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Male Mating Displays Can Evolve from Exploitative Origins to Cooperative Endings COMMENTARY Richard Gomulkiewicza,1

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Male Mating Displays Can Evolve from Exploitative Origins to Cooperative Endings COMMENTARY Richard Gomulkiewicza,1 COMMENTARY Male mating displays can evolve from exploitative origins to cooperative endings COMMENTARY Richard Gomulkiewicza,1 Animal mating displays provide some of nature’s most dramatic and curious spectacles. Ring doves (Strepto- pelia 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.” What could explain such elaborate mating behav- ior? Evolutionary biologists have been puzzling over this question since Darwin (2, 3). Many striking exam- ples of mating displays, including the large male ant- lers 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 car- olinensis (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 Fig. 1. A pair of ring doves (S. risoria) crossing. Image of mates a male can have each season. This excludes courtesy of Todd Petit (photographer). sexual selection as an explanation for their exagger- ated mating displays. Instead, male displays appear to stimulate female investment in reproduction (8). From Following convention, when sexes have conflicting an adaptive evolutionary standpoint, this is unex- interests, a male display trait that arises in a population pected since a male’s efforts would be better spent with receptive females will spread initially, which contributing resources directly to his offspring and the stimulates the females to overinvest in their offspring. female would be better off ignoring such displays if This, in turn, favors the evolution of females who her investment in the brood is already optimal. When ignore the male display. If the display is at all costly, it a male displays to a receptive female, the stimulation will then disappear from the population after which a may cause her to overinvest in the offspring, imposing new male display may arise, repeating the cycle and an immediate benefit to the male and future cost to maintaining sexual conflict in perpetuity. Servedio the female. This is a form of sexual conflict, in which et al. (10) reconsider this dynamic by formulating a traits favored in one sex harm the other (9). In PNAS, mathematical genetic model that recursively tracks Servedio et al. (10) show that evolution can result in the joint evolution of male display, female responsive- male displays that stimulate receptive females to in- ness, and constitutive female investment in reproduc- vest optimally in their offspring; that is, evolution can tion. Consistent with convention, they verify that convert sexual conflict into cooperation. Some have cycles driven by continual sexual conflict will evolve speculated that this reversal is logically impossible if costly female investment is coupled with large addi- (11), but Servedio et al. (10) prove otherwise. tional investments when she responds to the male aSchool of Biological Sciences, Washington State University, Pullman, WA 99164 Author contributions: R.G. wrote the paper. The author declares no competing interest. Published under the PNAS license. See companion article 10.1073/pnas.1904138116. 1Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1916912116 PNAS Latest Articles | 1of2 Downloaded by guest on September 25, 2021 display. However, the analyses revealed a heterodox prediction rational experimental designs that facilitate efficient and informa- when male displays simulate moderate added female investment. tive studies about the evolutionary causes of mating displays. In that scenario, evolution breaks from the initial sexual conflict Sexual stimulation can often be traced back to preexisting not by eliminating female responsiveness to male displays but perceptual biases that evolved in species because they offer rather by lowering the level of constitutive female reproductive advantages outside the context of mating, such as detection of investment. The result is that the male display is now essential for enemies or resources (12, 13). A male display that subsequently a female to optimize the amount she invests in her brood, which exploits an established sensory bias can cause a receptive female benefits both mates—a decidedly cooperative interaction. to increase her investment in reproduction. This benefits the male Beyond merely proving that pair-bonded species can escape partner. Servedio et al. (10) show that including the external ben- the evolutionary snare of sexual conflict, Servedio et al. (10) are efits to receptive females in their model further broadens the able to delineate the conditions under which conflict or coopera- theoretical scope under which females remain receptive to male tion (or neither one) is expected to evolve. Their analyses show displays and achieve optimal levels of reproductive investment that sexual cooperation should evolve over a broad range of con- when stimulated. They also conjecture that this evolutionary path ditions, which include survival costs for male display and female to sexual cooperation could set the stage for female self- reproductive investment. Showing that a wide range of theoretical stimulation. Perhaps this could explain the final act of the ring dove conditions are consistent with evolutionary transitions from sexual mating ritual. From Cheng (ref. 1, p. 2), after his solo display “the conflict to sexual cooperation need not imply that those transi- male allows the female to join in a nest cooing duet. The duet lasts tions occur frequently in the wild. The latter depends entirely on for a day or two, then the female assumes solo cooing while the how often conditions compatible with sexual cooperation occur in male perches nearby or actively procures nesting materials and nature, which is ultimately an empirical question. Theoretical stud- constructs a nest by giving the nesting materials to the female to ies like Servedio et al. (10) are especially useful to empirical evo- tuck beneath her chest as she crouches low while nest cooing.” lutionary biologists, not only because they present well-reasoned hypotheses that experimentalists can use to interpret their hard- Acknowledgments earned observations but also because they provide guidance for I thank H. Watts for helpful suggestions. 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., 10.1073/pnas.1904138116 (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). 2of2 | www.pnas.org/cgi/doi/10.1073/pnas.1916912116 Gomulkiewicz Downloaded by guest on September 25, 2021.
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