2D:4D digit ratio is not a biomarker of developmental programming in baboons (Papio hamadryas species)

We hypothesized second‐to‐fourth hand digit ratio (2D:4D) is a biomarker of developmental programming in 3 baboon groups: intrauterine growth restriction (7 females, 8 males), exposure during fetal life to synthetic glucocorticoids (4 females, 5 males), and controls (66 females, 20 males). 2D:4D was similar between sexes and groups.     

Relationship between canine dimorphism and mandibular morphology in the hamadryas baboon and the Japanese monkey

To examine morphological interrelationships between canine size and mandibular corpus shape, inter-sex comparisons were made in the hamadryas baboon and the Japanese monkey, known to display extreme and moderate canine dimorphism, respectively. Results of adult comparisons showed that all mandibular dimensions were significantly larger in the males than in the females in both species. In the hamadryas baboon, the males also exhibited a higher ratio of anterior to posterior corpus height than the females. This sex difference in corpus shape was not significant in the Japanese monkey, indicating lack of involvement of canine dimorphism. Analysis of mandibular growth patterns in the hamadryas baboon demonstrated that significant sexual size difference did not occur before incisor eruption, and that the anteriorly high corpus of the adult male mandible was associated with a rapidly increasing symphyseal height after incisor eruption. It was also shown that the female canine started to erupt shortly after incisor eruption, while the forming male canine continued to stay near the mandibular base and developed further in size until eruption. The relative positions of the incisors kept shifting upwards even after eruption in the males, while they hardly changed in the females. It is therefore suggested that the prolonged development and size increase of the male canine is accompanied by further enlargement of the symphysis, resulting in the higher anterior corpus of the adult males compared to the adult females. The results thus indicate the importance of understanding the spatial relationships of the developing teeth in interpreting mandibular morphology.     

Developmental patterns of serum luteinizing hormone, gonadal and adrenal steroids in the sooty mangabey (Cercocebus atys)

Serum levels of luteinizing hormone (LH), testosterone, dehydroepiandrosterone sulfate (DHAS), androstenedione and cortisol were determined in multiple samples from 86 sooty mangabeys of varying ages (0-17 years). Testosterone, androstenedione, DHAS and cortisol were measured by radioimmunoassay; LH was determined by in vitro bioassay. Serum LH concentrations were elevated in neonates (less than 6 months) and in animals older than 72 months of age. The higher LH levels were associated with increased circulating concentrations of testosterone in males but not females. The pubertal rise in serum testosterone at approximately 55-60 months of age in males was coincident with rapid body growth. No pubertal growth spurt was observed in females. Serum levels of androstenedione and DHAS were highest during early postnatal life (less than 6 months) with androstenedione exceeding 600 ng/dl in males and 250 micrograms/dl in females, but declined rapidly in both sexes to a baseline of 150 ng/dl by 19 months of age. Serum androstenedione did not fluctuate significantly in adult animals. The pattern of age-related changes in serum DHAS paralleled those of serum androstenedione, whereas serum cortisol values did not change significantly with age. Developmental changes in serum LH, testosterone and body weight suggest that the sooty mangabey matures substantially later than the rhesus monkey. The pattern of serum gonadal and adrenal steroids during sexual maturation is similar to that seen in the baboon with no evidence of an adrenarche.     

Uptake and retention of sex steroids by the baboon pituitary gland--evidence of sexual dimorphism with respect to dihydrotestosterone

The localization and identification of the target cells for estradiol (E2) and dihydrotestosterone (DHT) were studied in the pituitary gland of male and female baboons (Papio cynocephalus) using autoradiography and autoradiography combined with immunocytochemistry. The largest number of cells which sequestered 3H-E2 were located in the pars distalis of both the males and females. Immunocytochemistry revealed that these target cells were predominantly gonadotrophs and mammotrophs, albeit a few somatotrophs and thyrotrophs were also labeled. A distinct sexual dimorphism was not observed with respect to the uptake and retention of the tritiated estrogen but was clearly evident in those animals given 3H-DHT. Significantly more cells in all three lobes of the male baboon, the partes distalis, intermedia and nervosa, concentrated the radiolabeled androgen as compared to that found in the females. Regardless of sex, however, the gonadotrophs were the major cell type in the pars distalis which was labeled. A small population of mammotrophs, somatotrophs and thyrotrophs also retained 3H-DHT. In both males and females, the pars nervosa was the portion of the hypophysis most sensitive to 3H-DHT. These findings indicate that all three lobes of the hypophysis of the male and female baboon contain target cells for E2 and DHT and that the propensity for DHT uptake is greater in males than in females.     

