Jennifer E. Smith

Society, demography and genetic structure in the spotted hyena

Spotted hyenas (Crocuta crocuta) are large mammalian carnivores, but their societies, called ‘clans’, resemble those of such cercopithecine primates as baboons and macaques with respect to their size, hierarchical structure, and frequency of social interaction among both kin and unrelated group‐mates. However, in contrast to cercopithecine primates, spotted hyenas regularly hunt antelope and compete with group‐mates for access to kills, which are extremely rich food sources, but also rare and ephemeral. This unique occurrence of baboon‐like sociality among top‐level predators has favoured the evolution of many unusual traits in this species. We briefly review the relevant socio‐ecology of spotted hyenas, document great demographic variation but little variation in social structure across the species’ range, and describe the long‐term fitness consequences of rank‐related variation in resource access among clan‐mates. We then summarize patterns of genetic relatedness within and between clans, including some from a population that had recently gone through a population bottleneck, and consider the roles of sexually dimorphic dispersal and female mate choice in the generation of these patterns. Finally, we apply social network theory under varying regimes of resource availability to analyse the effects of kinship on the stability of social relationships among members of one large hyena clan in Kenya. Although social bonds among both kin and non‐kin are weakest when resource competition is most intense, hyenas sustain strong social relationships with kin year‐round, despite constraints imposed by resource limitation. Our analyses suggest that selection might act on both individuals and matrilineal kin groups within clans containing multiple matrilines.

Rank-related partner choice in the fission–fusion society of the spotted hyena (Crocuta crocuta)

When social partners vary in their relative value, individuals should theoretically initiate partnerships with conspecifics of the highest value. Here, we tested this prediction in a wild population of spotted hyenas (Crocuta crocuta). Crocuta live in complex, fission–fusion societies structured by dominance hierarchies in which individuals vary greatly in their value as social companions. Because patterns of association among Crocuta reflect social preferences, we calculated association indices (AIs) to examine how social rank influences intrasexual partner choice among unrelated adults of both sexes. The highest-ranking individuals were generally most gregarious in both sexes. Females associated most often with dominant and adjacent-ranking females. Females joined subgroups based on the presence of particular conspecifics such that subordinates joined focal females at higher rates than did dominants. Dominants benefit from associations with subordinates by enjoying priority of access to resources obtained and defended by multiple group members, but the benefits of these associations to subordinates are unknown. To investigate this, we tested three hypotheses suggesting how subordinates might benefit from rank-related partner choice among unrelated females. We found that subordinates who initiated group formation benefited by gaining social and feeding tolerance from dominants. However, rates at which dominants provided coalitionary support to subordinates did not vary with AIs. Overall, our data resemble those documenting patterns of association among cercopithecine primates. We consider our results in light of optimal reproductive skew theory, Seyfarth’s rank attractiveness model, and biological market theory. Our data are more consistent with the predictions of Seyfarth’s model and of biological market theory than with those of skew theory.

Greetings promote cooperation and reinforce social bonds among spotted hyaenas

Societies characterized by fission–fusion dynamics consist of subgroups that frequently change in size and composition. Although this flexible lifestyle permits individuals to reduce conflicts of interest, it simultaneously imposes a unique set of challenges on group members that are regularly subject to prolonged separation. Theory predicts animals should evolve ritualized and risky displays to quickly update relationships at reunions. Here we investigated the function of nonconciliatory greetings among adult female spotted hyaenas, Crocuta crocuta, belonging to a single, large female-dominated social group in Kenya. We tested three hypotheses forwarded to explain the occurrence of these multimodal signals: formal submission, tension reduction and social bonding hypotheses. In contrast to predictions of the formal submission hypothesis, rank distance and relative rank were excluded from our best model predicting greetings among adult females. Moreover, directional consistency of greetings was low (0.65) compared to that of submissive behaviours during dyadic agonistic interactions (0.97). Instead, our data revealed that adult females greeted coalition partners and close associates, including kin, most often per opportunity, and they did so in neutral contexts more frequently than in situations characterized by social tension. Although these findings are in direct contrast to the predictions of the tension reduction and formal submission hypotheses, they strongly support the social bonding hypothesis. Importantly, the immediate act of greeting promoted cooperation among allies during intragroup and intergroup coalition formation. Thus, these risky, multimodal signals permit hyaenas to effectively communicate cooperative affiliations within a continuously shifting social milieu.

