COMMENTARY
COMMENTARY
Primate model offers insights into male bonding in complex societies Cyril C. Grueter1 School of Anatomy, Physiology and Human Biology, The University of Western Australia, Crawley, WA 6009, Australia
Primatological research is often conducted for the purpose of clarifying the evolutionary trajectories of behavioral and morphological characters that are either unique to humans or are shared with closely related species. Nonhuman primate species—especially those whose common ancestry is relatively recent, such as chimpanzees—can serve as referential models that provide insights into our evolutionary history (1). However, there are other, lesser known primates that may shed complementary light on human traits. In PNAS, Patzelt et al. (2) show that a more distantly related taxon—the Guinea baboon (Papio papio) from West Africa, a hitherto poorly known and difficult to study species— shares with humans a combination of core socio-structural features, namely tolerant relations between males that materialize in a multilevel society. Baboons have been used as analogs for spawning ideas about human social evolution for two reasons: first, many taxa dwell in environments similar to those inhabited by our forebears (i.e., savanna-woodland habitats) (3); second, others exhibit a human-like
social organization (4). Guinea baboons have until recently remained largely neglected by the primatological and anthropological community. Patzelt et al. (2) offer the most rigorous attempt to date at elucidating the social system of this peculiar primate. The authors marshal evidence in favor of a multilevel society in this species, a previously disputed assumption. The data on social organization that emerged from earlier studies were inconclusive and did not paint a congruent picture (summarized in ref. 2). Patzelt et al. (2) used GPS technology combined with traditional observational methods and molecular genetics to powerful effect, and document (adult) male–male association, proximity, and genetic relatedness. Their key finding is that Guinea baboon society is multilevel—that is, it exhibits nested tiers of social groupings (units, parties, gangs, communities)—and features extensive male–male interaction and tolerance. In addition, Patzelt et al. report that closely associated males do not have to be close relatives (Fig. 1). Traditionally, baboon taxa were pigeonholed into multimale-multifemale “savanna
baboons” (i.e., yellow, olive, and chacma baboons) and multilevel hamadryas, even though it has been apparent for quite some time that Guinea baboons are different. With the new findings on Guinea baboons, this dichotomy is now a straw man. The more we study different populations and taxa, the more we become aware of the behavioral variability and plasticity in this phylogenetic group. In Guinea baboons, male–male bonds are stronger and play a larger role than in savanna and also hamadryas baboons. Another baboon species that has turned out to differ from the savanna baboon “norm” is the Kinda baboon, which has recently been shown to have curiously high levels of male affiliative investment in the maintenance of females (5). Guinea baboons can now be confidently added to the list of primate species that are organized into multilevel systems, which includes hamadryas baboons, geladas, snubnosed monkeys, douc langurs, and proboscis monkeys (reviewed in ref. 6). In line with other multilevel taxa, social interactions in Guinea baboons are more frequent within the inner layers of their society and progressively decline in frequency toward the outer layers. An analogous nested or federated system exists in humans (and likely extinct hominins), whereby smaller units are embedded in a Russian doll-like manner within larger ones (6, 7). However, what sets humans apart from all other primates is the unusually 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 cooperation (“ultrasociality”) (8, 9). A comprehensive understanding of human 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, Göttingen, Germany).
www.pnas.org/cgi/doi/10.1073/pnas.1416140111
See companion article on page 14740. 1
Email: [email protected].