The mycoflora of the subhuman primates

Summary For documentation of the mycoflora of the baboon, 127 vaginal and 165 rectal swabs were taken from males and females in captivity. A total of 176 and 171 yeast isolates were obtained from the vagina and rectum respectively. Candida was found to be the yeast most frequently found in both of these sites.C. albicans formed 14.6 % of the rectal yeasts and 7.9 % of the vaginal yeasts.No significant differences were found between the rectal isolates from the males and those from the females in the baboons. Furthermore, there is a strong indication that the mycoflora of both the rectum and the vagina of the baboon is similar to that of human beings, from both a qualitative and a quantitative point of view.This study was supported by U.S.P.H.S. Grant 5-R01-HE-3834-07.     

Infanticide in hamadryas baboons

The results of 20-year study of infanticide cases in hamadryas baboon troop of the Sukhumi colony and 10-year observations in Gumista Natural Reserve are presented. The allopatric behaviour which may be the cause of infant death, is shown to be common for 4-7 year old males. In behaviour of older males directed to the infants the elements of aggression predominate. The majority of injuries and infanticide by males takes place in the situations associated with a dominant male change in the group or with the introduction of new females into the groups. In the groups where the social relationships are not fully organized, the appearance of infant leads to decrease of dominant male function and to appropriation of infant by a male and its traumatizing. As a result of infanticide the infants of young 4-7 year old females die most of all. The death of infants commonly occurs during the introduction of young males into the group. The probability of infanticide during the introduction of older males is lower.     

The social interactions of adult conspecifics with an adult XY gonadal dysgenetic chacma baboon (Papio ursinus)

Two separate behavioral studies on an XY gonadal dysgenetic chacma baboon were carried out. In the first experiment the focal subject was treated identically as the control females by her adult male test partners. In contrast to the controls in this experiment the dysgenetic animal reciprocated the agonistic behaviors directed by the males toward her. In the second study intact and castrated males as well as ovariectomized females served as controls for the dysgenetic subject in tests with ovariectomized adult females. The stimulus females presented more to both classes of males than either the subject females or the gonadal dysgenetic individual, suggesting that the focal subject was treated by other female conspecifics as a female.     

Immunohistochemical detection and biological activities of CYP17 (P450c17) in the indifferent gonad of the frog Rana rugosa

Sex steroids play a crucial role in the gonad differentiation in various species of vertebrates. However, little is known regarding the localization and biological activity of steroid-metabolizing enzymes during gonadal sex differentiation in amphibians. In the present study, we showed by real-time RT-PCR analysis that the expression of CYP17, one of the key steroidogenic enzymes, was higher in the indifferent gonad during sex differentiation in male than in female tadpoles of Rana rugosa but that there was no difference detected in the 3betaHSD mRNA level between the male and female gonads. We next examined the localization of CYP17, 3betaHSD and 17betaHSD in the indifferent and differentiating gonads by using three kinds of antibodies specific for CYP17, 3betaHSD and 17betaHSD, respectively. Positive signals for CYP17, 3betaHSD and 17betaHSD were observed in somatic cells of the indifferent gonad of males and in the interstitial cell of the testis. The enzymatic activity of CYP17 was also examined in the gonad during sex differentiation in this species. [(3)H]Progesterone (Prog) was converted to [(3)H]androstenedione (AE) in the indifferent gonad in males and females, but the rate of its conversion was higher in males than in females. Moreover, fluorescence in situ hybridization (FISH) analysis revealed that the CYP17 gene was located on the q arm of chromosome 9, indicating that CYP17 was autosomal in R. rugosa. Taken together, the results demonstrate that the CYP17 protein is synthesized in somatic cells of the indifferent gonad during gonadal sex differentiation in R. rugosa and that it is more active in converting Prog to AE in males than in females. The data suggest that CYP17 may be involved in testicular formation during sex differentiation in this species.     

