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The Spotted Hyena (Crocuta crocuta) as a Model System for Study of the Evolution of Intelligence

Kay E. Holekamp , Sharleen T. Sakai , Barbara L. Lundrigan
DOI: http://dx.doi.org/10.1644/06-MAMM-S-361R1.1 545-554 First published online: 1 June 2007

Abstract

Large brains and great intelligence are metabolically costly, but the social complexity hypothesis suggests that these traits were favored nonetheless in primates by selection pressures associated with life in complex societies. If so, then cognitive abilities and nervous systems with primatelike attributes should have evolved convergently in nonprimate mammals living in large, elaborate societies in which social dexterity enhances individual fitness. Societies of spotted hyenas (Crocuta crocuta) are remarkably similar to those of cercopithecine primates with respect to size, structure, and patterns of competition and cooperation. These similarities set an ideal stage for comparative analysis of social intelligence and nervous system organization. As in cercopithecine primates, spotted hyenas use multiple sensory modalities to recognize their kin and other conspecifics as individuals, they know that some group-mates are more valuable social partners than others, they recognize 3rd-party kin and rank relationships among their clan-mates, and they use this knowledge adaptively during social decision-making. Examination of the available data strongly suggests convergent evolution of intelligence between spotted hyenas and primates. Evidence that less gregarious members of the family Hyaenidae lack some of the cognitive abilities found in spotted hyenas would provide further support for the idea that social complexity favors enhancement of intelligence in mammals.

Key words
  • Crocuta
  • hyaena
  • hyena
  • intelligence
  • social cognition

Mammalian brains are generally larger in relation to body mass than those of other vertebrates, but relative brain size also varies greatly among mammals (Jerison 1973; Northcutt 2002). Humans and other primates have larger brains for their body size than most other mammals, they possess a larger array of cognitive skills, and many cognitive abilities shared with species in other orders are best developed in primates (reviewed in Byrne and Whiten 1988; Harcourt and de Waal 1992; Tomasello and Call 1997). However, the development and maintenance of large brains entail huge metabolic costs (Aiello and Wheeler 1995; Aschoff et al. 1971), suggesting that the fitness benefits associated with large brains and great intelligence must be enormous in primates for these traits to have evolved. However, it is currently unknown how intelligence enhances fitness.

Two hypotheses have been advanced to suggest fitness advantages primates might gain by having relatively large brains and a large array of cognitive skills, despite the substantial metabolic costs of enlarged brains. The 1st hypothesis suggests that these traits were favored by selective forces in the physical environment, such as the need to learn and recall when fruit might become available on trees that fruit sporadically, how to use tools to extract difficult foods, or how to navigate visually through a 3-dimensional arboreal world (e.g., Milton 1981; Povinelli and Cant 1995). The 2nd hypothesis, known broadly as the “social complexity”hypothesis, suggests instead that the selective force favoring big brains and advanced cognition in primates was the need to anticipate, appropriately respond to, and manipulate the social behavior of conspecifics (reviewed in Byrne and Whiten 1988).

Although both hypotheses have received some support to date, by far the largest body of evidence from primate studies, both naturalistic and experimental, has accrued in support of the social complexity hypothesis. Unfortunately, however, we know little about social cognition in animals other than primates (Harcourt and de Waal 1992). The social complexity hypothesis predicts that, if indeed the large brains and great intelligence found in primates evolved in response to selection pressures associated with life in complex societies, then cognitive abilities and nervous systems with primate-like attributes should have evolved convergently in nonprimate mammals living in large, elaborate societies in which individual fitness is strongly influenced by social dexterity.

Mammalian carnivores represent an excellent group, outside of the primates, within which to evaluate the relationship between cognitive abilities and social complexity. Carnivores often form social groups that are comparable in size and complexity to those of primates; many carnivores live in large, permanent social units that contain both males and females from multiple, overlapping generations. Recent studies of phylogenetic relationships among the orders of eutherian mammals indicate that Carnivora and Primates are not sister taxa, but rather are members of distinct clades (Laurasiatheria and Euarchontoglires, respectively) that last shared a common ancestor between 90 and 100 million years ago (Springer et al. 2003, 2005). Therefore mammalian carnivores offer the opportunity for an independent test of the hypothesis that demands imposed by social living have driven the evolution of cognitive abilities and nervous systems in mammals. Gregarious carnivores engage in a variety of behaviors, such as cooperative hunting of large vertebrate prey, that have prompted many observers to infer that these predators must possess extraordinary intellectual powers (e.g., Guggisberg 1962). However, the cognitive abilities of carnivores have seldom been the subject of systematic study, and they are currently poorly understood (e.g., Byrne 1994).