PNAS | October 14, 2014 | vol. 111 | no. 41 | 14645–14646
dimensions need to be added: in particular, the female contribution to the system, including exclusivity of male–female bonds, female–female relationships, mating, and dispersal patterns. Elucidating the socioecological factors that give rise to this multitiered system and the adaptive function of the various tiers would also prove informative. Previous reconstructions of the evolutionary pathways leading to these systems in papionins (and hominins) point to a pattern whereby ancestrally mixed-sex groups underwent permanent internal fission in response to a mixture of social and ecological pressures. This step could have been favored by spatial dispersion of food coupled with male monopolization of females (or female-initiated protective bonds with males) (4, 6). Although male–male relations are typically characterized by competition over reproductive opportunities, intermale attraction and mutual tolerance can be advantageous and are prevalent in several primate species (often dubbed “male-bonded species”) (e.g., ref. 10). In addition, group-level coalitions of resident males who keep rivals at bay are common in primates and other mammals and can positively influence male reproductive success (11). However, acts of affiliation and cooperation among males associated with different social units are extremely uncommon. In bottlenose dolphins, we see complex nested alliances in a large open social network (12). In hamadryas baboons males of different “harems” are linked through social bonds at the clan level and can also function as allies in a competitive interaction (13); moreover, they show “respect of possession” toward a leader with his females (14). Similarly, in snub-nosed monkeys, males belonging to different one-male units have recently been shown to engage in joint collective action, such as patrolling behavior (15). In Guinea baboons, an elaborate repertoire of bonding mechanisms, including coalitions and ritualized greetings, involve males residing in different units but being members of the same party (and occasionally different parties). Future research will have to establish the fitness consequences of these male bonds. Male cooperative behavior constitutes a fundamental part of the human adaptive
14646 | www.pnas.org/cgi/doi/10.1073/pnas.1416140111
studies show that male–male interactions are more cooperative than female–female interactions (17). Male bonding is thought to have characterized early hominins (18), and from a functional point of view, the disposition toward intermale bonds must have had Darwinian ramifications for survival and reproductive performance. Such bonds have likely been under positive selection because they may have facilitated collective and cooperative activities aimed at resource and mate acquisition/defense, most notably hunting and warfare/intergroup conflict (19). Ultimately, through such activities males would have acquired fitness benefits in
terms of access to reproductively significant resources, such as food, territory, and mates. Using microsatellite markers, Patzelt et al. (2), demonstrate that the establishment of male–male bonds and cooperation is not conditional on close genetic relatedness. Similar conclusions have been drawn for snubnosed monkeys in multilevel societies (15), and an absence of strong kin bias also typifies male social bonds in other social systems (10, 11). This finding suggests that male cooperation is best understood in terms of the mutual direct benefits individuals obtain through acting together (20). In humans, inclusive fitness also cannot explain extensive cooperation in hunter-gatherer bands (9). In conclusion, it does seem that at least in the case of humans and some papionin primates, such as Guinea baboons, stability of interunit tolerance is predicated on male– male tolerance. Following this finding, it is reasonable to assume that male bonds play a part in promoting the maintenance of multilevel societies [although female dispersal also plays a role in unifying groups, at least in humans (8)]. Coresidence of several nuclear families in bands and metabands facilitates some key human universal traits, such as cooperative hunting and the recruitment of male allies for defense and warfare against enemy groups.
1 Wrangham RW (1987) The significance of African apes for reconstructing human social evolution. The Evolution of Human Behavior: Primate Models, ed Kinzey WG (State Univ of New York Press, Albany, NY), pp 51–71. 2 Patzelt A, et al. (2014) Male tolerance and male–male bonds in a multilevel primate society. Proc Natl Acad Sci USA 111:14740–14745. 3 DeVore I, Washburn SL (1963) Baboon ecology and human evolution. African Ecology and Human Evolution, eds Howell FC, Bourlière F (Aldine Publishing, Chicago), pp 335–367. 4 Swedell L, Plummer T (2012) A papionin multi-level society as a model for early hominin evolution. Int J Primatol 33(5):1165–1193. 5 Weyher AH, Phillips-Conroy JE, Fourrier MS, Jolly CJ (2014) Maledriven grooming bouts in mixed-sex dyads of Kinda baboons (Papio kindae). Folia Primatol (Basel) 85(3):178–191. 6 Grueter CC, Chapais B, Zinner D (2012) Evolution of multilevel societies in nonhuman primates and humans. Int J Primatol 33(5): 1002–1037. 7 Rodseth L, Wrangham RW, Harrigan AM, Smuts BB (1991) The human community as a primate society. Curr Anthropol 32(3):221–254. 8 Chapais B (2011) Anthropology. The deep social structure of humankind. Science 331(6022):1276–1277. 9 Hill KR, et al. (2011) Co-residence patterns in hunter-gatherer societies show unique human social structure. Science 331(6022):1286–1289. 10 Langergraber KE, Mitani JC, Vigilant L (2007) The limited impact of kinship on cooperation in wild chimpanzees. Proc Natl Acad Sci USA 104(19):7786–7790.
