Effect of prenatal androgens on click-evoked otoacoustic emissions in male and female sheep (Ovis aries)

Otoacoustic emissions (OAEs) were measured in male and female Suffolk sheep (Ovis aries). Some sheep had been administered androgens or estrogens during prenatal development, some were gonadectomized after birth, and some were allowed to develop normally. As previously reported for spotted hyenas, gonadectomy did not alter the OAEs for either sex; accordingly, the untreated/intact and the untreated/gonadectomized animals were pooled to form the control groups. The click-evoked otoacoustic emissions (CEOAEs) exhibited by the female control group (N = 12) were slightly stronger (effect size = 0.42) than those in the male control group (N = 15), which is the same direction of effect reported for humans and rhesus monkeys. Females administered testosterone prenatally (N = 16) had substantially weaker (masculinized) CEOAEs than control females (effect size = 1.15). Both of these outcomes are in accord with the idea that prenatal exposure to androgens weakens the cochlear mechanisms that underlie the production of OAEs. The CEOAEs of males administered testosterone prenatally (N = 5) were not different from those of control males, an outcome also seen in similarly treated rhesus monkeys. Males administered dihydrotestosterone (DHT) prenatally (N = 3) had slightly stronger (hypo-masculinized) CEOAEs than control males. No spontaneous otoacoustic emissions (SOAEs) were found in any ears, a common finding in non-human species. To our knowledge, this is the first ruminant species measured for OAEs.     

Sex differences in otoacoustic emissions measured in rhesus monkeys (Macaca mulatta)

Click-evoked otoacoustic emissions (CEOAEs) and distortion-product OAEs (DPOAEs) were measured in about 60 rhesus monkeys. CEOAE strength was substantially greater in females than in males, just as in humans. DPOAE strength was generally slightly stronger in females, just as in humans. In males, CEOAEs were weaker (more masculine) in the fall breeding season and in winter than in the summer. In females, CEOAEs were slightly stronger (more feminine) in the fall, when sex steroids are elevated in females (and males), than in the summer when rhesus monkeys are reproductively quiescent. Thus, the sex differences in CEOAEs were greater in the fall than in the summer. We presume that the seasonal fluctuations in OAEs reflect activational hormonal effects, while the basic sex differences in OAEs likely reflect organizational effects of prenatal androgen exposure. Some monkeys of both sexes had been treated with additional testosterone or the anti-androgen flutamide during prenatal development. In accord with expectations, prenatal androgen treatment weakened CEOAEs in females, and prenatal flutamide treatment strengthened CEOAEs in males. For DPOAEs, the differences between treated and untreated groups were mostly small and often inconsistent. Taken as a whole, the data from both rhesus monkeys and humans suggest that the linear, reflection-based mechanism of OAE production that underlies CEOAEs is more sensitive to prenatal androgenic processes than is the nonlinear distortion mechanism that underlies DPOAEs.     

Social intelligence in the spotted hyena (Crocuta crocuta)

If the large brains and great intelligence characteristic of primates were favoured by selection pressures associated with life in complex societies, then cognitive abilities and nervous systems with primate-like attributes should have evolved convergently in non-primate mammals living in large, elaborate societies in which social dexterity enhances individual fitness. The societies of spotted hyenas are remarkably like 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 recognize third-party kin and rank relationships among their clan mates, and they use this knowledge adaptively during social decision making. However, hyenas appear to rely more intensively than primates on social facilitation and simple rules of thumb in social decision making. No evidence to date suggests that hyenas are capable of true imitation. Finally, it appears that the gross anatomy of the brain in spotted hyenas might resemble that in primates with respect to expansion of frontal cortex, presumed to be involved in the mediation of social behaviour.     

