My research program in social behavior focuses on social learning and group cohesion. Using naturalistic tasks that I present to captive animals in socially relevant contexts, I can investigate how social interaction modulates behavior, problem- solving, and cognitive performance. By studying and comparing models of carnivore and primate foraging, I can better understand how group-living animals modify their actions to meet environmental demands. A primary interest is determining whether similar factors, related to having a complex social organization, influence learning and performance across taxonomic groups. I am also interested in how animals learn rules of social conduct and maintain social cohesion, as evidenced by their patterns of behavioral developmental, the intricate balance between aggression and play, the expression of scent marking, and the social facilitation or inhibition of behavior.
Deciphering the chemical components contained in olfactory cues has provided important insights into the functional significance of mammalian scent marking. Through advances in semiochemistry, volatile and non-volatile components of olfactory signals have been shown to vary by species, family, sex, reproductive state, dominance status, and even individual identity, supporting suggestions that scent marking serves to transmit information about e.g. group membership, kinship, sexual receptivity, competitive ability and resource ownership. Women and female mice behavioral response to conspecific male odorants has suggested that olfactory cues may also transmit information about genetic quality and compatibility and recent evidence confirms that genes from the major histocompatibility complex influence rodent semiochemical profiles. Here, using a primate model and a new analytical approach, we provide the first semiochemical evidence relating male olfactory signals to genetic characteristics, including both genome-wide heterozygosity and genetic relatedness. The relationship between olfactory profiles and genetic constitution is apparent, however, only during the highly competitive breeding season. As heterozygosity in lemurs accurately predicts health and survivorship, our findings identify olfactory cues as honest indicators of individual quality. Therefore, beyond showing that semiochemicals could underlie olfactory-guided kin recognition and nepotism, we provide a putative olfactory mechanism to guide female mate choice and male-male competition.
To better understand the relation between form and function in the complex olfactory com-munication system of the ringtailed lemur (Lemur catta), we integrated observational, experimental, and chemical approaches applied to a population of semi free-ranging animals at the Duke Lemur Center in Durham, North Carolina. Our aim was to examine sex-role reversal in the expression and function of scent marking and unravel the contribution of multimodal components of information transfer, with the unifying framework for all three avenues of our research being that multiplicity of form implies multiplicity of function.
Female social dominance characterizes many strepsirrhine primates endemic to Madagascar, but currently there is no comprehensive explanation for how or why female lemurs routinely dominate males. Reconstructing the evolutionary pressures that may have shaped female dominance depends on better understanding the mechanism of inheritance, variation in trait expression, and correlating variables. Indeed, relative to males, many female lemurs also display delayed puberty, size monomorphism, and ‘masculinized’ external genitalia. As in the spotted hyena (Crocuta crocuta), a species characterized by extreme masculinization of the female, this array of traits focuses attention on the role of androgens in female development. Consequently, I examined endocrine profiles and social interaction in the ringtailed lemur (Lemur catta) to search for a potential source of circulating androgen in adult females and an endocrine correlate of female dominance or its proxy, aggression. I measured serum androstenedione (A4), testosterone (T), and estradiol (E2) in reproductively intact, adult lemurs (10 females; 12 males) over four annual cycles. Whereas T concentrations in males far exceeded those in females, A4 concentrations were only slightly greater in males than in females. In both sexes, A4 and T were positively correlated, implicating the ∆4-biosynthetic pathway. Moreover, seasonal changes in reproductive function in both sexes coincided with seasonal changes in behavior, with A4 and T in males versus A4 and E2 in females increasing during periods marked by heightened aggression. Therefore, A4 and/or E2 may be potentially important steroidal sources in female lemurs that could modulate aggression and underlie a suite of masculinized features.
