The Infertility Trap: The Fertility Costs of Group-Living in Mammalian Social Evolution

Abstract

Mammal social groups vary considerably in size from single individuals to very large herds. In some taxa, these groups are extremely stable, with at least some individuals being members of the same group throughout their lives; in other taxa, groups are unstable, with membership changing by the day. We argue that this variability in grouping patterns reflects a tradeoff between group size as a solution to environmental demands and the costs created by stress-induced infertility (creating an infertility trap). These costs are so steep that, all else equal, they will limit group size in mammals to ∼15 individuals. A species will only be able to live in larger groups if it evolves strategies that mitigate these costs. We suggest that mammals have opted for one of two solutions. One option (fission-fusion herding) is low cost but high risk; the other (bonded social groups) is risk-averse, but costly in terms of cognitive requirements.

Socioecological complexity in primate groups and its cognitive correlates

“…Together, this separation between the ‘cognitive’ and the ‘energetic’ (i) explains why previous analyses have found evidence to support seemingly contradictory positions, and (ii) underscores the fact that primate absolute brain size and architecture consistently predict social and cognitive traits. This is a timely reminder that stable, bonded groups of the kind characteristic of primates do not come for free: they are socially and cognitively expensive to maintain because the pressures promoting fragmentation in mammal groups are extremely high [ 4 , 62 ]. In addition, brains are nutritionally expensive and require dietary strategies that enable them to be both evolved and maintained.…”

“…One is that monogamy can only evolve in habitats of low predation risk, where animals can afford to live in very small social groups. In the absence of factors influencing male mating strategies, females would do best to live and forage alone (in the company of their offspring) [ 4 ]. The other is that living in large stable congregations (as opposed to aggregations or fission-fusion structures) is demanding both in terms of building consensus, making collective decisions, and mitigating the effects of resource competition across individuals with differing energy budgets and resource holding potential [ 9 ].…”

“…A higher proportion of primate species live and forage in stable social groups than in any other mammalian order [ 1 ]. Although group-living primates reap clear benefits in terms of predation avoidance [ 2 , 3 ], they pay ecological and physiological costs associated with increased competition for access to resources [ 4 , 5 ]. Among the challenges faced by individuals within social groups are managing dominance relationships, coordinating activity schedules and making collective decisions about foraging routes, sleeping sites and patch residency times.…”

“…In addition, relational complexity increases with group size as a result of individuals with differing energy budgets, resource holding potential, and reproductive and development states [9]. The result of this variance is that the more individuals there are in a group, and the more divergent their foraging strategies become, the more likely their time budgets will become desynchronized [10][11][12][13][14], and the more intense will be the stresses to which they are subjected if they stay together [4].…”

The Social Role of Self-Control

“…For species that form aggregations (unstable flocks or herds), differences in the rate of gut fill result in animals' time budgets getting out of synchrony [11][12][13], causing groups to fragment and disperse on a timescale of hours [8,[14][15][16][17]. Joiner-leaver models [18] remind us that, whereas small groups typically attract members, large groups lose them, especially when food patches become exhausted or the stresses of group-living become too great [19]. In such groups, individuals maintain weak (or simply casual) relationships with other members of group.…”