Population Of Baboons Research Articles

Parallel effects of genetic variation in ACE activity in baboons and humans

Like humans, savannah baboons (Papio sp.) show heritable interindividual variation in complex physiological phenotypes. One prominent example of such variation involves production of the homeostatic regulator protein angiotensin converting enzyme (ACE), which shows heritable variation in both baboons and humans. In humans, this phenotypic variation is associated with an Alu insertion-deletion polymorphism in the ACE gene, which explains approximately half of the variation in serum ACE activity. We identified a similar Alu insertion-deletion polymorphism in the baboon ACE homologue and measured its frequency in a wild population and a captive population of baboons. We also analyzed the contribution of ACE genotype at this indel to variation in serum ACE activity in the captive population. When conditioned on weight, a known factor affecting ACE activity in humans, age and ACE genotype both accounted for variance in ACE activity; in particular, we identified a significant nonadditive interaction between age and genotype. A model incorporating this interaction effect explained 21.6% of the variation in residual serum ACE activity. Individuals homozygous for the deletion mutation exhibited significantly higher levels of ACE activity than insertion-deletion heterozygotes at younger ages (10-14 years), but showed a trend towards lower levels of ACE activity compared with heterozygotes at older ages (> or =15 years). These results demonstrate an interesting parallel between the genetic architecture underlying ACE variation in humans and baboons, suggesting that further attention should be paid in humans to the relationship between ACE genetic variation and aging.

Population structure and habitat use of baboons (<i>Papio hamadryas ursinus</i>) in the Blyde Canyon Nature Reserve

Baboons are highly intelligent and ecologically flexible animals with attributes that allow them to exploit diverse habitats. As a result of their dietary flexibility they often exploit human habitats, causing damage to crops and forest plantations as well as to human dwellings. In the South African context this has led to baboons being regarded as problem animals and attempted extirpation is the most common approach to the damage they cause. This perception of and attitude toward baboons gives many conservationists cause for concern since all southern African cercopithecine primates are CITES listed and it has not been proven that this strategy is the best long-term solution. As part of a research programme focusing on the damage done by chacma baboons in pine plantations along the Drakensberg escarpment in Mpumalanga, a single troop in the Blyde Canyon Nature Reserve was studied to describe their patterns of habitat use. Vegetation and habitat surveys were conducted within the home range of the troop. The troop was habituated and each member’s activity, location and food items utilised were recorded over a 12 month period. The results of this study indicate that baboons utilised plant communities based on food production and availability rather than size in hectares. The results also indicate that the group size, foraging and food search strategies of this troop resembles that of the Drakensberg troops previously studied. The study troop employs two different forage modes of engagement depending on where they choose to forage while they avoid utilising an easily accessible pine plantation. Due to the troop’s long inter-birth intervals it is likely that the current forestry practice of extirpation may have a negative influence on baboon population viability in these areas.

Genetic correlations between mandibular molar cusp areas in baboons

Primate evolutionary studies rely significantly on dental variation given the large role that teeth play in how an organism interacts with its environment (animal and plant) and conspecifics. Variation in cusp size has been shown to vary among primate taxa, although most studies to date focused on extant and extinct hominoids. Here we test the assumed hypothesis that a significant proportion of this variation in baboons is due to the additive effects of genes. We perform quantitative genetic analyses on variation in two-dimensional (2-D) mandibular molar cusp size in a captive pedigreed breeding population of baboons (Papio hamadryas) from the Southwest National Primate Research Center. These analyses show that variation in cusp size is heritable and sexually dimorphic. Additionally, we tested for genetic correlations between cusps on the same crown, between morphological homologues along the tooth row, and between cusp area and crown buccolingual width. We find that four of the six cusp pairs on the first molar have a genetic correlation of one, save for the metaconid-hypoconid and entoconid-hypoconid, which are not statistically different from zero. The second and third molars have lower genetic correlations, although the metaconid-hypoconid correlation is similarly estimated at zero and the entoconid-protoconid correlation is estimated to be one. This cross pattern of genetic and no genetic correlation does not immediately accord with the known pattern of development and/or calcification. We propose two explanative hypotheses.