11 Schülke O, Bhagavatula J, Vigilant L, Ostner J (2010) Social bonds enhance reproductive success in male macaques. Curr Biol 20(24): 2207–2210. 12 Randic S, Connor RC, Sherwin WB, Krützen M (2012) A novel mammalian social structure in Indo-Pacific bottlenose dolphins (Tursiops sp.): Complex male alliances in an open social network. Proc Biol Sci 279(1740):3083–3090. 13 Abegglen J (1984) On Socialization in Hamadryas Baboons: A Field Study (Bucknell Univ Press, Lewisburg, PA). 14 Kummer H, Götz W, Angst W (1974) Triadic differentiation: An inhibitory process protecting pair bonds in baboons. Behaviour 49(1):62–87. 15 Xiang ZF, et al. (2014) Males collectively defend their one-male units against bachelor males in a multi-level primate society. Am J Primatol 76(7):609–617. 16 van Schaik CP, Kappeler PM (2006) Cooperation in primates and humans: Closing the gap. Cooperation in Primates and Humans: Mechanisms and Evolution, eds Kappeler P, van Schaik CP (Springer, New York), pp 3–21. 17 Balliet D, Li NP, Macfarlan SJ, Van Vugt M (2011) Sex differences in cooperation: A meta-analytic review of social dilemmas. Psychol Bull 137(6):881–909. 18 Foley RA (1989) The evolution of hominid social behaviour. Comparative Socioecology: The Behavioural Ecology of Humans and other Mammals, eds Standen V, Foley RA (Blackwell, Oxford), pp 474–493. 19 Bowles S (2009) Did warfare among ancestral hunter-gatherers affect the evolution of human social behaviors? Science 324(5932):1293–1298. 20 Clutton-Brock T (2009) Cooperation between non-kin in animal societies. Nature 462(7269):51–57.
pattern (16), and male bonding and cooperation across unit boundaries are hallmarks of many human societies and ubiquitous in everyday life: consider fraternities (and fraternal interest groups), gangs, military units, sports teams, and other such groups. Meta-analytic
Patzelt et al. demonstrate that the establishment of male–male bonds and cooperation is not conditional on close genetic relatedness.
Grueter
COMMENTARY
Primate model offers insights into male bonding in complex societies Cyril C. Grueter1 School of Anatomy, Physiology and Human Biology, The University of Western Australia, Crawley, WA 6009, Australia
Primatological research is often conducted for the purpose of clarifying the evolutionary trajectories of behavioral and morphological characters that are either unique to humans or are shared with closely related species. Nonhuman primate species—especially those whose common ancestry is relatively recent, such as chimpanzees—can serve as referential models that provide insights into our evolutionary history (1). However, there are other, lesser known primates that may shed complementary light on human traits. In PNAS, Patzelt et al. (2) show that a more distantly related taxon—the Guinea baboon (Papio papio) from West Africa, a hitherto poorly known and difficult to study species— shares with humans a combination of core socio-structural features, namely tolerant relations between males that materialize in a multilevel society. Baboons have been used as analogs for spawning ideas about human social evolution for two reasons: first, many taxa dwell in environments similar to those inhabited by our forebears (i.e., savanna-woodland habitats) (3); second, others exhibit a human-like
social organization (4). Guinea baboons have until recently remained largely neglected by the primatological and anthropological community. Patzelt et al. (2) offer the most rigorous attempt to date at elucidating the social system of this peculiar primate. The authors marshal evidence in favor of a multilevel society in this species, a previously disputed assumption. The data on social organization that emerged from earlier studies were inconclusive and did not paint a congruent picture (summarized in ref. 2). Patzelt et al. (2) used GPS technology combined with traditional observational methods and molecular genetics to powerful effect, and document (adult) male–male association, proximity, and genetic relatedness. Their key finding is that Guinea baboon society is multilevel—that is, it exhibits nested tiers of social groupings (units, parties, gangs, communities)—and features extensive male–male interaction and tolerance. In addition, Patzelt et al. report that closely associated males do not have to be close relatives (Fig. 1). Traditionally, baboon taxa were pigeonholed into multimale-multifemale “savanna
baboons” (i.e., yellow, olive, and chacma baboons) and multilevel hamadryas, even though it has been apparent for quite some time that Guinea baboons are different. With the new findings on Guinea baboons, this dichotomy is now a straw man. The more we study different populations and taxa, the more we become aware of the behavioral variability and plasticity in this phylogenetic group. In Guinea baboons, male–male bonds are stronger and play a larger role than in savanna and also hamadryas baboons. Another baboon species that has turned out to differ from the savanna baboon “norm” is the Kinda baboon, which has recently been shown to have curiously high levels of male affiliative investment in the maintenance of females (5). Guinea baboons can now be confidently added to the list of primate species that are organized into multilevel systems, which includes hamadryas baboons, geladas, snubnosed monkeys, douc langurs, and proboscis monkeys (reviewed in ref. 6). In line with other multilevel taxa, social interactions in Guinea baboons are more frequent within the inner layers of their society and progressively decline in frequency toward the outer layers. An analogous nested or federated system exists in humans (and likely extinct hominins), whereby smaller units are embedded in a Russian doll-like manner within larger ones (6, 7). However, what sets humans apart from all other primates is the unusually 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 cooperation (“ultrasociality”) (8, 9). A comprehensive understanding of human 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, Göttingen, Germany).