The relationships between otoacoustic emissions and relative lengths of fingers and toes in humans

Both otoacoustic emissions (OAEs) and the relative length of the index and ring fingers (the 2D:4D ratio) exhibit large sex differences, and both exhibit masculinization effects in female homosexuals and bisexuals. Because these sex differences exist in young children, the implication is that both types of measure are affected by prenatal androgen exposure, but it has been unknown to what degree these two types of measure are related. Accordingly, OAEs and the relative lengths of the fingers and the toes were measured in 59 heterosexual females, 55 heterosexual males, 29 homosexual females, and 33 homosexual males. The correlations between the two types of measure were unexpectedly quite low in both the heterosexual and nonheterosexual groups. For example, the correlation between number of spontaneous OAEs per ear and 2D:4D was less than 0.25, for both sexes and both sexual orientations. One interpretation of these results is that the prenatal hormonal mechanisms producing the sex differences in OAEs differ in quality, degree, or timing from those producing the sex differences in relative finger length. That is, OAEs and 2D:4D may be windows onto slightly different prenatal processes or times during prenatal development. Measures of mental-rotation ability also were obtained on these participants, and those correlations with relative finger length also were small.     

Androgens and the role of female "hyperaggressiveness" in spotted hyenas (Crocuta crocuta)

It has been suggested that female dominance in spotted hyenas evolved due to selection for "hyperaggressive" androgenized females. According to this view, virilized external genitalia of female hyenas developed as a byproduct of selection for "androgen-facilitated social dominance." The evidence that female hyenas have higher androgen levels than males or other female mammals is inconclusive. We compared concentrations of testosterone (T), 5alpha-dihydrotestosterone (DHT), and androstenedione (AE) from a population in the Serengeti. Females had significantly lower T and DHT levels than predispersal and postdispersal males. AE levels did not significantly differ between females and postdispersal males, but were significantly lower in predispersal males. Our results, and those from studies that have demonstrated that male and female hyenas experience similar levels of maternal androgens during fetal development, provide little support for a theory of selection for female dominance and hyperaggressiveness through enhanced secretion of androgens. Our data are consistent with an alternative view that female virilization is a byproduct of selection for precocial aggressive cubs of both sexes. According to this view, high investment in lactation favored selection for accelerated fetal development, high neonatal aggression, and facultative siblicide.     

Patterns of growth of the mandibular corpus in spotted hyenas (Crocuta crocuta) and cougars (Puma concolor)

Differences in jaw morphology among adult carnivorans are well established, but the ontogenetic mechanisms by which these differences arise are largely unexplored. Mandibular ontogeny in Crocuta crocuta and Puma concolor is analysed biomechanically using principles of beam theory. In each species, the development of cross-sectional properties of the mandibular corpus associated with rigidity under loading follows a biphasic pattern of growth. In early postnatal growth, deposition of cortical bone appears to be constrained by the overall weaker tissue with which juvenile skeletons are constructed and by the need to volumelrically accommodate the developing teeth within their bony crypts. Thus, this stage of growth is characterized by a net periosteal deposition of bone and a swelling of the medullary cavity. In late postnatal growth, the constraints on endosteal deposition of bone are relieved as the permanent teeth erupt; thus, cortical thicknesses increase sharply by periosteal expansion as well as medullary contraction. Finally, it is noted that basic differences in jaw construction between Crocuta and Puma appear to develop prenatally as they are largely in place at birth. Hence, postnatal development enhances, but does not soley contribute to, the biomechanical differences in the jaws of these species.     

Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females

A long-term study of immigrant male spotted hyenas (Crocuta crocuta) living in large multimale/multifemale groups (clans) demonstrated that males acquire social status by queuing. Maximumlikelihood estimates of parameters of a stochastic queuingmodel that assessed queuing discipline confirmed that immigrantmales respected the convention that their positions in a queueof typically 15 or more individuals was determined by theirsequence of arrival. Levels of aggression among males were low;males did not attempt to improve their social status throughphysical contests. Size and body mass did not influence malesocial status. The stability of queues was insured by an increasein the rate at which males formed coalitions against othermales as they rose in social status and by coalitions between high-ranked males and dominant females. High-ranked, long-tenuredmales chiefly consorted with ("shadowed") and focused theiraffiliative behavior on females of high reproductive valueand disrupted attempts by subordinate males to associate withthese females. High-ranked males also supported females againstlower-ranked males that harassed them. In contrast, lower-ranked,short-tenured males focused their affiliative behavior on young adult females and rarely shadowed or defended females. Malesthat did not disperse from their natal clan (nondispersers)quickly acquired top rank in the male social hierarchy. Irrespectiveof the social status acquired from their mother when young,nondisperser adult males submitted to all adult females.     

