the paper.

Competing Interests

The author declares no competing interest.

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Male mating displays can evolve from exploitative origins to cooperative endings
Proceedings of the National Academy of Sciences
  • Vol. 116
  • No. 46
  • pp. 22885-23363

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