The extravagance and diversity of external genitalia have been well characterized in male primates; however, much less is known about sex differences or variation in female form. Our study represents a departure from traditional investigations of primate reproductive anatomy because we (1) focus on external rather than internal genitalia, (2) measure both male and female structures, and (3) examine a strepsirrhine rather than an anthropoid primate. The subjects for morphological study were 21 reproductively intact, adult ring-tailed lemurs (Lemur catta), including 10 females and 11 males, two of which (one per sex) subsequently died of natural causes and also served as specimens for gross anatomical dissection. Male external genitalia presented a typical masculine configuration, with a complex distal penile morphology. In contrast, females were unusual among mammals, presenting an enlarged, pendulous external clitoris, tunneled by the urethra. Females had a shorter anogenital distance and a larger urethral meatus than did males, but organ diameter and circumference showed no sex differences. Dissection confirmed these characterizations. Noteworthy in the male were the presence of a ‘levator penis’ muscle and discontinuity in the corpus spongiosum along the penile shaft; noteworthy in the female were an elongated clitoral shaft and glans clitoridis. The female urethra, while incorporated within the clitoral body, was not surrounded by erectile tissue, as we detected no corpus spongiosum. The os clitoridis was 43% the length and 24% the height of the os penis. Based on these first detailed descriptions of strepsirrhine external genitalia (for either sex), we characterize those of the female ring-tailed lemur as moderately ‘masculinized.’ Our results highlight certain morphological similarities and differences between ring-tailed lemurs and the most male-like of female mammals, the spotted hyena (Crocuta crocuta), and call attention to a potential hormonal mechanism of ‘masculinization’ in female lemur development.
The function of olfactory signaling in social species is less well understood than in asocial species. Consequently, we examined olfactory communication in the ringtailed lemur (Lemur catta) – a socially complex primate that retains a functional vomeronasal organ, possesses well-developed scent glands, and exhibits a suite of scent-marking behaviour. To assess the information content of different types of scent gland secretions, we decoupled olfactory cues from the visual and behavioural modalities with which scent marking is normally associated. We presented male and female subjects (signal receivers) with a series of choice tests between odours derived from conspecific donors (signaler senders) varying by sex, age, social status, and reproductive condition. We additionally examined the influence of the receivers’ reproductive state and familiarity with the signaler. The reproductive condition, social status, and familiarity of senders and receivers impacted signal transmission; specifically, male receivers attended most to the odours of conspecifics in breeding condition and to the odours of familiar, dominant animals. By contrast, females varied their responses according to both their own reproductive state and that of the sender. Based on male and female patterns of countermarking, we suggest that scent marking serves a function in intergroup spacing and intrasexual competition for both sexes, as might be expected in a female-dominant species. By contrast, minimal female interest in male odours counters a female mate-choice function for scent marking in this species. Nonetheless, scent marks are critical to male-male competition and, therefore, may be subject to sexual selection.
This chapter focuses on the ‘social intelligence’ of spotted hyenas (Crocuta crocuta), as inferred by the manner in which they solve daily problems arising from behavioral interactions. For comparative purposes, we frame our review in the context of evolutionary models of primate intelligence. We begin with a presentation of spotted hyena natural history, underscoring some of this species’ unusual attributes, followed by a discussion of their life history variables, highlighting certain features shared with primates. The ensuing commentary on social organization and behavioral ecology centers on the balance between aggression and affiliation, and provides an account of various mechanisms that contribute toward maintaining group cohesion. Our final discussion of cooperative hunting and commuting addresses the cognitive implications of elaborate foraging strategies. Throughout, we consider aspects of the spotted hyena’s behavioral repertoire that reflect the complexity of social interaction and the capacity for individual storage and retrieval of information about a changing environment. We propose that current hypotheses relating life history variables, feeding ecology, and social complexity to the evolution of primate intelligence should be tested against other taxa in which species display similar attributes.
Among all extant mammals, only the female spotted hyaena (Crocuta crocuta) mates and gives birth through the tip of a peniform clitoris. Clitoral morphology is modulated by foetal exposure to endogenous, maternal androgens. First births through this organ are prolonged and remarkably difficult, often causing death in neonates. Additionally, mating poses a mechanical challenge for males, as they must reach an anterior position on the female’s abdomen and then achieve entry at the site of the retracted clitoris. Here we report that interfering with the actions of androgens prenatally permanently modifies hyaena urogenital anatomy, facilitating subsequent parturition in nulliparous females who, thereby, produce live cubs. By contrast, comparable, permanent anatomical changes in males probably preclude reproduction, as exposure to prenatal anti-androgens produces a penis that is too short and has the wrong shape necessary for insertion during copulation. These data demonstrate that the reproductive costs of clitoral delivery result from exposure of the female foetus to naturally circulating androgens. Moreover, the same androgens that render an extremely unusual and laborious process even more reproductively costly in the female are apparently essential to the male’s physical ability to reproduce with a normally masculinized female.