In this paper we examine the perceptual, cognitive, and neural mechanisms underlying complex social behavior in 1 gregarious carnivore, the spotted hyena (Crocuta crocutd). Throughout this paper we will refer to members of this species merely as “hyenas”unless indicated otherwise. Spotted hyenas share many aspects of their social lives and life histories with cercopithecine primates, which comprise 1 subfamily of the Old World primate family Cercopithecidae. Members of the subfamily Cercopithecinae include baboons, macaques, vervets, guenons, talapoins, patas monkeys, and mangabeys. The many similarities between spotted hyenas and cercopithecine primates set an ideal stage for comparative analysis of social cognition and nervous system organization. After briefly summarizing the relevant aspects of hyena socioecology, we review what is known about hyena communication signals, perception of those signals, and demonstrated abilities in the domain of social cognition. In particular, we review what spotted hyenas know about their social companions, and how they use that knowledge. We then briefly describe 2 new lines of work comparing cognitive abilities in spotted hyenas with those in less-gregarious members of the hyena family, and comparing brain structure among these and other carnivores. Our primary objective in this paper is to inquire whether or not spotted hyenas exhibit some of the same specific cognitive abilities and patterns of brain organization as those found in primates. Evidence for the existence of shared cognitive abilities and neural traits would suggest convergent evolution in these 2 distantly related taxa, and would strongly support the social complexity hypothesis.

Socioecology of Spotted Hyenas

Spotted hyenas are large terrestrial predators occurring throughout sub-Saharan Africa. Although they occupy a different trophic niche from primates and have various sensory capabilities not shared with primates, hyenas nevertheless exhibit many remarkable similarities to cercopithecine primates with respect to their life histories and to the size and complexity of their social groups (Table 1).

View this table:
Table 1

Comparison of the life-history parameters, social structures, social cognitive abilities, and brain organization between spotted hyenas and cercopithecine primates.

CharacteristicSpotted hyenasCercopithecine primates
Life history
Litter size1 or 21
Weaning ageRange 7–24 months, X̄ = 13.5 months6 weeks (talapoins) to 14 months (baboons)
Age at reproductive maturity2–3 years2.5–7 years
Life span (captivity)41 years20–46 years
Male dispersal and female philopatry?YesYes
DietCarnivorousOmnivorous
Socioecology
Group size10–9010–97
Group compositionMultiple females and multiple malesMultiple female and 1 to several males
Multiple generations present in group?YesYes
Core of groupFemale kin groupsFemale kin groups
Hierarchical dominance structure?YesYes
Dominant sexFemalesMales
Cooperative resource defense against conspecifics?YesYes
Cooperative defense against predators andYesYes
interspecific competitors?
Cooperative hunting?YesNo
Intragroup resource competition?YesYes
Communication and social cognition
Elaborate communication using multipleYesYes
sensory modalities?
Recognition of individual conspecifics?YesYes
Recognition of both maternal and paternal kin?YesYes
Maternal rank inheritance?YesYes
Primary mechanisms of maternal rank inheritance?Coalition formation and maternal interventionsCoalition formation and maternal interventions
Social rank affects mate choice?YesYes
Preferred nonkin same-sex social partners?Adjacent but higher-ranking animalsAdjacent but higher-ranking animals
Nepotistic treatment of kin?YesYes
Closest associates?KinKin
Conciliatory tendency15%3–51%
Recognition of 3rd-party relationships?YesYes
Brain organization
Expansion of frontal cortex?UnknownYes