Evolution of Cooperation among Mammalian Carnivores and Its Relevance to Hominin Evolution

Anthropological theory suggests direct links between the origins of cooperation in hominins and a shift toward an energy-rich diet. Although the degree to which early hominins ate meat remains controversial, here we reevaluate the notion, originally suggested by Schaller and Lowther in 1969, that mammalian carnivores can shed light on human origins. Precisely when cooperation evolved in hominins or carnivores is unknown, but species from both groups cooperatively hunt large game, defend resources, guard against predators, and rear young. We present a large-scale comparative analysis of extant carnivore species, quantifying anatomical, ecological, and behavioral correlates of cooperation to determine whether metabolic rate, body and relative brain size, life history traits, and social cohesion coevolved with cooperation. We focus heavily on spotted hyenas, which live in more complex societies than other carnivores. Hyenas regularly join forces with kin and nonkin to hunt large antelope and to defend resources during intergroup conflicts and disputes with lions. Our synthesis highlights reduced sexual dimorphism, increased reproductive investment, high population density, fission-fusion dynamics, endurance hunting of big game in open habitats, and large brains as important correlates of cooperation among carnivores. We discuss the relevance of our findings to understanding the origins of cooperation in hominins.

Early play may predict later dominance relationships in yellow-bellied marmots (Marmota flaviventris)

Play has been defined as apparently functionless behaviour, yet since play is costly, models of adaptive evolution predict that it should have some beneficial function (or functions) that outweigh its costs. We provide strong evidence for a long-standing, but poorly supported hypothesis: that early social play is practice for later dominance relationships. We calculated the relative dominance rank by observing the directional outcome of playful interactions in juvenile and yearling yellow-bellied marmots (Marmota flaviventris) and found that these rank relationships were correlated with later dominance ranks calculated from agonistic interactions, however, the strength of this relationship attenuated over time. While play may have multiple functions, one of them may be to establish later dominance relationships in a minimally costly way.

Leadership in Mammalian Societies: Emergence, Distribution, Power, and Payoff

Leadership is an active area of research in both the biological and social sciences. This review provides a transdisciplinary synthesis of biological and social-science views of leadership from an evolutionary perspective, and examines patterns of leadership in a set of small-scale human and non-human mammalian societies. We review empirical and theoretical work on leadership in four domains: movement, food acquisition, within-group conflict mediation, and between-group interactions. We categorize patterns of variation in leadership in five dimensions: distribution (across individuals), emergence (achieved versus inherited), power, relative payoff to leadership, and generality (across domains). We find that human leadership exhibits commonalities with and differences from the broader mammalian pattern, raising interesting theoretical and empirical issues.

Hamilton's legacy: kinship, cooperation and social tolerance in mammalian groups

In 1964, W. D. Hamilton proposed a novel solution to the long-standing evolutionary puzzle: why do individuals cooperate? Hamilton predicted that, if individuals possess the ability to discriminate on the basis of kinship, then they should gain inclusive fitness benefits by biasing helpful behaviour towards relatives and harmful behaviour away from them. The possibility that kin selection might favour social evolution has now inspired five decades of active research. Here, I synthesize this evidence for social mammals. First, I report on the methodological advances that allow for pedigree construction, and review the evidence for maternal and paternal kin discrimination. Second, I recognize that a substantial body of evidence for the evolution of cooperative breeding via kin selection exists, and then focus on the potential for kin selection to favour less well understood, yet equally salient, targets of selection: social partner choice, coalition formation and social tolerance (withholding aggression). I find that kin selection favours remarkably similar patterns of nepotism in primate and nonprimates with respect to these short-lived social acts. Although social alliances among maternal and paternal kin are common in mammalian societies, kinship largely fails to protect individuals from aggression. Thus, an individuals closest associates and allies, many of whom are kin, are most often an individuals closest competitors within mammalian social groups. Taken together, these findings highlight the value of Hamiltons holistic approach in simultaneously considering the direct benefits of competition and the indirect fitness benefits of cooperation. Despite major empirical advances since the inception of kin selection theory, future tests using newly available molecular and statistical methods in combination with longitudinal behavioural data are required to partition the relative contributions of direct and indirect fitness on the lifetime inclusive fitness. Such approaches will elucidate the relative influences of evolutionary and ecological forces favouring social evolution across the mammalian lineage of social mammals.