www.pnas.org/cgi/doi/10.1073/pnas.1416140111
See companion article on page 14740. 1
Email: [email protected].
PNAS | October 14, 2014 | vol. 111 | no. 41 | 14645–14646
dimensions need to be added: in particular, the female contribution to the system, including exclusivity of male–female bonds, female–female relationships, mating, and dispersal patterns. Elucidating the socioecological factors that give rise to this multitiered system and the adaptive function of the various tiers would also prove informative. Previous reconstructions of the evolutionary pathways leading to these systems in papionins (and hominins) point to a pattern whereby ancestrally mixed-sex groups underwent permanent internal fission in response to a mixture of social and ecological pressures. This step could have been favored by spatial dispersion of food coupled with male monopolization of females (or female-initiated protective bonds with males) (4, 6). Although male–male relations are typically characterized by competition over reproductive opportunities, intermale attraction and mutual tolerance can be advantageous and are prevalent in several primate species (often dubbed “male-bonded species”) (e.g., ref. 10). In addition, group-level coalitions of resident males who keep rivals at bay are common in primates and other mammals and can positively influence male reproductive success (11). However, acts of affiliation and cooperation among males associated with different social units are extremely uncommon. In bottlenose dolphins, we see complex nested alliances in a large open social network (12). In hamadryas baboons males of different “harems” are linked through social bonds at the clan level and can also function as allies in a competitive interaction (13); moreover, they show “respect of possession” toward a leader with his females (14). Similarly, in snub-nosed monkeys, males belonging to different one-male units have recently been shown to engage in joint collective action, such as patrolling behavior (15). In Guinea baboons, an elaborate repertoire of bonding mechanisms, including coalitions and ritualized greetings, involve males residing in different units but being members of the same party (and occasionally different parties). Future research will have to establish the fitness consequences of these male bonds. Male cooperative behavior constitutes a fundamental part of the human adaptive
14646 | www.pnas.org/cgi/doi/10.1073/pnas.1416140111
studies show that male–male interactions are more cooperative than female–female interactions (17). Male bonding is thought to have characterized early hominins (18), and from a functional point of view, the disposition toward intermale bonds must have had Darwinian ramifications for survival and reproductive performance. Such bonds have likely been under positive selection because they may have facilitated collective and cooperative activities aimed at resource and mate acquisition/defense, most notably hunting and warfare/intergroup conflict (19). Ultimately, through such activities males would have acquired fitness benefits in
terms of access to reproductively significant resources, such as food, territory, and mates. Using microsatellite markers, Patzelt et al. (2), demonstrate that the establishment of male–male bonds and cooperation is not conditional on close genetic relatedness. Similar conclusions have been drawn for snubnosed monkeys in multilevel societies (15), and an absence of strong kin bias also typifies male social bonds in other social systems (10, 11). This finding suggests that male cooperation is best understood in terms of the mutual direct benefits individuals obtain through acting together (20). In humans, inclusive fitness also cannot explain extensive cooperation in hunter-gatherer bands (9). In conclusion, it does seem that at least in the case of humans and some papionin primates, such as Guinea baboons, stability of interunit tolerance is predicated on male– male tolerance. Following this finding, it is reasonable to assume that male bonds play a part in promoting the maintenance of multilevel societies [although female dispersal also plays a role in unifying groups, at least in humans (8)]. Coresidence of several nuclear families in bands and metabands facilitates some key human universal traits, such as cooperative hunting and the recruitment of male allies for defense and warfare against enemy groups.