Like macaques and baboons, spotted hyenas are large-bodied mammals with slow life histories. Although the hyena's diet matches that of other large African carnivores (Caro 1994; Kruuk 1972; Mills 1990; Schaller 1972), the foods of both hyenas and cercopithecine primates generally occur in rich, scattered patches appearing unpredictably in space and time. Female hyenas bear litters containing only 1 or 2 cubs, and they nurse each litter for up to 24 months. Thus, hyenas, like primates, produce small litters at long intervals, and their offspring require an unusually long period of nutritional dependence on the mother. Both hyenas and primates experience a long juvenile period during which every individual must learn a great deal about its physical and social environments. Male hyenas reach reproductive maturity at 24 months of age, and most females start bearing young in their 3rd or 4th year. Like many primates, hyenas have a long life span; they are known to live up to 19 years in the wild (Drea and Frank 2003) and they live up to 41 years in captivity (Jones 1982).

The complexity of spotted hyena societies is comparable in most respects to that found in societies of cercopithecine primates, and far exceeds that found in the social lives of any other terrestrial carnivore (e.g., Gittleman 1989, 1996; Holekamp et al. 2000). These hyenas live in permanent complex social groups, called clans, composed of 6–90 individuals. All members of a clan recognize each other, cooperatively defend a common territory, and rear their cubs together at a communal den (Henschel and Skinner 1991; Kruuk 1972). Like cercopithecine primates, hyenas establish enduring relationships with clan-mates that often last many years. Clan size and territory size vary with prey abundance across the species' range, but the clans inhabiting the prey-rich plains of eastern Africa are as large as sympatric baboon troops (e.g., Sapolsky 1993) and they often contain more than 70 individuals (Kruuk 1972). Like baboon troops, hyena clans contain multiple adult males and multiple matrilines of adult female kin with offspring, including individuals from several overlapping generations. Relatedness is high within matrilines but, on average, clan members are only very distantly related because of high levels of male-mediated gene flow among clans, and mean relatedness declines only slightly across clan borders (Van Horn et al. 2004).

Like many primates, hyenas within each clan can be ranked in a linear dominance hierarchy based on outcomes of agonistic interactions, and priority of resource access varies with social rank (Andelman 1985; Frank 1986; Tilson and Hamilton 1984). As in female cercopithecine primates, dominance ranks in hyena society are not correlated with size or fighting ability; instead, power in hyena society resides with the individuals having the best network of allies. In both hyenas and cercopithecine primates, members of the same matriline occupy adjacent rank positions in the group's hierarchy, and female dominance relations are extremely stable across a variety of contexts and over periods of many years. One interesting difference between hyenas and cercopithecine primates in regard to rank is that adult female hyenas dominate adult males, whereas male cercopithecines dominate females. However, as in virtually all cercopithecine species, male hyenas disperse voluntarily from their natal groups after puberty, whereas females are usually philopatric (Boydston et al. 2005; Cheney and Seyfarth 1983; Henschel and Skinner 1987; Mills 1990; Smale et al. 1997). Although adult natal male hyenas dominate adult females ranked lower than their own mothers in the clan's dominance hierarchy while they remain in the natal clan, when males disperse they behave submissively to all new hyenas encountered outside the natal area. This is the time during ontogenetic development at which females begin to dominate males (Smale et al. 1993, 1997). When a male joins a new clan, he assumes the lowest rank in that clan's dominance hierarchy (Smale et al. 1997). Immigrant males rarely fight among themselves; instead they form a queue in which the immigrant who arrived 1st in the clan holds the highest rank in the male hierarchy, and the most recently arrived male the lowest (East and Hofer 2001; Smale et al. 1997).