Transient genital abnormalities in striped hyenas (Hyaena hyaena)

The highly masculinized genitalia of female spotted hyenas Crocuta crocuta is unique among mammals: Crocuta have no external vagina so urination, penile intromission and parturition take place through the clitoris, which mimics a fully erectile male penis. Among hyenids, virilization of external female genitalia has previously been observed only in Crocuta, so functional explanations of masculinization have focused on aspects of social ecology unique to the species. Here we first show that the striped hyena Hyaena hyaena exhibits both unusual similarity in male and female androgen concentrations and transient genital anomalies characterized by a convergence in genital appearance among young males and females. We then evaluate hypotheses regarding the evolution of genital masculinization in the Hyaenidae and other taxa. Hyaena are behaviorally solitary, so discovery of unusual genital development patterns in this species does not support any current evolutionary models for masculinization in Crocuta, which all rely on the trait originating within a highly social species. Some hypotheses can be modified so that masculinization in Crocuta represents an extreme elaboration of a preexisting trait, shared as a homology with Hyaena.     

Of arcs and vaults: the biomechanics of bone‐cracking in spotted hyenas (Crocuta crocuta)

The ability to break open large bones has evolved independently in only three groups of carnivorous mammals, all of which have robust teeth, vaulted foreheads, and pronounced sagittal crests. One unusual skull feature, present in bone‐cracking members of the family Hyaenidae, is a caudally elongated frontal sinus, hypothesized to function in resistance to bending and stress dissipation during bone‐cracking. In the present study, we used finite element (FE) analysis to examine patterns of stress distribution in the spotted hyena (Crocuta crocuta) skull during unilateral biting, and inquire about the functional role of the fronto‐parietal sinus in stress dissipation. We constructed and compared three FE models: (1) a ‘normal’ model of an adult Crocuta skull; (2) a model in which the caudal portion of the fronto‐parietal sinus was filled with bone; and (3) a model in which we flattened the sagittal crest to resemble the plate‐like crests of other mammals. During biting, an arc of stress extends from the bite point up through the vaulted forehead and along the sagittal crest. Our results suggest that pneumatization of the hyena's skull both enhances its ability to resist bending and, together with the vaulted forehead, plays a critical role in evenly dissipating stress away from the facial region. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 246–255.     

An Ice Age spotted hyena Crocuta crocuta spelaea (Goldfuss 1823) population,their excrements and prey from the Late Pleistocene hyena den of the Sloup Cave in the Moravian Karst,Czech Republic

A Late Pleistocene spotted hyena Crocuta crocuta spelaea (Goldfuss 1823) population from the cave bear den Sloup Cave, Moravia (Czech Republic) consists of mainly adult/senior and few cub/juvenile remains and coprolites, and 139 prey bones. Hyenas used the Nicová Cave branch that is connected to the entrance area mainly as a communal den site. Prey bone damage is most visible on the imported woolly rhinoceros remains. The partly excavated prey bone accumulation consists of a single woolly mammoth Mammuthus primigenius (Blumenbach 1799) tooth (2%), mainly Coelodonta antiquitatis (Blumenbach 1807) remains (16%), 4% Bos primigenius (Bojanus 1827) and 1% each of Megaloceros giganteus (Blumenbach 1799) and Rangifer tarandus (Linnaeus 1758). The other carnivores such as Panthera leo spelaea (Goldfuss 1810), Gulo gulo (Linnaeus 1758) and Canis lupus (Linnaeus 1758) subsp. are less represented (1–3%). Wolverines might have been imported also as prey remains, whereas wolves also possibly used this cave on a short-term basis, whereas steppe lions seem to have preyed upon cave bears deeper in the cave periodically, where even skeletons of P. leo spelaea were found in the Elisabeth Cave part.