A life-history perspective on sexual selection in a polygamous species

Abstract

Background: Ever since Darwin, evolutionary biologists have studied sexual selection driving differences in appearance and behaviour between males and females. An unchallenged paradigm in such studies is that one sex (usually the male) signals its quality as a mate to the other sex (usually the female), who is choosy in accepting a partner. Here, we hypothesize that in polygamous species these roles change dynamically with the mating status of males and females, depending on direct reproductive costs and benefits of multiple matings, and on sperm competition. We test this hypothesis by assessing fitness costs and benefits of multiple matings in both males and females in a polygamous moth species, as in moths not males but females are the signalers and males are the responders. Results: We found that multiple matings confer fitness costs and benefits for both sexes. Specifically, the number of matings did not affect the longevity of males or females, but only 67% of the males and 14% of the females mated successfully in all five nights. In addition, the female's reproductive output increased with multiple matings, although when paired with a new virgin male every night, more than 3 matings decreased her reproductive output, so that the Bateman gradient for females fit a quadratic model better than a linear model. The male's reproductive success was positively affected by the number of matings and a linear regression line best fit the data. Simulations of the effect of sperm competition showed that increasing last-male paternity increases the steepness of the male Bateman gradient and thus the male's relative fitness gain from additional mating. Irrespective of lastmale paternity value, the female Bateman gradient is steeper than the male one for up to three matings. Conclusion: Our results suggest that choosiness in moths may well change throughout the mating season, with males being more choosy early in the season and females being more choosy after having mated at least three times. This life-history perspective on the costs and benefits of multiple matings for both sexes sheds new light on sexual selection forces acting on sexual signals and responses.

Mating status affects female choice when females are signalers

“…Matings occurred throughout the entire period in which females signaled. The fact that we found virgin and mated signaling females equally ready to mate further makes sense because multiple matings increase female fitness in this species (Gao et al, 2020 ).…”

“…subflexa , a lower percentage of females was found calling in the night after mating, however, calling effort increased to about 50% again in subsequent nights (Blankers et al, 2021 ). The fact that mated females continue to signal emphasizes that both sexes may benefit from mating multiply (Blankers et al, 2021 ; Gao et al, 2020 ).…”

“…Recently, Gao et al ( 2020 ) discovered that C . virescens females reach maximal fitness with three matings, which suggests that females should maintain a (low) level of choosiness to increase their mating chances until they have reached their mating “optimum” (Gao et al, 2020 ).…”

“…Recently, Gao et al (2020) discovered that C. virescens females reach maximal fitness with three matings, which suggests that females should maintain a (low) level of choosiness to increase their mating chances until they have reached their mating "optimum" (Gao et al, 2020). However, because female fitness declines after three matings (Gao et al, 2020), thrice-mated females may become choosier, potentially to such an extent that these females will not mate if no male meets their mate acceptance threshold (De Jong & Sabelis, 1991). To unravel how females optimize their fitness, it would thus be interesting to assess whether mate preferences become stronger when females mate more than twice, and how sequential mate choice translates into paternity (see also Kokko et al, 2006;Slatyer et al, 2012).…”

Moth Mating: Modeling Female Pheromone Calling and Male Navigational Strategies to Optimize Reproductive Success

“…It is worth noting that, although the process described above is the most common, in some polyandrous species, females mate more than once, with the last male to arrive physically displacing any previously deposited spermatophore (Xu and Wang [34]). Female/male selectivity may also change dynamically, depending on seasonal effects or trade-offs between reproductive benefits and costs (Gao et al [35]). Finally, in species where male reproductive efforts are costly, it may be the male that chooses which female to mate with.…”