In contrast to social groups of most cercopithecine primates, which tend to be extremely cohesive, hyena clans are fission-fusion societies in which individuals spend much of their time alone or in small groups, particularly when foraging (Holekamp et al. 1997a, 1997b). Ungulate carcasses represent extremely rich but ephemeral food resources; a group of hungry hyenas can reduce a large antelope to a few scattered bones in less than half an hour. Competition when feeding at carcasses is therefore extremely intense, and dominant hyenas, who can most effectively displace conspecifics from food, gain access to the choicest bits and largest quantities of food. Hyenas often require kin and other allies to defend a carcass from other clan-mates. In addition, hyenas need allies during cooperative defense of the clan's territory against alien conspecifics (e.g., Boydston et al. 2001; Henschel and Skinner 1991). Members of multiple hyena matrilines frequently cooperate to defend their kills against lions or hyenas from other clans, and by doing so risk serious injury or death (Boydston et al. 2001; Henschel and Skinner 1991; Hofer and East 1993; Kruuk 1972; Mills 1990). Help from clan-mates is also often required while hunting ungulate prey: the probability of successfully making a kill increases by approximately 20% with the presence of each additional hunter (Holekamp et al. 1997b). Thus, as in cercopithecine primates, the enduring cooperative relationships found among these long-lived carnivores affect survival and reproduction of individual group members.

Communication Signals, Perceptual Abilities, and Social Cognition

Cercopithecine primates possess well-developed cognitive abilities, making them unusually adept at predicting outcomes of behavioral interactions among their group-mates (e.g., Byrne 1994; Byrne and Whiten 1988; Cheney and Seyfarth 1990, 2003; Harcourt and de Waal 1992; Kamil 1987). They recognize individual conspecifics based on information acquired via multiple sensory modalities, they remember outcomes of earlier encounters with particular conspecifics, and they modify their social behavior on the basis of interaction histories. Furthermore, cercopithecines clearly possess knowledge about social relationships among other group members and adaptively base their decision-making in social situations upon this knowledge (e.g., Cheney and Seyfarth 1990).

Individual recognition.—Spotted hyenas emit a rich repertoire of visual, acoustic, and olfactory signals. They use these signals to distinguish clan members from alien hyenas (Henschel and Skinner 1991; Kruuk 1972; Mills 1990), to recognize other members of their social units as individuals, and to obtain information about signalers' affect and current circumstances. Hyenas can recognize their group-mates using visual, acoustic, or olfactory cues (Kruuk 1972). In the presence of conspecifics, hyenas attend closely to body postures and visual displays of other animals and, especially while feeding at a carcass, they attend to the relative positions of conspecifics; young hyenas, in particular, attempt to gain access to carcasses by entering each feeding melee next to 1 or more potential allies. Hyenas are capable of identifying individual conspecifics on the basis of their long-distance “whoop”vocalizations, and whoops also convey information about the caller's age and sex (East and Hofer 1991a, 1991b; Holekamp et al. 1999). In addition, hyenas encode information about their current motivational state by altering the rate at which they produce individual whoops within a whoop bout and by adjusting the length of the intervals between these calls (Theis et al., in press a). Olfaction plays a similarly important role in the social lives of spotted hyenas. These animals have a keen olfactory sense, and they engage in frequent scent-marking behavior. Each clan appears to have a unique scent signature (Hofer et al. 2001), and wild hyenas mark the boundaries of their group territories with secretions from their scent glands (Boydston et al. 2001; Henschel and Skinner 1991; Kruuk 1972). Hyenas can use olfactory cues to discriminate sex and familiarity of conspecifics (Drea et al. 2002a, 2002b). Both cubs and older hyenas can distinguish scents of their clan-mates from those of hyenas from other clans (Theis et al., in press b).

Recognition of kin.—As in most primates (e.g., Seyfarth 1980; Seyfarth and Cheney 1984), nepotism is common among hyenas, kin spend more time together than do nonkin (Holekamp et al. 1997a), and individuals direct affiliative behavior toward kin more frequently than toward nonkin (East et al. 1993; Wahaj et al. 2004). Hyenas can distinguish vocalizations of kin from those of nonkin, and the intensity of their responses to whoop vocalizations increases with degree of relatedness between vocalizing and listening animals (Holekamp et al. 1999). Although male hyenas do not participate in parental care, sires can recognize their offspring, as is the case in baboons (Buchan et al. 2003), and offspring can also recognize their sires (Van Horn et al. 2004). Furthermore, full siblings from twin litters associate more closely, and direct more affiliative behavior toward each other, than do half-sibling littermates (Wahaj et al. 2004).

