Female resistance to sexual coercion can evolve to preserve the indirect benefits of mate choice

Abstract

Sexual conflict over the indirect benefits of mate choice may arise when traits in one sex limit the ability of the other sex to freely choose mates but when these coercive traits are not necessarily directly harmful (i.e. forced fertilization per se). Although we might hypothesize that females can evolve resistance in order to retain the indirect, genetic benefits (reflected in offspring attractiveness) of mating with attractive males, up to now it has been difficult to evaluate potential underlying mechanisms. Traditional theoretical approaches do not usually conceptually distinguish between female preference for male mating display and female resistance to forced fertilization, yet sexual conflict over indirect benefits implies the simultaneous action of all of these traits. Here, we present an integrative theoretical framework that draws together concepts from both sexual selection and sexual conflict traditions, allowing for the simultaneous coevolution of displays and preferences, and of coercion and resistance. We demonstrate that it is possible for resistance to coercion to evolve in the absence of direct costs of mating to preserve the indirect benefits of mate choice. We find that resistance traits that improve the efficacy of female mating preference can evolve as long as females are able to attain some indirect benefits of mating with attractive males, even when both attractive and unattractive males can coerce. These results reveal new evolutionary outcomes that were not predicted by prior theories of indirect benefits or sexual conflict.

Female emancipation in a male dominant, sexually dimorphic primate under natural conditions

“…Yet, a few studies show intersexual dominance is evolutionary meaningful [19]; for example, females may compete with males for access to food, as in several species of capuchin monkeys (genus Sapajus [35,36], genus Cebus [37]). Female dominance over males may be a strategy to resist sexual coercion by males [38,39] and a guarantee for female mate choice [40]. Female dominance over males is found more typically in species where males and females have equal body size, such as lemurs [41] and marmosets (Callithrix spp.…”

Fighting isn’t sexy in lekking Greater Sage-grouse (Centrocercus urophasianus)

“…Given the extreme skew in mating success in lek breeding systems (Bradbury & Gibson, 1983), males would be incentivized to disrupt one-another’s copulations/courtship to the detriment of the group as a whole (Chapman, 1935; Foster, 1983; Prum, 2017) – a situation similar to the “Tragedy of the Commons” (Hardin, 1968). To overcome this “Tragedy of the Lek”, resist sexually coercive behavior, and allow for the persistence of lekking systems that we observe in nature, females would be expected to select for reduced aggression, and male behaviors that regulate aggression, instead of selecting for more aggressive males as previous theory has suggested, (Prum, 2017; Snow et al ., 2019). Moreover, if fighting is in conflict with, as opposed to aligned with, female choice in some contexts, we may also expect to concurrently observe fighting behaviors serving a regulatory role in other contexts and/or the self-regulation of aggression.…”

“…Classic theory suggests that fighting demonstrates “good genes” fitness benefits for females (Cox & Le Boeuf, 1977; Andersson, 1994) and feeds into narratives of lek evolution wherein the lek system offers more opportunities for females to view contests (Beehler & Foster, 1988; Kokko, 1997). However, recent theoretical work has supported the notion that male aggression that hinders the efficacy of female mate choice can give rise to selection for female behaviors or morphologies that resist those effects, even when there is an apparent association between attractiveness and aggression in males (Snow et al ., 2019). Selection for resistance behaviors can lead to drastically different expected outcomes in the trajectory of the evolution of mating interactions, as compared to models that assume male aggression and female mate choice are aligned (e.g., Rosenthal & Servedio, 1999; Lessells, 2006; Snow et al ., 2019).…”

Evolution of reduced mate harming tendency of males inDrosophila melanogasterpopulations selected for faster life history

“…However, in absence of female counter evolution in response to the evolution of increasingly competitive (and hence, harmful) males, SC can lead to the extinction of a population/species, an outcome dubbed as the "tragedy of commons" (Le Galliard et al 2005;Rankin and Kokko 2006;Rankin et al 2007). Populations subjected to SC can avert this debilitating outcome by evolving female resistance (Holland and Rice 1999;Wigby and Chapman 2004;Friberg 2005;Rankin et al 2011;Dougherty et al 2017;Snow et al 2019). There is a second way in which a population can avert the tragedy of commons.…”

“…However, such an extreme outcome of interlocus sexual conflict is unusual, because of, at least, three reasons. First, as mentioned earlier, female counter adaptation to mate harm can result in a chase-away process where evolution of mate harming ability of males is neutralised by the emergence of female resistance (Holland and Rice 1998, Holland and Rice 1999; Wigby and Chapman 2004; Friberg 2005; Rankin et al 2011; Dougherty et al 2017; Snow et al 2019). Secondly, traits that inflict mate harm, i.e., the sexually antagonistic male traits, are energetically expensive to express and hence, increase in such traits is constrained by trade-offs involving costly life history traits (Wedell et al 2006; Bonduriansky et al 2008; Adler and Bonduriansky 2014; Lemaître et al 2020).…”