Male cooperation for breeding opportunities contributes to the evolution of multilevel societies

Abstract

A small number of primate species including snub-nosed monkeys (colobines), geladas (papionins) and humans live in multilevel societies (MLSs), in which multiple one-male polygamous units (OMUs) coexist to form a band, and non-breeding males associate in bachelor groups. Phylogenetic reconstructions indicate that the papionin MLS appears to have evolved through internal fissioning of large mixed-sex groups, whereas the colobine MLS evolved through the aggregation of small, isolated OMUs. However, how agonistic males maintain tolerance under intensive competition over limited breeding opportunities remains unclear. Using a combination of behavioural analysis, satellite telemetry and genetic data, we quantified the social network of males in a bachelor group of golden snub-nosed monkeys. The results show a strong effect of kinship on social bonds among bachelors. Their interactions ranged from cooperation to agonism, and were regulated by access to mating partners. We suggest that an ‘arms race’ between breeding males' collective defence against usurpation attempts by bachelor males and bachelor males' aggregative offence to obtain reproductive opportunities has selected for larger group size on both sides. The results provide insight into the role that kin selection plays in shaping inter-male cohesion which facilities the evolution of multilevel societies. These findings have implications for understanding human social evolution, as male–male bonds are a hallmark of small- and large-scale human societies.

Seasonal changes in social cohesion among males in a same‐sex primate group

“…In most other species of Asian langurs, the leader male of a single OMU defends a territory and his OMU from neighboring OMUs, solitary bachelor males, or members of an AMU (Sterck, ; Yeager & Kool, ). In the case of snub‐nosed monkeys, although bachelor males may live together for several years, and in some cases are close relatives (Qi et al, ), it is rare for bachelor males to act collectively to attempt to take over an OMU.…”

“…In such a polygynous setting, extra males are largely excluded from breeding groups by resident males and either remain solitary or form all‐male groups (Bennett & Sebastian, ; Dunbar & Dunbar, ; Levréro et al, ; Rajpurohit, ). These bachelor groups may contain ousted males that have lost their reproductive monopoly (Rajpurohit, Sommer, & Mohnot, ), males that are at their reproductive peak (i.e., prime males), as well as young pre‐prime males waiting to fully mature and obtain mating opportunities (Qi et al, ).…”

“…All‐male groups vary in stability and cohesiveness across species; for example, in Thomas langurs ( Presbytis thomasi ), all‐male groups are unstable and characterized by frequent fission and fusion events (Wich et al, ), whereas in mountain gorillas ( Gorilla beringei beringei ) (Robbins, ) and African elephants ( Loxodonta africana ) (Chiyo et al, ), marginalized males either remain solitary or alternate between a solitary and a same‐sex social state. In contrast, gelada ( Theropithecus gelada ) and golden snub‐nosed monkey ( Rhinopithecus roxellana ) all‐male units (AMUs) are relatively stable and the same set of bachelor males remain together for several years (Dunbar, ; Qi et al, ).…”

“…In the case of mountain gorillas, males residing in an all‐male group were found to spend more time in close proximity (<2 min) during resting (a median of 11.14 vs. 2.97%), and exhibit higher levels of affiliation (physical contact: 0.37 vs. 0.03 times/hr, grooming: 0.22 vs. 0.002 times/hr, play: 0.52 vs. 0.005 times/hr) and homosexuality (male–male mounting or touching of genitals by another male, 0.06 vs. 0 times/hr) than males living in multimale‐multifemale groups (Robbins, ). In addition, genetic relatedness is reported to have a positive influence on affiliative within‐AMU male associations in African elephants and golden snub‐nosed monkeys (Chiyo et al, ; Qi et al, ). Similarly, in several primate species in which males are philopatric (e.g., chimpanzees (Mitani, ), spider monkeys (Di Fiore, Link, Schmitt, & Spehar, ), and muriquis [ Brachyteles arachnoides ] (Strier, )), group males form strong social alliances, engage in cooperative behavior.…”

Male-Male Mounting Behaviour in Free-Ranging Golden Snub-Nosed Monkeys (Rhinopithecus roxellana)

“…Each unit contains, on average, 9 monkeys; a resident (or leader) adult male, 2-5 adult females and offspring of varying ages Qi et al, 2009]. Maturing animals often emigrate from their natal groups, and males may join all-male units, several of which may coalesce into an all-male band [Qi et al, 2014[Qi et al, , 2017. Breeding bands consist of an aggregation of several 1-male units, and all-male bands consist of an aggregation of several all-male units.…”