Rank acquisition and social memory.—During an early period of intensive learning, each hyena comes to understand its own position in a dominance hierarchy that may contain dozens of other individuals (Holekamp and Smale 1993). Spotted hyenas then appear to remember the identities and ranks of their clan-mates throughout their lives. In the first 2 years of life, juvenile hyenas of both sexes acquire ranks immediately below those of their mothers (Holekamp and Smale 1991, 1993; Smale et al. 1993). This occurs through an elaborate process of associative learning called “maternal rank inheritance”in which the mediating mechanisms are virtually identical to those operating during the process of rank acquisition in many cercopithecine primates (Engh et al. 2000; Horrocks and Hunte 1983; Jenks et al. 1995). In particular, coalitionary aggression plays an important role in acquisition and maintenance of social rank in hyenas (Holekamp and Smale 1993; Mills 1990; Smale et al. 1993; Zabel et al. 1992), as it does in vervets, macaques, and baboons (e.g., Chapais 1992; Cheney 1977; Datta 1986; Walters 1980). By the time hyenas are 8–9 months of age, attack behavior directed at higher-born peers has been completely extinguished and they restrict their attacks to lower-born individuals. The process of rank acquisition relative to nonpeer clan-mates appears to be complete by around 18 months of age (Smale et al. 1993). Furthermore, nonlittermate hyena siblings assume relative ranks that are inversely related to age in a pattern of “youngest ascendancy”exactly like that seen in cercopithecine primates (Holekamp and Smale 1993; Horrocks and Hunte 1983). Here too, the mechanisms involved appear to be identical to those in primates (Chapais and Schulman 1980; Kurland 1977); mothers assist their youngest cubs during resource competition, even when this forces mothers to behave aggressively toward their older offspring (Holekamp and Smale 1993).

Application of knowledge about social rank.—Two types of situations in which knowledge of the social ranks of group-mates can be adaptively applied by hyenas occur during competitive feeding at kills and in choice of mates. Adult hyenas at kills attack animals lower ranking than themselves in the clan's dominance hierarchy, but they never attack higher-ranking individuals because to do so would most likely result in counterattack by the target animal and its allies, as well as potentially serious injury. Only young hyenas with little or no prior experience with particular conspecifics err by inappropriately attacking relatively high-ranking individuals. Male-female interactions in hyenas are almost exclusively initiated and maintained by males (Szykman et al. 2001), and the social ranks of both male and female hyenas influence intersexual patterns of association. Males prefer to associate most closely and mate with the highest-ranking females, although we have not yet identified the mechanism by which males discriminate female rank. Because female reproductive success varies enormously with social rank in this species (Frank et al. 1995; Hofer and East 2003; Holekamp et al. 1996), this discriminatory ability appears to be highly adaptive for male hyenas.

Partner choice and recognition of relationship value.—The value of a relationship reflects the magnitude of social or ecological benefits likely to accrue from it, with highly valuable relationships the most worthy of maintenance and protection (Cords 1988). Because of the strict linear dominance hierarchy that structures every hyena clan, an individual's social rank should reflect its value as a social partner, and thus potential social partners should vary greatly in their value to conspecifics in this species. When conspecifics vary in their relative value as social partners, individuals should possess the ability to assess the value of each potential partner and compete for partners of the highest relative value based on those assessments (Noë and Hammerstein 1994). Primatologists have long known that cercopithecine primates associate most closely with unrelated dominants ranking immediately above them in the social hierarchy (see Cheney et al. [1986] and Schino [2001] for reviews), and they even assign higher value to information they receive about high-ranking social partners than they do to information about low-ranking partners (e.g., Deaner et al. 2005). Similarly, hyenas strongly prefer high-ranking nonkin over low-ranking nonkin as social companions (Holekamp et al. 1997a). Furthermore, patterns of hyena greeting behavior resemble primate patterns of social grooming (East et al. 1993) in which individuals prefer to spend time with, and direct affiliative behavior toward, high-ranking nonkin (Seyfarth and Cheney 1984). This pattern indicates that hyenas, like many primates, recognize that some group members are more valuable social partners than others. Adult hyenas of both sexes associate most often with nonkin holding ranks similar to their own, and high-ranking animals are more gregarious than low-ranking individuals (Smith et al. 2007).