Agonistic Interactions of Juvenile Savanna Baboons

19 juvenile members of known genealogies in two wild baboon groups were studied over a 16-month period to compare the ontogeny of agonistic experience and dominance relations for males and females. Juveniles of all age-sex classes were disproportionately likely to receive aggression from and submit to adult males per unit of time spent in proximity. This pattern intensified with increasing juvenile age. With age, juvenile females more often submitted to unrelated adult females from higher-ranking families, whereas this was not true for juvenile males. All juveniles received aggression from older group members more often during feeding than was expected by chance. High rates of agonistic interaction with unrelated adult females accounted for old juvenile females (3–5.5 years-old) interacting agonistically more frequently than male age peers and young juveniles of either sex (1–2.5 years-old). Adult females were also more aggressive toward females among young juveniles, suggesting that adult females target females among juveniles for aggression and resistance to rank reversal. Within juvenile age groups, males dominated all females and all younger males, irrespective of maternal dominance status. Dominance relations among female age-peers were generally isomorphic with relations among their mothers. No juvenile targeted any older male for rank reversal. Males targeted all older females, whereas females typically targeted only older females from families lower-ranking than their own. The strong sexual dimorphism in adult body size in baboons may explain why juvenile males' dominance relations with peers and adult females are not structured along lines of family membership as is true for the less dimorphic macaques. Acquisition of higher agonistic status probably allows juveniles of both sexes to increase their success in within-group feeding competition during late stages of juvenility, which, in turn, could affect important life-history traits such as age at menarche and adult body size.     

Alternative routes to the leader male role in a multi-level society: follower vs. solitary male strategies and outcomes in hamadryas baboons

The nested one-male units (OMUs) of the hamadryas baboon are part of a complex social system in which "leader" males achieve near exclusive mating access by forcibly herding females into permanent consortships. Within this multi-level social system (troops, bands, clans and OMUs) are two types of prereproductive males--the follower and solitary male--whose different trajectories converge on the leader role. Here we compare OMU formation strategies of followers, who associate with a particular OMU and may have social access to females, with those of solitary males, who move freely within the band and do not associate regularly with OMUs. Data were derived from 42 OMU formations (16 by followers and 26 by solitary males) occurring over 8 years in a hamadryas baboon band at the Filoha site in Ethiopia. "Initial units" (IUs) with sexually immature females (IU strategy) were formed by 44% of followers and 46% of solitary males. The remaining followers took over mature females when their leader was deposed (challenge strategy) or disappeared (opportunistic strategy), or via a seemingly peaceful transfer (inheritance strategy). Solitary males took over mature females from other clans and bands, but mainly from old, injured or vanished leaders within their clan (via both the challenge and opportunistic strategies). Former followers of an OMU were more successful at taking over females from those OMUs than any other category of male. Despite this advantage enjoyed by ex-follower leaders, ex-solitary leaders were equally capable of increasing their OMU size at a comparable rate in their first 2 years as a leader. These results demonstrate the potential for males to employ both multiple roles (follower vs. solitary male) and multiple routes (IU, inheritance, challenge, opportunistic) to acquire females and become a leader male in a mating system characterized by female defense polygyny in a competitive arena.     

Social Structure of a Semi-Free Ranging Group of Mandrills (Mandrillus sphinx): A Social Network Analysis

The difficulty involved in following mandrills in the wild means that very little is known about social structure in this species. Most studies initially considered mandrill groups to be an aggregation of one-male/multifemale units, with males occupying central positions in a structure similar to those observed in the majority of baboon species. However, a recent study hypothesized that mandrills form stable groups with only two or three permanent males, and that females occupy more central positions than males within these groups. We used social network analysis methods to examine how a semi-free ranging group of 19 mandrills is structured. We recorded all dyads of individuals that were in contact as a measure of association. The betweenness and the eigenvector centrality for each individual were calculated and correlated to kinship, age and dominance. Finally, we performed a resilience analysis by simulating the removal of individuals displaying the highest betweenness and eigenvector centrality values. We found that related dyads were more frequently associated than unrelated dyads. Moreover, our results showed that the cumulative distribution of individual betweenness and eigenvector centrality followed a power function, which is characteristic of scale-free networks. This property showed that some group members, mostly females, occupied a highly central position. Finally, the resilience analysis showed that the removal of the two most central females split the network into small subgroups and increased the network diameter. Critically, this study confirms that females appear to occupy more central positions than males in mandrill groups. Consequently, these females appear to be crucial for group cohesion and probably play a pivotal role in this species.     

