The erect ?penis? is a flag of submission in a female-dominated society: greetings in Serengeti spotted hyenas

Abstract

In East Africa, spotted hyenas live in large clans in a highly structured society dominated by females. A clan is a fission-fusion society where members are often solitary or in small groups. Spotted hyenas have a ritualized greeting during which two individuals stand parallel and face in opposite directions. Both individuals usually lift their hind leg and sniff or lick the anogenital region of the other. The unique aspect of greetings between individuals is the prominent role of the erect 'penis' in animals of both sex. Female spotted hyenas have fused outer labiae and a 'pseudo-penis' formed by the clitoris which closely resembles the male penis and can be erected. During greetings subordinates signalled submission with gestures which were not necessarily reciprocated by the dominant participant. Asymmetries were most pronounced in greetings between adult females where the probability of asymmetries increased with the divergence in rank between partners. Greetings between adult females and males were uncommon and restricted to males above median rank, principally the alpha male. Models of primate affiliative behavior assume that benefits derived from social relationships with different individuals are not equal and that individuals are selected to maximize the benefits they receive from social relationships with others. The observed distribution of greetings between partners of different rank matched the predictions of these models. An examination of non-adaptive hypotheses on the evolution of the 'pseudo-penis' demonstrated that the conventional scenario linking (initial) virilization of female genitalia with selection for female dominance does not explain either the initial virilization, nor the evolution of the 'pseudo-penis' to its current form and use. We sketch a new scenario that links (1) initial virilization to the occurrence of neonatal siblicide amongst members of a twin litter, and (2) costs of maintenance, 'pseudo-penile' control over copulation and male submission. Our analysis confirms previous adaptive hypotheses on the function of the 'pseudo-penis' in greetCorrespondence to: M.L. East ings and suggests new hypotheses to account for hitherto unexplained features.

Context modulates signal meaning in primate communication

“…Unidirectional subordination signals also have been reported in chimpanzees (39,40) and, possibly, are used by wolves and dogs (41,42), hyenas (43), and ring-tailed lemurs (44).…”

Exposure to naturally circulating androgens during foetal life incurs direct reproductive costs in female spotted hyenas, but is prerequisite for male mating

“…B (2002) Authors have previously proposed varying explanations for the evolution of 'masculinized' external genitalia in female spotted hyenas (reviewed in Glickman et al 1993;Frank 1997). The majority have hypothesized that such masculinization was an incidental by-product of selection for raised foetal androgens (Gould 1981;Gould & Vrba 1982), stipulating that these androgens either facilitated adult competitive success during feeding at a kill (Hamilton et al 1986), for example by mediating dominant social status (Frank 1997), or promoted successful neonatal aggression during competitive nursing (East et al 1993). Others have provided alternative explanations that involve clitoral maculinization as a direct target of selection.…”

Adaptation, Exaptation, and Constraint: A Hormonal Perspective

“…As an unselected but beneficial trait, its role in the greeting ceremony would be an exaptation. Current students of hyenas (East et al 1993;Frank 1997a) seem to agree that the female penile clitoris is probably an unselected side effect of selection for female aggressiveness, although they disagree on how aggressiveness benefits females (East et al 1993;East and Hofer 1997;Frank 1997aFrank , 1997b.…”