Repair of damaged relationships.—Affiliative gestures functioning to repair social relationships damaged during a fight are called reconciliation behaviors (de Waal 1993). Reconciliation is an important behavioral mechanism regulating social relationships and reducing social tension in hierarchical primate societies (Aureli and de Waal 2000). Reconciliation occurs in many primates during friendly reunions between former opponents shortly after aggressive conflicts (reviewed by Aureli and de Waal 2000). Similarly, spotted hyenas use unsolicited appeasement and greeting behaviors to reconcile approximately 15% of their fights (East et al. 1993; Hofer and East 2000; Wahaj et al. 2001). As is also true in many primates (Aureli 1992; Aureli and van Schaik 1991a, 1991b; Kappeler 1993), victims in hyena fights are significantly more likely to initiate reconciliation than are aggressors, and male hyenas are more likely to initiate reconciliation than females. The latter finding is not surprising in a female-dominated society because males may benefit from information about the state of their relationship with each higher-ranking female (Wahaj et al. 2001).

Recognition of 3rd-party relationships.—One aspect of social intelligence in which, until recently, primates appeared to differ qualitatively from other gregarious mammals was their ability to recognize tertiary, or 3rd-party, relationships among conspecific group members (Tomasello and Call 1997). These involve interactions and relationships in which the observer is not directly involved. For example, female vervet monkeys (Chlorocebus aethiops) respond to the distress call of an infant by orienting toward the infant's mother, indicating that they perceive an association between the mother and infant regardless of whether or not they are related to that mother-infant pair (Cheney and Seyfarth 1980). Several primate species, including vervets and various baboons, have been shown to use information about social relationships among conspecifics in activities such as recruiting useful allies, challenging competitors, redirecting aggression, and reconciling after fights (Bachmann and Kummer 1980; Cheney and Seyfarth 1989; Silk 1999). Laboratory tests have suggested that macaques can use mental representations to categorize tertiary kin relationships (Dasser 1988), and recent field experiments have shown that Chacma baboons (Papio ursinus) categorize information hierarchically about tertiary rank and kin relationships among other group members (Bergman et al. 2003).

We expected that, if indeed hyenas can recognize 3rd-party relationships based on the social ranks and kin relationships of other hyenas, then they would be able to use this knowledge adaptively in 2 ways during and after agonistic interactions (Engh et al. 2005). First, we predicted that hyenas would be able to discriminate between the ranks of 2 individuals engaged in a fight, and that they would aid the higher-ranking combatant, regardless of their own social rank in relation to those of the fighters. Second, we predicted that hyenas would be able to recognize the relatives of their former opponents, and that they would increase their rates of aggression toward relatives of their opponents after a fight, as occurs in cercopithecine primates (e.g., Cheney and Seyfarth 1986, 1989). Our analyses of aggressive interactions strongly indicated that hyenas can and do recognize 3rd-party relationships (Engh et al. 2005).

When aggression between 2 hyenas escalates, 1 or more others may join the skirmish by forming a coalition with the attacker against the target individual. Typically, animals joining to form coalitions are all dominant to the victim (Zabel et al. 1992). Thus, a hyena considering an attack might benefit, for example, when attempting to displace a larger subordinate animal from food, by delaying its attack until the arrival of a potential ally who is higher ranking than the target animal. If a hyena increases its rate of aggression only after a hyena that is higher ranking than itself arrives on the scene, then the animal might be following a simple rule of thumb, such as “Only attack a larger subordinate when another individual is present who is higher ranking than yourself.”Use of this sort of simple mental algorithm would not require that hyenas be able to recognize 3rd-party relationships among their group-mates. However, if a hyena's attack rate also increases after the arrival of an individual who is dominant to the victim but subordinate to the attacker, then the attacking hyena must recognize the relative ranks of the other 2 individuals. In the latter case, the hyena would be demonstrating that it can indeed recognize tertiary relationships.