A multivariate comparison of dental variation in wild and captive populations of baboons ( Papio hamadryas)

Phenotypic variation is critical to many aspects of biological research. Use of a captive population to address questions concerning the genetics and evolution of dental variation raises the question of how the pattern of phenotypic variation under study compares with that in a wild population of the same species. Differences in the pattern of variation within wild and captive populations may indicate different genetic and non-genetic factors, and also may have implications for how well the captive group can serve as a model for its wild type relatives. We compared dental size measures from two Papio hamadryas populations, one captive and one wild. Lengths and widths of maxillary and mandibular second molars (M2s) were collected from 630 baboons from a captive pedigreed breeding colony housed at the Southwest National Primate Research Center in San Antonio, Texas, and 125 baboons from a wild population culled from a sisal plantation in Kibweze, Kenya. Although the two populations consistently differed with respect to lengths and widths of the M2s, principal components analyses show that the basic pattern to variation in these molar crown traits is remarkably similar in both populations; and linear functions based on these measures cannot reliably discriminate between the two groups. This similarity in the pattern of variation among these dental crown measures in these two groups suggests that analyses to dissect their genetic architecture in captive populations is likely to be highly relevant to dental variation in wild baboons as well.

Mechanisms of sexual selection: Sexual swellings and estrogen concentrations as fertility indicators and cues for male consort decisions in wild baboons

Male mate-guarding episodes (‘consortships’), are taxonomically widespread, yet costly to individual males. Consequently, males should bias consortships toward females with whom the probability of conception is high. We combined data on consortships with visual scoring of sexual swellings and assays of fecal estrogen concentrations (fE) in a wild population of baboons ( Papio cynocephalus) to test the hypotheses that sexual swellings are reliable indicators of (1) within-cycle timing of ovulation, (2) differences in conception probability among females that differ in maturational stage, and (3) conceptive versus non-conceptive cycles of parous females. We also evaluated whether adult males might rely on swellings or other estrogen-dependent signals (e.g., fE) for mate-guarding decisions. We found that sexual swellings reflected conception probability within and among cycles. Adult males limited their consortships to the turgescent phase of cycles, and consorted more with adult females than with newly cycling adolescents. The highest ranking (alpha) males discriminated more than did males of other ranks; they (1) limited their consortships to the 5-day peri-ovulatory period, (2) consorted more with adult than with adolescent females, and (3) consorted more with adult females on conceptive cycles than on non-conceptive cycles, all to a greater extent than did males of other ranks. Male mate choice based on sexual swellings and other estrogenic cues of fertility may result in sexual selection on these female traits and enhance dominance-based reproductive skew in males. Alpha males are the least constrained in their mating behavior and can best take advantage of these cues to mate selectively.

Evolution of genetically correlated traits: Tooth size and body size in baboons

Within a population, only phenotypic variation that is influenced by genes will respond to selection. Genes with pleiotropic effects are known to influence numerous traits, complicating our understanding of their evolution through time. Here we use quantitative genetic analyses to identify and estimate the shared genetic effects between molar size and trunk length in a pedigreed, breeding population of baboons housed at the Southwest National Primate Research Center. While crown area has a genetic correlation with trunk length, specific linear measurements yield different results. We find that variation in molar buccolingual width and trunk length is influenced by overlapping additive genetic effects. In contrast, mesiodistal molar length appears to be genetically independent of body size. This is the first study to demonstrate a significant genetic correlation between tooth size and body size in primates. The evolutionary implications are discussed.

