Socioecology, but not cognition, predicts male coalitions across primates

Behavioral Ecology The official journal of the ISBE International Society for Behavioral Ecology Behavioral Ecology (2014), 25(4), 794–801. doi:10.1093/beheco/aru054 Original Article Socioecology, but not cognition, predicts male coalitions across primates Annie Bissonnette,a Mathias Franz,a Oliver Schülke,a and Julia Ostnera aPrimate Social Evolution Group, Courant Research Centre Evolution of Social Behaviour, GeorgAugust-University Göttingen, Kellnerweg 6, Göttingen 37077, Germany Humans form agonistic coalitions and alliances in many contexts, but this behavior is thought to be rare in other species. A prominent hypothesis states that coalitions may be under cognitive constraints, but this idea is debated and remains to be tested empirically. In this study, we evaluate the cognitive constraint hypothesis against 3 alternative hypotheses that stress the role of demography, substrate use, and resource competition, for the evolution of male coalitions. A comparative analysis of a unique data set of 86 multimale multifemale groups of 38 nonhuman primate species from all major radiations revealed no evolutionary association of male coalition frequency with cognitive capacity (as indexed by neocortex ratio and endocranial volume). The observed variation was best explained by demography and resource competition in that male coalitions were more likely to occur in species characterized by larger male groups and reduced levels of contest competition (after controlling for phylogeny). These findings suggest that constraints imposed by the socioecological setting, rather than cognition, explain best why some primate species evolved customary coalitionary behavior while others did not. This study presents the first empirical evidence against the long-standing view that cognitive abilities may impose a limit on the use of coalitions in animals. Key words: brain size, competition, cooperation, demography, males, mating skew. Introduction Male–male coalitionary aggression is ubiquitous in humans (Chagnon and Bugos 1979; Hruschka and Henrich 2006; Flinn and Ponzi 2012), and the evolutionary roots of human coalitionary behavior can be traced by investigating similar behavior in nonhuman animals. Among our closest relatives, the primates, intragroup coalition among males show striking interspecific variation even between closely related taxa (van Schaik et al. 2006; e.g., Henzi et al. 1999). Males living in mixed-sex groups sometimes use coalitions to increase or maintain their rank (e.g., Kutsukake and Hasegawa 2005; Schülke et al. 2010), or increase their access to mates without affecting dominance (e.g., Bercovitch 1988; Bissonnette et al. 2011). This behavior, however, appears to be rare or completely absent in many more species (e.g., Henzi et al. 1999; Paul et al. 2000), a surprising finding given the mating (e.g., Nishida 1983; Bercovitch 1988; Watts 1998; Bissonnette et al. 2011) and reproductive (e.g., Witt et al. 1981; Schülke et al. 2010; Gilby et al. 2013) benefits that this behavior may provide. Although in most primate species the males in a group are not closely related, Address correspondence to Annie Bissonnette, who is now at Anthropological Institute and Museum, University of Zurich, 190 Winterthurerstrasse, Zurich 8057, Switzerland. E-mail: . M.F. Coauthor is now at Department of Biology, Duke University, Box 90338, Durham, NC 27708, USA A.B. and M.F. contributed equally to this study. © The Author 2014. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: the absence of kin does not seem to be a serious obstacle to the evolution of male coalitions (van Schaik et al. 2006; e.g., Bercovitch 1988; Schülke et al. 2010; Bissonnette et al. 2011). It is likely that other socioecological or cognitive processes are responsible for driving and keeping coalitions in place (Olson and Blumstein 2009). Given the lack of formal quantification of coalitionary behavior in most species, however, this statement remains speculative. In this paper, we compiled a unique data set of 86 multimale multifemale groups of 38 primate species from all major radiations to test 4 evolutionary hypotheses for the evolution of male coalitions. Many have argued that coalitions are, at a minimum, a prime example of how social interactions can become complex, and at most, may be the kind of behavior that drove brain evolution generally (Alexander 1989; Harcourt 1992; Connor 2007). Coalitions are thought to be complex because they involve triadic interactions (cf., Kummer 1967) where an individual, in order to be efficient, must take into account not only its direct relationships with others, but also the details of the relationships between other group members (e.g., Kummer 1967; Harcourt 1992; Tomasello and Call 1997; Silk 1999). Coalitions can become cognitively more demanding if individuals use affiliative interactions to cultivate relationships with powerful supporters, to compete for powerful allies, or prevent rivals from forming potentially disruptive alliances (de Waal 1982; Harcourt 1992; Silk 1992; Schülke et al. 2010). The extent to which coalitions may be under cognitive constraints, however, is Received 10 October 2013; revised 18 February 2014; accepted 24 February 2014; Advance Access publication 8 April 2014. Bissonnette et al. • No effect of cognition on male coalitions incidence of coalitions and contest potential. Specifically, very high levels of contest competition may hinder coalitionary behavior if males are less tolerant of each other, which hamper cooperation (e.g., Melis et al. 2006; Hare et al. 2007; Olson and Blumstein 2009). Moreover, mounting a coalitionary challenge may be particularly risky at higher contest potential (van Schaik et al. 2006) due to an increased likelihood of retaliation by the target thus making the benefit to cost ratio of coalitions less favorable. If these effects are present and strong enough to override the effects of increasing benefits with increasing contest competition, we should find a negative association between competition levels and the incidence of male coalitions (Olson and Blumstein 2009). Although the 4 above factors (cognitive capacity, substrate use, demography, and contest potential) are not mutually exclusive, and in fact there is some evidence that each may play at least some role in individual species, their relevance at a broader taxonomic level is still unknown. Thus, we investigated the distribution of male coalitions across the primate phylogeny and the evolutionary association of male coalition frequency with these factors, using phylogenetically based methods. Materials and Methods Data collection An extensive survey of the primate literature was undertaken to obtain reports of coalition behavior among adult males (principal key words for search: coalition, alliance, intervention, aid, support). Because p (...truncated)