1 Wrangham RW (1987) The significance of African apes for reconstructing human social evolution. The Evolution of Human Behavior: Primate Models, ed Kinzey WG (State Univ of New York Press, Albany, NY), pp 51–71. 2 Patzelt A, et al. (2014) Male tolerance and male–male bonds in a multilevel primate society. Proc Natl Acad Sci USA 111:14740–14745. 3 DeVore I, Washburn SL (1963) Baboon ecology and human evolution. African Ecology and Human Evolution, eds Howell FC, Bourlière F (Aldine Publishing, Chicago), pp 335–367. 4 Swedell L, Plummer T (2012) A papionin multi-level society as a model for early hominin evolution. Int J Primatol 33(5):1165–1193. 5 Weyher AH, Phillips-Conroy JE, Fourrier MS, Jolly CJ (2014) Maledriven grooming bouts in mixed-sex dyads of Kinda baboons (Papio kindae). Folia Primatol (Basel) 85(3):178–191. 6 Grueter CC, Chapais B, Zinner D (2012) Evolution of multilevel societies in nonhuman primates and humans. Int J Primatol 33(5): 1002–1037. 7 Rodseth L, Wrangham RW, Harrigan AM, Smuts BB (1991) The human community as a primate society. Curr Anthropol 32(3):221–254. 8 Chapais B (2011) Anthropology. The deep social structure of humankind. Science 331(6022):1276–1277. 9 Hill KR, et al. (2011) Co-residence patterns in hunter-gatherer societies show unique human social structure. Science 331(6022):1286–1289. 10 Langergraber KE, Mitani JC, Vigilant L (2007) The limited impact of kinship on cooperation in wild chimpanzees. Proc Natl Acad Sci USA 104(19):7786–7790.
11 Schülke O, Bhagavatula J, Vigilant L, Ostner J (2010) Social bonds enhance reproductive success in male macaques. Curr Biol 20(24): 2207–2210. 12 Randic S, Connor RC, Sherwin WB, Krützen M (2012) A novel mammalian social structure in Indo-Pacific bottlenose dolphins (Tursiops sp.): Complex male alliances in an open social network. Proc Biol Sci 279(1740):3083–3090. 13 Abegglen J (1984) On Socialization in Hamadryas Baboons: A Field Study (Bucknell Univ Press, Lewisburg, PA). 14 Kummer H, Götz W, Angst W (1974) Triadic differentiation: An inhibitory process protecting pair bonds in baboons. Behaviour 49(1):62–87. 15 Xiang ZF, et al. (2014) Males collectively defend their one-male units against bachelor males in a multi-level primate society. Am J Primatol 76(7):609–617. 16 van Schaik CP, Kappeler PM (2006) Cooperation in primates and humans: Closing the gap. Cooperation in Primates and Humans: Mechanisms and Evolution, eds Kappeler P, van Schaik CP (Springer, New York), pp 3–21. 17 Balliet D, Li NP, Macfarlan SJ, Van Vugt M (2011) Sex differences in cooperation: A meta-analytic review of social dilemmas. Psychol Bull 137(6):881–909. 18 Foley RA (1989) The evolution of hominid social behaviour. Comparative Socioecology: The Behavioural Ecology of Humans and other Mammals, eds Standen V, Foley RA (Blackwell, Oxford), pp 474–493. 19 Bowles S (2009) Did warfare among ancestral hunter-gatherers affect the evolution of human social behaviors? Science 324(5932):1293–1298. 20 Clutton-Brock T (2009) Cooperation between non-kin in animal societies. Nature 462(7269):51–57.
pattern (16), and male bonding and cooperation across unit boundaries are hallmarks of many human societies and ubiquitous in everyday life: consider fraternities (and fraternal interest groups), gangs, military units, sports teams, and other such groups. Meta-analytic
Patzelt et al. demonstrate that the establishment of male–male bonds and cooperation is not conditional on close genetic relatedness.
Grueter