Transmission dynamics of simian T-lymphotropic virus type 1 (STLV1) in a baboon breeding colony: predominance of female-to-female transmission

We investigated the prevalence, distribution, and transmission of simian T-lymphotropic virus type 1 (STLV1) in a baboon breeding colony over a 4-y period. We used polymerase chain reaction amplification of the proviral tax gene to assess the infection status of 272 animals housed in 4 separate corrals. Sequencing the proviral envelope gene from individual baboons detected several molecular subtypes (genotypes) of STLV1. At the start of the study, 31% (54 of 176) of all baboons were infected; the majority of infections (91%) were in mature females, with only 3 of 12 mature males and 2 of 48 infants and juveniles being infected. Over the next 4 years, 41 new infections were diagnosed. Of these, 83% occurred in sexually mature female baboons (at least 3 y of age), 17% in infants and juveniles (younger than 3 y), and 0% in mature males. The 7 infections in juveniles were probably derived from mother-to-infant transmission because mother-infant pairs consistently were infected with the same viral genotype. Of the 34 new infections in sexually mature female baboons, the genotyping data showed that 25 (73%) originated from other infected females as opposed to males. Male-to-female sexual transmission may have accounted for the remaining 9 new infections. There was no evidence of female-to-male sexual transmission. The high percentage of female-to-female transmission of STLV1 in our baboons was unexpected; we speculate that transmission may have occurred due to blood contamination from biting during aggressive behavior between females in establishing hierarchical dominance.     

The spread of exclusive mating in a chacma baboon population

Mating has progressively tended toward pair bonding in a chacma baboon (Papio cynocephalus ursinus) population during eight years of study. Both males and females have been mating with a smaller and smaller percentage of the potential mates available to them. Troop subdivision during the dry winter in the absence of predation was the original cause of mating limitation, but most members of winter subtroops only rarely mated with adults who had not belonged to the same winter subtroop during the summers as well. Following reintroduction of potential predation, both subtroop size and frequency decreased, but mating did not become less exclusive.     

Ecologically differentiated patterns of aggressive and sexual behavior in two troops of Ugandan baboons, Papio anubis

Two baboon troops from different ecological conditions — a thicket savanna in Queen Elizabeth Park, and a forest edge in the Budongo Forest — were studied during a 15 month period. Two different social structures were found and various levels of aggressive activity were observed, both among males and among females and juveniles. The patterns of female sexual behavior differed widely between the two troops. These patterns are examined, and the genetic and environmental factors involved in the determination of aggressive and sexual behavior among baboons are discussed.     

Movement patterns of yellow baboons (Papio cynocephalus): Sex differences in juvenile development toward adult patterns

Age-sex differences in the sociospatial positioning of progressing baboon troops have been postulated as an important, protective aspect of baboon adaptation to a terrestrial existence. The protection theory is an ultimate hypothesis which can be disproven by showing that the postulated age-sex positioning fails to occur. Alternatively, confidence in the protection theory can be increased if the postulated positioning persists across several troops despite significant opportunities for variation, and if progression order is shown to be linked to biological phenomena such as sex differences in physical maturation. Data from 73 individually identified, free-ranging juveniles of both sexes were compared with previous findings. Small juveniles of several troops were more centrally located than large juveniles. Large juveniles males were more toward the front than were large juvenile females. As male walking infants and juveniles aged, a change in positioning (i.e., location) occurred: males were located increasingly toward the front of progressions. Comparable data from females suggest that the adult female pattern had begun to form among large juveniles. Data are consistent with an ultimate protection theory.     

Sex differences in adrenal function in the lizard Cnemidophorus sexlineatus: I. Seasonal variation in the field.