Interactions in male baboons: the importance of both males’ testosterone

To date, research on testosterone and behavior has focused on individuals, even when studying social behaviors that necessarily involve multiple participants. Here, we explore male responses to other males of different dominance ranks and testosterone levels in a population of wild baboons. In chacma baboons (Papio hamadryas ursinus) of the Okavango Delta, a male's testosterone is related to his rank trajectory and, therefore, the threat he poses to other males. To examine the effects of testosterone and rank on male-male interactions, we used playback experiments to measure how a target male responded to the simulated approach of another male, scoring responses by whether or not the subject moved away from the speaker in the first minute. High testosterone subjects did not move away from the speaker more often than low testosterone subjects, but high testosterone callers elicited a move more often than low testosterone callers. When the combined testosterone of the subject and caller was high, moves were most common. The rank relationship between subject and caller did not predict moves, but the effect of combined testosterone on moving was most pronounced in adjacently ranked males. Adjacently ranked, high testosterone males are the most likely to be competing for each others' rank, and our experiments on these dyads elicited the most moves. Both behavioral and experimental observations indicate that testosterone may be more important than the rank relationship in predicting the outcome of male-male interactions. Furthermore, combined information on the testosterone of both males was the best predictor of results, highlighting the utility of dyadic analyses when relating testosterone to behavior.

Female testosterone, dominance rank, and aggression in an Ethiopian population of hybrid baboons

Studies on the relationship between female testosterone (T) measures and behavior, particularly in free-ranging primate populations, remain scant. In this study we used fecal steroid analysis to examine the effects of seasonal, reproductive, and social factors on female T in a group of free-ranging hybrid baboons (Papio sp.) in the Awash National Park of Ethiopia. We collected behavioral and hormonal data from 25 adult females across an 11-month period. Solid phase extraction and radioimmunoassay (RIA) techniques were used to quantify T in 776 fecal samples collected weekly from each female. The results indicate that 1) the females had elevated T during pregnancy and during the wet season relative to other periods, 2) female dominance rank was positively related to T measures, and 3) female T and aggression were positively related within subjects but not across subjects. Higher T concentrations during pregnancy are consistent with other published profiles of pregnancy in primates. In combination with data on foraging, wet season increases in T may indicate contest competition for females. The rank-T relationship may be mediated by supplants or aggression. Finally, we discuss the different interpretations of the hormone-behavior relationship based on within- and across-subject analyses.

Coming of age: steroid hormones of wild immature baboons (Papio cynocephalus)

Large gaps exist in our knowledge about common patterns and variability in the endocrinology of immature nonhuman primates, and even normal hormonal profiles during that life stage are lacking for wild populations. In the present study we present steroid profiles for a wild population of baboons (Papio cynocephalus) from infancy through reproductive maturation, obtained by noninvasive fecal analyses. Fecal concentrations of glucocorticoid (fGC) and testosterone (fT) metabolites for males, and of fGC, estrogen (fE), and progestin (fP) metabolites for females were measured by radioimmunoassay (RIA). In males, infancy was characterized by high and declining levels of fGC and fT, whereas steroid concentrations were low during the juvenile years. During the months immediately prior to testicular enlargement, fT (but not fGC) concentration tended to increase. Males that matured early consistently had higher fT and fGC concentrations than those that matured late, but not significantly so at any age. Individual differences in fT concentrations were stable across ages, and average individual fT and fGC concentrations were positively correlated. For females, high and declining levels of fE characterized infancy, and values increased again after 3.5 years of age, as some females reached menarche by that age. Both fP and fGC were relatively low and constant throughout infancy and the juvenile period. During the months immediately prior to menarche, fGC concentration significantly decreased, while no changes were observed for fE levels. fP exhibited a complicated pattern of decrease that was subsequently followed by a more modest and nonsignificant increase as menarche approached. Early- (EM) and late-maturing (LM) females differed only in fP concentration; the higher fP concentrations in EM females reached significance at 4-4.5 years of age. Maternal rank at offspring conception did not predict concentrations of any hormone for either sex. Our results demonstrate the presence of individual endocrine variability, which could have important consequences for the timing of sexual maturation and subsequently for individual reproductive success. Further evaluation of the factors that affect hormone concentrations during the juvenile and adolescent periods should lead to a better understanding of mechanisms of life-history variability.