Ontogeny and symmetry of social partner choice among free-living yellow-bellied marmots

Affiliative interactions have important fitness consequences for individuals. Yet, precisely how social roles emerge across ontogeny outside of the context of agonistic interactions is largely unknown, particularly in free-living species of nonprimates. Here we used longitudinal data on yellow-bellied marmots, Marmota flaviventris, residing around the Rocky Mountain Biology Laboratory in Colorado, U.S.A., to investigate the development of social partner choice in free-living rodents. We first characterized the symmetry of affiliative interactions between mother–offspring pairs and within cohorts of individuals as they developed across discrete life history stages. Affiliative behaviours generally increased in symmetry such that exchanges became more reciprocal as individuals matured. We then evaluated the extent to which individuals biased their affiliative behaviour towards, and agonistic behaviour away from, genetic relatives. As predicted by kin selection theory, rates of affiliation increased with the degree of relatedness among individuals at all three life history stages. Thus, nepotism emerged within cohorts of newly weaned pups and persisted into adulthood despite prolonged annual separations due to hibernation. Surprisingly, close relatives also exchanged the highest rates of agonistic behaviour. After accounting for the degree of relatedness, rates of affiliative behaviours given and agonistic behaviours received remained positively correlated, suggesting that close affiliates are each others closest competitors. Thus, although reciprocity of affiliative exchanges within cohorts increased as individuals matured, competition among genetic relatives emerged early in ontogeny and persisted into adulthood. Taken together, these results highlight changes in social roles shown by individuals across ontogeny and shed light on theories of life history and social evolution.

Collective movements, leadership and consensus costs at reunions in spotted hyaenas

Because collective movements have fitness consequences for all participants, group travel can impose conflicts of interest when group-mates vary. Challenges associated with coordinating activities of group-mates, such as during travel, may potentially be mitigated through the use of simple rules governing leadership and other behaviours to minimize conflict. Although individuals living in groups with fission–fusion dynamics may temporarily separate, leadership determination at subsequent reunions, and events occurring during reunions, are poorly understood. Here we investigate leadership during travel prior to reunions of spotted hyaenas, Crocuta crocuta, living in one large social group in the Masai Mara National Reserve, Kenya. Whereas individuals often arrived at dens or joined hunting parties alone, those joining others to participate in group defence of shared resources typically did so when accompanied by group-mates. Although most hyaenas led processions, the attributes of members within each travelling party consistently predicted leadership roles. The highest-ranking adult within each travelling subgroup, often a lactating female, typically assumed the vanguard position prior to reunions. Reunions promoted conflict, particularly at kills. However, as predicted by the conflict mitigation hypothesis, individuals that greeted conspecifics were significantly less likely to fight at reunions than were hyaenas that failed to greet at reunions. Thus, whereas temporary separations may reduce immediate conflicts of interest in fission–fusion societies, hyaenas pay consensus costs at subsequent reunions, particularly in the context of feeding competition, and greetings appear to reduce such costs. Finally, we propose a novel scheme for leadership categorization in which leadership depends on whether or not leadership is based on specific attributes of individual group members. We apply this attribute-based framework to quantify the patterns and mechanisms of leadership during group travel for 52 species of mammals, including the spotted hyaenas studied here, and place findings in a broad evolutionary context.

Behavioral interactions between fire ants and vertebrate nest predators at two black-capped vireo nests

Abstract We report on behavioral interactions between fire ants (Solenopsis invicta) and vertebrate predators at two Black-capped Vireo (Vireo atricapilla) nests at Fort Hood, Texas. In the presence of fire ants, an eastern woodrat (Neotoma floridana) failed to depredate a clutch of vireo eggs at one nest, while a rat snake (Elaphe obsoleta lindheimeri) depredated nestlings at another nest, despite fire ants swarming the nest. Neither nest was successful. Direct and indirect effects of interactions among nest predators on avian nesting success need further assessment.