Richard Gomulkiewicz; PNAS November 12, 2019 116 (46) 22899-22900

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.”

Figure: 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.

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.”

See https://www.pnas.org/content/116/46/22899