Growth rates in a wild primate population: ecological influences and maternal effects

Growth rate is a life-history trait often linked to various fitness components, including survival, age of first reproduction, and fecundity. Here we present an analysis of growth-rate variability in a wild population of savannah baboons (Papio cynocephalus). We found that relative juvenile size was a stable individual trait during the juvenile period: individuals generally remained consistently large-for-age or small-for-age throughout development. Resource availability, which varied greatly in the study population (between completely wild-foraging and partially food-enhanced social groups), had major effects on growth. Sexual maturity was accelerated for animals in the food-enhanced foraging condition, and the extent and ontogeny of sexual dimorphism differed with resource availability. Maternal characteristics also had significant effects on growth. Under both foraging conditions, females of high dominance rank and multiparous females had relatively large-for-age juveniles. Large relative juvenile size predicted earlier age of sexual maturation for both males and females in the wild-feeding condition. This confirmed that maternal effects were pervasive and contributed to differences among individuals in fitness components.

Adenomyosis in the baboon is associated with primary infertility

To determine whether an association exists between the histopathologic diagnosis of adenomyosis and infertility in a population of captive baboons. Case-control study. Southwest National Primate Research Center. Necropsy records of 37 baboons diagnosed with adenomyosis uteri and 38 baboons with normal uterine histology. None. Chi2 analysis of the association between adenomyosis, primary infertility, and the presence of coexisting endometriosis. Endometriosis was associated with the presence of adenomyosis (OR = 31.5, 95% CI 4.2-1,348). There was a trend toward an association of endometriosis with the presence of lifelong infertility, but this correlation did not quite achieve statistical significance (OR = 3.6, 95% CI 0.9-15.8). Adenomyosis was associated with the presence of lifelong infertility (OR = 20.6, 95% CI 2.7-897). This association was maintained when cases of coexisting endometriosis (n = 17) were excluded (OR = 20.1, 95% CI 2.1-921). Adenomyosis is strongly associated with lifelong primary infertility in the baboon, even in the absence of coexisting endometriosis.

Trade-offs in skillacquisition and time allocation among juvenile chacma baboons.

We hypothesize that juvenile baboons are less efficient foragers than adult baboons owing to their small size, lower level of knowledge and skill, and/or lesser ability to maintain access to resources. We predict that as resources are more difficult to extract, juvenile baboons will demonstrate lower efficiency than adults will because of their lower levels of experience. In addition, we hypothesize that juvenile baboons will be more likely to allocate foraging time to easier-to-extract resources owing to their greater efficiency in acquiring those resources.We use feeding efficiency and time allocation data collected on a wild, free-ranging, non-provisioned population of chacma baboons (Papio hamadryas ursinus) in the Moremi Wildlife Reserve, Okavango Delta, Botswana to test these hypotheses. The major findings of this study are:1. Juvenile baboons are significantly less efficient foragers than adult baboons primarily for difficult-to-extract resources.We propose that this age-dependent variation in efficiency is due to differences in memory and other cognitive functions related to locating food resources, as is indicated by the greater amount of time juvenile baboons spend searching for food. There is no evidence that smaller body size or competitive disruption influences the differences in return rates found between adult and juvenile baboons in this study.2. An individual baboon's feeding efficiency for a given resource can be used to predict the duration of its foraging bouts for that resource.These results contribute both to our understanding of the ontogeny of behavioral development in nonhuman primates, especially regarding foraging ability, and to current debate within the field of human behavioral ecology regarding the evolution of the juvenile period in primates and humans.

Social bonds of female baboons enhance infant survival.

Among nonhuman primates, females often form strong bonds with kin and other group members. These relationships are thought to have adaptive value for females, but direct effects of sociality on fitness have never been demonstrated. We present 16 years of behavioral data from a well-studied population of wild baboons, which demonstrate that sociality of adult females is positively associated with infant survival, an important component of variation in female lifetime fitness. The effects of sociality on infant survival are independent of the effects of dominance rank, group membership, and environmental conditions. Our results are consistent with the evidence that social support has beneficial effects on human health and well-being across the life span. For humans and other primates, sociality has adaptive value.