Engh et al. (2005) found evidence that hyenas that join ongoing disputes do so in a manner consistent with recognition of relative rank relationships. When hyenas joined fights in progress, they almost always joined on the side of the dominant animal, even when that animal was lower ranking than they were. Zabel et al. (1992) suggested that hyenas have a strong tendency to do what other hyenas are doing and therefore that hyenas often join coalitions as a result of social facilitation (Zajonc 1965) rather than based on an assessment of relative ranks. Because most aggression in hyena society is directed toward lower-ranking individuals, simply joining an aggressor is likely to result in the pattern observed by Engh et al. (2005), in which the dominant animal is aided far more frequently than the subordinate animal. However, when we examined rare instances of rank reversals, situations in which the initiator of aggression was lower ranking than the target, animals that intervened in these fights overwhelmingly helped the dominant animal. This observation suggests that hyenas recognize 3rd-party rank relationships, and that they are not just following simple rules that are cognitively less demanding, such as “join in support of aggressors”or “join whichever animal is winning.”Clearly, hyenas will aid the dominant animal even when that individual is losing the fight. Examination of our postconflict aggression data also strongly supported the notion that hyenas recognize tertiary kin relationships. Aggressors were more likely to attack the relatives of their opponents after a fight than during a matched control period, and after a fight they were more likely to attack relatives of their opponents than to attack other lower-ranking animals unrelated to their opponents (Engh et al. 2005).

Future directions in the study of hyena cognition.—An ideal test of the social complexity hypothesis would involve comparative analysis of the cognitive abilities of multiple hyena species. The 4 extant species comprising the family Hyaenidae exhibit a spectrum of sociality ranging from the solitary striped hyena (Hyaena hyaenaKruuk 1976; Wagner, in press) to the highly gregarious spotted hyena. The existence of this social spectrum offers a powerful tool for understanding the evolution of many different aspects of social behaviour (e.g., Lacey 2000), including social intelligence. If we find evidence that less-gregarious hyaenids (e.g., striped hyenas and brown hyenas [Parahyaena brunnea]) lack some of the cognitive abilities previously documented in spotted hyenas, this will support the notion that social complexity favors enhancement of intelligence. We have recently initiated a field study of striped hyenas; here we will administer the same simple standardized “intelligence tests”we are currently administering to free-living spotted hyenas. Although these 2 species are very closely related and confront many of the same ecological problems, the social complexity hypothesis predicts that spotted hyenas should perform far better on such standardized tests than striped hyenas because spotted hyenas have been challenged for many thousands of generations by the labile behavior of conspecifics whereas striped hyenas have not.

Brain Organization

Cognitive processes are, of course, mediated by nervous systems; thus, the social complexity hypothesis predicts that nonprimates living in complex societies should possess brain structures mediating social behavior that show the same relative enlargement as that seen in primates. The social complexity hypothesis considered specifically in relation to nervous systems has been dubbed “the social brain hypothesis”(Barton and Dunbar 1997; Brothers 1990). In relation to overall body size, the brains of primates are relatively large and complex compared to those of other animals, including most nonprimate mammals (Harvey and Krebs 1990; Jerison 1973; Macphail 1982). The relatively large brain size noted among primates is primarily due to the unusually large expanse of neocortex, the laminated gray matter covering much of the outer surface of the brain (Dunbar 2003). Such variables as social group size (Dunbar 1992, 1995), number of social partners, grooming clique size (Kudo and Dunbar 2001), and frequency of social play (Lewis 2001) all correlate strongly with neocortical volume in primates.

The mammalian brain comprises a number of functionally distinct systems, and natural selection acting on particular behavioral capacities causes size changes selectively in the systems mediating those capacities (Barton and Harvey 2000). Frontal cortex is known to mediate complex social behavior in humans and other mammals (Adolphs 2001; Amodio and Frith 2006), so the social brain hypothesis predicts we should find larger frontal cortex volumes in gregarious species than in closely related solitary species. Among primates, the frontal area is covered by a disproportionately voluminous neocortex, whereas a similar relationship may not exist among other mammalian species. Dunbar (2003) suggested that the relatively large frontal neocortex in primates is specifically associated with the demands imposed by life in complex -societies. Thus, social complexity in primates appears to be related broadly to greater brain volume and specifically to expansion of frontal cortex (Dunbar and Bever 1998). If the social brain hypothesis is correct, we should find these same patterns in the brains of nonprimate mammals that, although closely related to each other, vary with respect to the complexity of their social lives. We are currently attempting to evaluate this prediction of the social brain hypothesis within the family Hyaenidae (Holekamp et al., 2007).

