Saturday, May 21, 2022

In mammalian societies... How reproductive control promotes social control

The eco-evolutionary landscape of power relationships between males and females. Eve Davidian et al. Trends in Ecology & Evolution, May 18, 2022. https://doi.org/10.1016/j.tree.2022.04.004

Highlights

. Inequality in the degree of control (or ‘power’) that members of one sex exert over members of the other sex is a pervasive characteristic of mammalian societies, including our own.

. The study of the drivers of male–female power relationships has been impeded by methodological limitations and a lack of conceptual embedding in theories of sexual conflict, sexual selection and social evolution.

. Recent evidence challenges long-standing views by showing that (i) power ranges along a continuum from strictly male- to strictly female-dominated animal societies and (ii) intersexual power relationships are not fixed attributes of species.

. Here we break with dichotomist and static approaches to adopt a dynamic, theory-driven framework that provides a better understanding of the power struggles between the sexes, and how these relate to the social and mating system of a species.

Abstract: In animal societies, control over resources and reproduction is often biased towards one sex. Yet, the ecological and evolutionary underpinnings of male–female power asymmetries remain poorly understood. We outline a comprehensive framework to quantify and predict the dynamics of male–female power relationships within and across mammalian species. We show that male–female power relationships are more nuanced and flexible than previously acknowledged. We then propose that enhanced reproductive control over when and with whom to mate predicts social empowerment across ecological and evolutionary contexts. The framework explains distinct pathways to sex-biased power: coercion and male-biased dimorphism constitute a co-evolutionary highway to male power, whereas female power emerges through multiple physiological, morphological, behavioural, and socioecological pathways.

How reproductive control promotes social control

Here we propose that the degree of male and female reproductive control determines whether and how members of each sex can empower themselves socially, with respect to access to nonreproductive resources. We further illustrate how the mechanism by which power emerges may influence its durability.

 Coercion: an evolutionary highway to male power

Male coercive reproductive control is facilitated by large male-biased sexual dimorphism in size and weaponry, which is typical of contest-based mating systems, and includes most polygynous and some polygynandrous societies [
,
,
] (Figure 1). In these systems, males often extend their use of coercion to dominate females when competing over nonreproductive resources. Large males may further reinforce intersexual asymmetries in coercive potential and limit female empowerment by controlling their social environment and preventing them from recruiting social allies (Box 2). The tight association between the pervasive use of coercion by males and male-biased sexual dimorphism likely emerges from a co-evolutionary feedback with the mating system (Figure 2). When males gain reproductive pay-offs from aggressively monopolising females against competitors, this will often (i) promote contest-based competition between males; (ii) subsequently drive the evolution of male-biased sexual dimorphism [
,
], which will (iii) promote male coercive reproductive control over females; and (iv) drive male social empowerment and dominance over females [
,
,
]. This will (v) ultimately close the loop by strengthening male reproductive control over females [
,
,
,
]. When female resistance strategies fail to prevent or disrupt this potent self-reinforcing loop, it may catalyse the emergence and maintenance of male-biased power over evolutionary times. This likely explains why males often exert both high reproductive and social control over females in contest-based mating systems (Figure 1), and why contest-based systems are widespread among mammals. In addition, female strategies may sometimes reinforce rather than disrupt the loop favouring male power. For example, where males already have high reproductive control and females cannot mate promiscuously to dilute paternity, they may instead concentrate paternity to seek paternal protection in response to infanticidal threats [
]. Such paternity concentration strategies may contribute to locking females into male-dominated societies.

Figure 2Eco-evolutionary pathways to male and female empowerment in mammals.

 Why the coercive pathway is not the females’ way

A similar coercive co-evolutionary pathway is unlikely to drive female social empowerment because mammalian species in which females concurrently exhibit contest-based intrasexual competition to monopolise access to multiple males and larger body sizes are currently unreported [
,
]. In some species, reproductive competition may be most intense among females; yet, contrary to what would be expected for this co-evolutionary pathway, these species either exhibit sexual monomorphism, as in the polyandrous moustached tamarins (Saguinus mystax) [
] and cooperatively breeding meerkats [
] (Figure 1A), or male-biased size dimorphism as in Damaraland mole rats (Fukomys damarensis) [
]. This apparent paradox probably reflects inherent differences in the life history and modality of intrasexual competition in females and males [
]. Female mammals often compete using subtle forms of coercion – for example, using threats and agonistic signals – which do not select for increased body size and weaponry. There are at least three reasons for this: first, theory predicts avoidance of overt aggression for the sex that faces highest costs of offspring production [
]; second, the incentive for females to engage in physical contest may be low because sharing resources is often less costly for females than for males; third, mammalian females are usually philopatric and thus predominantly compete with close female kin, with whom they may avoid engaging in costly contests [
]. These insights emphasise key differences in the pathways to female and male power (Figure 2), in particular that a large body size and coercion are not prerequisites for female empowerment.

 Female social empowerment from leverage based on sex

When females retain some reproductive control – usually in species with moderate sexual size dimorphism as in monogamous, polyandrous, and scramble-based polygynandrous species (Figure 1) – they can trade copulations for resources or services that males can provide, such as protection for themselves or their offspring against conspecifics or predators. Yet, such leverage is usually restricted to periods of female sexual receptivity and thereby only confer short-term social empowerment to females, as in some mouse lemurs (Microcebus spp.) where female social control over males is more pronounced during the breeding season [
,
]. Leverage-based power may therefore explain female social empowerment over males in species where males are nonpermanent residents and join groups only during the mating season, as in rock hyraxes [
]. In species living in permanent groups where males and females maintain long-term, differentiated social relationships, females can extend their leverage beyond the receptive period. This strategy may durably promote cooperative behaviour or inhibit aggression from males through mating markets, as in long-tailed macaques (Macaca fascicularis) [
] and Guinea baboons (Papio papio) [
]. Leverage can then represent a potent source of social control that may, even under male-biased dimorphism, allow females to manipulate the social rank of subordinate males, as in vervet monkeys [
], or to influence male social and competitive relationships, as in bonobos (Box 3). Similar to males, but through a different mechanism, increased social control by females may subsequently reinforce female reproductive control by facilitating their resistance to unwanted solicitations in a positive feedback loop (Figure 2).

 Female social empowerment from mate choice

When female reproductive control enables them to exercise precopulatory mate choice, they may select male traits (e.g., social deference, cooperative personalities, or a smaller body size) that may, over evolutionary time, increase female social control in a process described by the ‘docile male’ hypothesis [
]. In bonobos, the related ‘self-domestication’ hypothesis posits that selection for nonaggressive males, which may partly result from female choice, has contributed to the contrasts in morphology, physiology, behaviour, and cognition between male bonobos and chimpanzees (Pan troglodytes) [
]. Empirical evidence of female mate choice for such male traits is scarce in mammals, however [
]. Female preferences for males with whom they are socially bonded have been reported [
,
], but may reflect leverage rather than choice for male traits that are relevant to intersexual power. Alternatively, female mate choice can promote intersexual power asymmetries indirectly. For example, in spotted hyenas, female reproductive control and mate preferences drive male dispersal [
], which decreases the number of social allies that males can recruit and thus reduces male social control [
].
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