Extra-unit paternity of hamadryas baboons (Papio hamadryas) in Saudi Arabia

Sex-biased dispersal and female choice for non-related mates are mechanisms of inbreeding avoidance in animals. In species with limited dispersal of both sexes, the latter mechanism is of greater importance. We investigated a wild population of hamadryas baboons (Papio hamadryas) living in Saudi Arabia and surviving on human garbage. Paternity relationships between adult males and juveniles of three social units were analyzed using 12 loci of tetra-repeat microsatellite DNA. Of 16 juveniles and infants (0-3 years old), 13 were not sired by the leader male of each unit. This extra-unit paternity suggests the possibility that females conducted extra-unit copulations (EUCs) leading to extra-unit fertilizations (EUFs). We discuss this and other possible explanations for the apparent extra-unit paternity, as well as the plausibility of EUFs as a function of inbreeding avoidance in the hamadryas baboon. This is the first molecular study to investigate kin relationships within wild units of hamadryas baboons.

True paternal care in a multi-male primate society.

Although male parental care is rare among mammals, adult males of many cercopithecine primate species provide care for infants and juveniles. This care is often in the form of grooming, carrying, support in agonistic interactions, and protection against infanticide. For these behaviours to be interpreted as true parental care, males must selectively direct care towards their own offspring and this care must result in fitness benefits. With the exception of males defending probable offspring from infanticide, male primates living in multi-male, multi-female social groups have not been shown to selectively direct care towards their own offspring. We determined paternity for 75 juveniles in a population of wild savannah baboons (Papio cynocephalus) and collected data on interventions in agonistic disputes by adult males on behalf of juveniles as a form of male care. Here we show that adult males differentiate their offspring from unrelated juveniles and selectively support their offspring in agonistic disputes. As support in agonistic disputes is likely to contribute to rank acquisition and protect juveniles from injury and stress, this can be considered true parental care.

Science on the fly.

As an ecologist, demographer, evolutionary biologist, and experimental geneticist all rolled into one, Marc Tatar cuts a wide swath in his studies linking reproduction, mortality, and longevity. He began his scientific training as a butterfly-chasing field biologist in the 1980s and, for a time, taught science in high school. Since then he has metamorphosed into a leader in investigating how insulin-like hormones influence aging in fruit flies. Using the tools of demography, he has studied senescence in fruit flies, seed beetles, and wild populations of grasshoppers, lions, and baboons. For fun, Tatar used to race bicycles and today swims 10 miles a week.

Morbidity and immune response to natural schistosomiasis in baboons ( Papio anubis )

The morbidity and immunological response to naturally acquired Schistosoma mansoni infection in a population of wild baboons ( n=28) was investigated. Serum obtained from the baboons was assayed for adult worm (SWAP) and schistosome egg (SEA)-specific immunoglobulin (Ig)G and IgM antibodies. The animals were euthanised, perfused to recover adult schistosome worms and schistosome-related pathology was assessed. Nineteen animals (68%) had high serum levels of SWAP-specific IgG antibodies and 15 (54%) had high levels of SEA-specific IgG antibodies. Nine animals (32%) had high levels of SWAP-specific IgM antibodies and six (21%) had high levels of SEA-specific IgM antibodies. Mild schistosome-related pathology was noted in 18 animals (64%). However, adult schistosome worms were recovered from only three animals (10%). The results indicate a high exposure to schistosomiasis for free-ranging baboons inhabiting an endemic area, as evidenced by the high prevalence of parasite-specific humoral antibody response. However, this high exposure is associated with low worm recovery and mild pathology. In addition, parasite-specific IgM antibodies provided a good indicator of an active schistosome infection.

Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus

In many animals, variance in male mating success is strongly correlated with male dominance rank or some other measure of fighting ability. Studies in primates, however, have varied greatly in whether they detect a relationship between male dominance rank and mating success. This variability has led to debate about the nature of the relation between rank and mating success in male primates. We contribute to the resolution of this debate by presenting an analysis of the relationship between dominance rank and male mating success over 32 group-years in a population of wild savannah baboons. When data were pooled over the entire period, higher-ranking males had greater access to fertile females. However, when we examined successive 6-month blocks, we found variance in the extent to which rank predicted mating success. In some periods, the dominance hierarchy functioned as a queue in which males waited for mating opportunities, so that rank predicted mating success. In other periods, the queuing system broke down, and rank failed to predict mating success when many adult males were in the group, when males in the group differed greatly in age, and when the highest-ranking male maintained his rank for only short periods. The variance within this single population is similar to the variance observed between populations of baboons and between species of primates. Our long-term results provide strong support for the proposition that this variance is not an artefact of methodological differences between short-term studies, but is due to true variance in the extent to which high-ranking males are able to monopolize access to females. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.

Changes in unit structures and infanticide observed in Arsi geladas.

In 1989 a new gelada baboon ( Theropithecus gelada) population was found in Arsi, on the opposite side of the Rift Valley to that of the known gelada populations of Semien and Showa. Previous comparisons of units of the band at Gado Goro, Arsi, in the same season in consecutive years, indicated that unit structure is less stable among Arsi geladas as compared to the Semien population. Gelada units of the band at Gado-Goro were studied for 7 months in order to investigate the processes of social changes. Changes in unit structure were observed. Provisioning was carried out for 1.5 months at the beginning of the 7-month study period, in order to capture and obtain blood samples from the geladas. Following this, changes in male leadership of some units were observed, presumably as a consequence of the capture. However, natural changes also occurred. One change in unit structure occurred after a female gave birth, and changes in another unit occurred after the disappearance of the leader male. These changes involved female desertion of a unit, her subsequent transfer to a male unit, and culminated in the formation of a unit consisting of one female and one male. One successful and one attempted case of unification of units, and one case of change of a unit leader male are reported. These changes occurred among eight resident units in a period of 7 months (196 female months). Though the types of social changes were not much different from previous observations in Semien National Park, their frequencies seemed to be much higher. The characteristics of Arsi gelada social changes are proposed to be related to the small size of the units. We also describe a new confirmed case and one suspected case of infanticide, as well as one case of abortion at the time of male leader change.

Day length, latitude and behavioural (in)flexibility in baboons (Papio cynocephalus ursinus)

Annual cycles in day length are an important consideration in any analysis of seasonal behaviour patterns, since they determine the period within which obligate diurnal or nocturnal animals must conduct all of their essential activities. As a consequence, seasonal variation in day length may represent an ecological constraint on behaviour, since short winter days restrict the length of the time available for foraging in diurnal species (with long summer days, and thus short nights, a potential constraint for nocturnal species). This paper examines monthly variation in activity patterns over a 4-year study of chacma baboons (Papio cynocephalus ursinus) at De Hoop Nature Reserve, South Africa. Time spent feeding, moving, grooming and resting are all significant positive functions of day length, even before chance events such as disease epidemics and climatically mediated home range shifts have been accounted for. These results provide strong support for the idea that day length acts as an ecological constraint by limiting the number of daylight hours and thus restricting the active period at certain times of year. Day length variation also has important implications across populations. Interpopulation variation in resting time, and non-foraging activity in general, is a positive function of latitude, with long summer days at temperate latitudes apparently producing an excess of time that cannot profitably be devoted to additional foraging or social activity. However, it is the short winter days that are probably of greatest importance, since diurnal animals must still fulfil their foraging requirements despite the restricted number of daylight hours and elevated thermoregulatory requirements at this time of year. Ultimately this serves to restrict the maximum ecologically tolerable group sizes of baboon populations with increasing distance from the equator. Seasonal variation in day length is thus an important ecological constraint on animal behaviour that has important implications both within and between populations, and future studies at non-equatorial latitudes must clearly be mindful of its importance.