One of our goals in this work is to conduct accurate volumetric assessments of frontal cortex in relation to total brain volume in spotted hyenas and compare these measurements with those obtained from the closest living relatives of spotted hyenas and also from other carnivore species that vary with respect to social complexity. The spotted hyena is 1 of only 4 extant species in the family Hyaenidae, but these 4 species span a wide spectrum of social complexity. In contrast to either the highly gregarious spotted hyena or the solitary striped hyena, the aardwolf (Proteles cristata) lives in monogamous pairs (Richardson 1988), and the brown hyena lives in small family groups (Mills 1990). Spotted hyenas occur sympatrically with all 3 of these other species in Africa. The 4 hyena species last shared a common ancestor approximately 11 million years ago (Koepfli et al. 2006). Using skeletal material from the 4 extant hyaenids, we have recently started using computed tomography to image the endocranial cavity in order to create a virtual brain endocast. The endocasts will be used to examine the relationship between frontal cortex volume and social complexity.

Our preliminary work suggests that the relative amount of frontal cortex exclusive of motor control areas is greater in spotted hyenas than in the other carnivore species examined to date. Our computed tomography analysis of virtual brains reconstructed from multiple skulls from each hyena species, combined with our on-going cytoarchitectonic analysis, should offer a strong test of the social brain hypothesis. Specifically, the hypothesis predicts that size of frontal cortex should increase relative to total cortical volume and brain volume in the following order within the family Hyaenidae, as we move from solitary to highly gregarious: striped hyenas, aardwolves, brown hyenas, and spotted hyenas. We expect that our current work with the hyena family will set the stage for a larger-scale analysis of the relationship between social complexity and brain structure in other carnivores to determine whether the same relationship between frontal cortex and social complexity found in primates holds within this 2nd large order of mammals.

Conclusions

The social complexity hypothesis posits that big brains and great intelligence have been favored by selection pressures imposed by life in challenging social environments (Byrne and Whiten 1988; Humphrey 1976; Jolly 1966). De Waal and Tyack (2003) suggest the most challenging societies are those in which animals live in stable multigenerational units, group members recognize each other individually, individuals cooperate as well as compete for resource access, and a substantial amount of learning occurs during social development. Although some primatologists claim primate societies are more complex than those of other mammals (e.g., Dunbar 2003), we disagree. Work to date on spotted hyenas has shown that they live in social groups just as large and complex as those of cercopithecine primates, that they experience an extended early period of intensive learning about their social worlds like primates, that the demand for social dexterity during their competitive and cooperative interactions is no less intense than it is in primates, and that hyenas appear to be capable of many primate-like feats of social recognition and cognition.

Much remains to be learned about social cognition in hyenas. For example, we do not yet know whether hyenas use hierarchical classification of rank and kinship, as occurs in baboons (Bergman et al. 2003). Nor do we know to what extent hyenas might be able to “keep score,”as tamarins do (Hauser et al. 2003), of earlier altruistic and selfish acts directed at them by conspecifics. Whether hyenas are capable of tactical deception or cultural transmission of behavior will not be known until the appropriate controlled experiments can be conducted. In any case, along with odontocete cetaceans and elephants, hyenas continue to offer a useful model system in which to test hypotheses suggesting cognitive abilities that distinguish primates from other mammals. Furthermore, a comparison between the cognitive abilities and brains of spotted hyenas and those of other hyena species with less complex social systems should allow us to determine whether convergent evolution of brain and behavior has occurred in nonprimate mammals in response to social complexity.

Acknowledgments

This work was supported by National Science Foundation grant IOB0618022. We thank L. Smale and B. H. Blake for insightful comments on an earlier draft of this paper.

Footnotes

  • Kay E. Holekamp was the C. Hart Merriam Award recipient.

  • Associate Editor was Barbara H. Blake.

Literature Cited

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