In order to document sex differences in adrenal function and how this relates to gonadal function during the period of seasonal activity, blood samples from male and female six-lined racerunners, Cnemidophorus sexlineatus, were taken immediately after capture in the field for determination of plasma corticosterone and gonadal steroid concentrations. Plasma testosterone and dihydrotestosterone levels for males, and 17 beta-estradiol and progesterone levels for females, were measured. Trends in the concentration of plasma corticosterone differed significantly between males and females. In males the highest concentrations of corticosterone were measured in late spring and the lowest concentrations were measured in late summer. Whereas half of the variation in corticosterone levels among males could be explained as seasonal change, less than 1% of the variation among females could be explained as seasonal change. In males plasma corticosterone and androgens exhibited similar seasonal decreases. Corticosterone levels for females were not correlated with progesterone or 17 beta-estradiol levels. Sex differences in seasonal variation in plasma corticosterone concentrations suggest that corticosterone may be involved in the different reproductive strategies and energy requirements of males and females during the seasonal period of activity.     

Pregnancy and early reproductive failure in the baboon

We documented normal pregnancy and the rate of pregnancy failure in female baboons by measuring chorionic gonadotropin (bCG) and progesterone (P) levels in 162 mated cycles of 70 baboon females on days 10, 12, and 14 postovulation. Females were mated with males during turgescene. The presence of pregnancy was defined by bCG levels >20 μg/ml by day 14 postovulation and/or documentation of a gestational sac using ultrasonography. Of the 162 cycles, 75 were fertile. Of these animals, 33 were used in other studies and thus were not included in these analyses. The analyses are based on 43 pregnancies from 91 cycles that were untreated throughout their gestations. Twenty-six of these pregnancies had abnormal bCG and/or progesterone levels in early pregnancy. All of those pregnancies with abnormal endocrine parameters terminated with spontaneous abortion (60%). Certain abnormal bCG patterns were repeatedly observed in some animals and were correlated with repeated spontaneous abortions. Of 17 pregnancies with normal bCG and P patterns, 15 (88%) continued to term with a normal fetal outcome. In this study, a pregnancy rate per mated cycle of 47% was observed, yet 60% of untreated pregnancies abortyed spontaneously. Overall 16% of the mated cycles had continuing pregnancies with normal outcome. These studies demonstrate that a high rate of early abortions occurs in the baboon and that a single bCG determination is insufficient to define the presence of a “normal” pregnancy which might be expected to carry to term with a normal outcome.     

Characteristics of hamadryas-like male baboons living in anubis baboon troops in the Awash hybrid zone, Ethiopia.

In the twenty-two years since the Awash baboon hybrid zone was first described, about 25-30 hamadryas or hamadryas-like hybrid males have taken up residence in anubis baboon groups. Most enter as mature adults, though some may immigrate as juvenile followers. Long-term tracking of known immigrants indicates that they may reside for four years or more in their adopted troop, during which time they establish a series of comparatively short-term harems, and probably sire hybrid offspring. "Abductions" of anubis females to hamadryas troops, as postulated by early observers, were not seen, though their occurrence cannot be ruled out. Younger, more recent immigrants tend to be "purer" hamadryas in phenotype, perhaps reflecting a more distant origin, or a change in the composition of neighboring hamadryas populations. Coexisting hamadryas and anubis show no signs of reproductive isolation by behavioral barriers, and evidently belong to a single "recognition species."     

Male rank and reproductive activity in Savanna baboons

Access to sexually receptive baboon females has been linked to male dominance rank. An intensive 19-month field study of mate choice and mate competition among savanna baboons was undertaken in order to elucidate those factors influencing mating success. During this study, male agonistic rank was not correlated with male mating success among adult males. However, the inclusion of adolescent males into the analysis yielded significant correlations between rank and mating success. Examination of prior fieldwork revealed that no baboon field study has conclusively demonstrated a significant correlation between male rank and reproduction among adult males. Most studies reporting a correlation between male rank and reproduction have included subadult males in the analysis. It is concluded that male rank is an unreliable predictor of male reproductive activity among adult male baboons. A low agonistic rank need not reduce male mating success because adult male baboons utilize a variety of reproductive tactics in gaining access to consort females.