Primate Model Offers Insights Into Male Bonding in Complex Societies Cyril C
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COMMENTARY COMMENTARY Primate model offers insights into male bonding in complex societies Cyril C. Grueter1 baboons” (i.e., yellow, olive, and chacma School of Anatomy, Physiology and Human Biology, The University of Western Australia, baboons) and multilevel hamadryas, even Crawley, WA 6009, Australia though it has been apparent for quite some time that Guinea baboons are different. With Primatological research is often conducted social organization (4). Guinea baboons have the new findings on Guinea baboons, this for the purpose of clarifying the evolutionary until recently remained largely neglected by dichotomy is now a straw man. The more trajectories of behavioral and morphological the primatological and anthropological com- we study different populations and taxa, the more we become aware of the behavioral characters that are either unique to humans munity.Patzeltetal.(2)offerthemostrig- variability and plasticity in this phylogenetic or are shared with closely related species. orous attempt to date at elucidating the social group. In Guinea baboons, male–male bonds Nonhuman primate species—especially those system of this peculiar primate. The authors are stronger and play a larger role than in whose common ancestry is relatively recent, marshal evidence in favor of a multilevel so- savanna and also hamadryas baboons. An- such as chimpanzees—can serve as referential ciety in this species, a previously disputed other baboon species that has turned out to models that provide insights into our evolu- assumption. The data on social organization differ from the savanna baboon “norm” is tionary history (1). However, there are other, that emerged from earlier studies were incon- the Kinda baboon, which has recently been lesser known primates that may shed com- clusive and did not paint a congruent picture shown to have curiously high levels of male plementary light on human traits. In PNAS, (summarized in ref. 2). Patzelt et al. (2) used affiliative investment in the maintenance of Patzeltetal.(2)showthatamoredistantly GPS technology combined with traditional females (5). related taxon—the Guinea baboon (Papio observational methods and molecular genet- Guinea baboons can now be confidently papio) from West Africa, a hitherto poorly ics to powerful effect, and document (adult) — – added to the list of primate species that are known and difficult to study species male male association, proximity, and ge- organized into multilevel systems, which shares with humans a combination of core netic relatedness. Their key finding is that — includes hamadryas baboons, geladas, snub- socio-structural features, namely tolerant Guinea baboon society is multilevel that is, nosed monkeys, douc langurs, and proboscis relations between males that materialize it exhibits nested tiers of social groupings monkeys (reviewed in ref. 6). In line with — in a multilevel society. (units,parties,gangs,communities) and fea- other multilevel taxa, social interactions in – Baboons have been used as analogs for tures extensive male male interaction and Guinea baboons are more frequent within spawning ideas about human social evolution tolerance. In addition, Patzelt et al. report that the inner layers of their society and progres- for two reasons: first, many taxa dwell in closely associated males do not have to be sively decline in frequency toward the outer environments similar to those inhabited by close relatives (Fig. 1). layers. An analogous nested or federated our forebears (i.e., savanna-woodland hab- Traditionally, baboon taxa were pigeon- system exists in humans (and likely extinct “ itats) (3); second, others exhibit a human-like holed into multimale-multifemale savanna hominins), whereby smaller units are embed- ded in a Russian doll-like manner within larger ones (6, 7). However, what sets humans apart from all other primates is the unusu- ally high degree of social integration at the community level; such massive integration is achieved by interconnections among groups via cross-cutting kinship and affinity ties, as well as reciprocal exchange and coop- eration (“ultrasociality”)(8,9). A comprehensive understanding of hu- man and primate modular sociality requires insights into the fabric of relationships within the core social units and how these core units interact with neighboring units to create the multilayered structure. For a full description of the society of Guinea baboons, additional Author contributions: C.C.G. wrote the paper. The author declares no conflict of interest. Fig. 1. A trio of closely bonded male Guinea baboons. Image courtesy of Julia Fischer (German Primate Center, See companion article on page 14740. Göttingen, Germany). 1Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1416140111 PNAS | October 14, 2014 | vol. 111 | no. 41 | 14645–14646 Downloaded by guest on September 23, 2021 dimensions need to be added: in particular, pattern (16), and male bonding and cooper- terms of access to reproductively significant the female contribution to the system, in- ation across unit boundaries are hallmarks of resources, such as food, territory, and mates. cluding exclusivity of male–female bonds, fe- many human societies and ubiquitous in ev- Using microsatellite markers, Patzelt et al. male–female relationships, mating, and eryday life: consider fraternities (and fraternal (2), demonstrate that the establishment of dispersal patterns. Elucidating the socioeco- interest groups), gangs, military units, sports male–male bonds and cooperation is not logical factors that give rise to this multitiered teams, and other such groups. Meta-analytic conditional on close genetic relatedness. Sim- system and the adaptive function of the var- ilar conclusions have been drawn for snub- ious tiers would also prove informative. Pre- Patzelt et al. demon- nosed monkeys in multilevel societies (15), vious reconstructions of the evolutionary strate that the estab- and an absence of strong kin bias also typifies pathways leading to these systems in papio- lishment of male–male male social bonds in other social systems (10, nins (and hominins) point to a pattern 11). This finding suggests that male cooper- whereby ancestrally mixed-sex groups under- bonds and cooperation ationisbestunderstoodintermsofthemu- went permanent internal fission in response is not conditional tual direct benefits individuals obtain through to a mixture of social and ecological pressures. on close genetic acting together (20). In humans, inclusive fit- This step could have been favored by spatial ness also cannot explain extensive coopera- dispersion of food coupled with male mo- relatedness. tion in hunter-gatherer bands (9). nopolization of females (or female-initi- studies show that male–male interactions are In conclusion, it does seem that at least ated protective bonds with males) (4, 6). – inthecaseofhumansandsomepapionin Although male–male relations are typically more cooperative than female female inter- actions (17). Male bonding is thought to have primates, such as Guinea baboons, stability of characterized by competition over reproduc- – characterized early hominins (18), and from interunit tolerance is predicated on male tive opportunities, intermale attraction and male tolerance. Following this finding, it is mutual tolerance can be advantageous and a functional point of view, the disposition reasonable to assume that male bonds play are prevalent in several primate species (often toward intermale bonds must have had a part in promoting the maintenance of mul- dubbed “male-bonded species”) (e.g., ref. 10). Darwinian ramifications for survival and re- tilevel societies [although female dispersal In addition, group-level coalitions of resident productive performance. Such bonds have also plays a role in unifying groups, at least males who keep rivals at bay are common in likely been under positive selection because in humans (8)]. Coresidence of several nu- primates and other mammals and can posi- they may have facilitated collective and clear families in bands and metabands facil- tively influence male reproductive success cooperative activities aimed at resource (11). However, acts of affiliation and cooper- and mate acquisition/defense, most no- itates some key human universal traits, such ation among males associated with differ- tably hunting and warfare/intergroup con- as cooperative hunting and the recruitment ent social units are extremely uncommon. flict (19). Ultimately, through such activities of male allies for defense and warfare against In bottlenose dolphins, we see complex males would have acquired fitness benefits in enemy groups. nested alliances in a large open social net- work (12). In hamadryas baboons males of 1 Wrangham RW (1987) The significance of African apes for 11 Schülke O, Bhagavatula J, Vigilant L, Ostner J (2010) Social bonds different “harems” are linked through so- reconstructing human social evolution. The Evolution of Human enhance reproductive success in male macaques. Curr Biol 20(24): cial bonds at the clan level and can also Behavior: Primate Models, ed Kinzey WG (State Univ of New York 2207–2210. Press, Albany, NY), pp 51–71. 12 Randic S, Connor RC, Sherwin WB, Krützen M (2012) A novel function as allies in a competitive inter- – mammalian social structure in Indo-Pacific bottlenose dolphins “ 2 Patzelt A, et al. (2014) Male tolerance and male male bonds in action (13); moreover, they show respect a multilevel primate society. Proc Natl Acad Sci USA (Tursiops sp.): Complex male alliances in an open