Many primates, including humans, live in complex, hierarchical societies where social context and status affect daily life. Nevertheless, primate learning studies typically test single animals in limited laboratory settings where important effects of social interactions and relationships cannot be studied. As a first investigation of the impact of sociality on associative learning, we compared individual performances of group-tested rhesus monkeys (Macaca mulatta) across various social contexts. We used a traditional discrimination paradigm that measures an animal’s ability to form associations between cues and obtaining food in choice situations, but adapted the task for group-testing. After training a 55-member colony to separate on command into two subgroups, composed of either high- or low-status families, we exposed animals to two color discrimination problems, one with all monkeys present (combined condition), the other in their ‘dominant’ and ‘subordinate’ cohorts (split condition). Next, we manipulated learning history by testing animals on the same problems, but with the social contexts reversed. Monkeys from dominant families excelled in all conditions, but subordinates performed well in the split condition only, regardless of learning history. Subordinate animals had learned the associations, but expressed their knowledge only when segregated from higher-ranking animals. Because aggressive behavior was rare, performance deficits likely reflected voluntary inhibition. This experimental evidence of rank- related, social modulation of performance calls for greater consideration of social factors when assessing learning and may have relevance to evaluating human scholastic achievement.
To interfere with the unusually masculine ‘phallic’ development that characterizes female spotted hyaenas, pregnant hyaenas were treated with anti-androgens. Effects on genital morphology and plasma androgen concentrations of infants were studied during the first 6 months of life. Although there were consistent ‘feminizing’ effects of prenatal anti-androgen treatment on genital morphology in both sexes, such exposure did not produce males with extreme hypospadia, as it does in other species, nor did it produce females with a ‘typical’ mammalian clitoris and external vagina. ‘Feminization’ of males resulted in a penis with the morphological features of the hyaena clitoris, and ‘feminization’ of females exaggerated the sex differences that are typical of this species. Effects of treatment were present at birth and persisted for at least six months. Flutamide and finasteride treatment of pregnant females also markedly reduced circulating concentrations of testosterone and dihydrotestosterone in maternal plasma during pregnancy. In the infants of treated mothers, plasma ?4 androstenedione was reduced in daughters, but not sons, consistent with an epigenetic hypothesis previously advanced to explain hormonal ‘masculinization’ of females. The present ‘feminizing’ effects of prenatal anti- androgen treatment are consistent with contemporary understanding of sexual differentiation, that accounts for morphological variation between the sexes in terms of steroids. However, current theory does not account for the basic genital structure of females and our data suggest that development of the male penis and scrotum, and the female clitoris and pseudoscrotum, in the spotted hyaena may involve both androgen-dependent and androgen-independent components.
The early social development of spotted hyaenas, Crocuta crocuta, is marked by a dramatic transition at 2-3 weeks of age, when infants are taken from the isolation of their natal den, where they are intensely aggressive, to the communal den, where they meet most clan members for the first time. This study examined behaviour in eight sets of captive twins during the first month of life to document the changes that prepare young hyaenas for social integration at the communal den. Bite shakes, the most extreme aggressive behaviour, declined markedly within the first week of life, but other forms of aggression remained constant. During week 1, low-intensity prosocial behaviour occurred primarily between mother and cub. By week 2, higher-intensity social play emerged, occurring mainly between siblings. In weeks 3 and 4, cub interactive play was most frequent, lasted longer and was more vigourous. Locomotor and object play did not emerge until weeks 3 and 4, respectively. Dominance relations between siblings were operationally defined by submissive withdrawals. Accordingly, aggression was unidirectional, with dominants initiating most interactions. By contrast, play was reciprocal and equally initiated by dominant and subordinate cubs. Maternal interruption of cub behaviour mainly occurred during extreme aggressive interactions, but rarely during vigourous play. Results showed that prosocial behaviour emerged in captive hyaena cubs following a decline in severe aggression and before the time wild cubs are taken from the natal to the communal den. We suggest that play may modulate aggression, following the establishment of a dominance relationship, and may serve an immediate prosocial function to prepare aggressive infant hyaenas for integration into the clan.