Mitochondrial phylogeny and systematics of baboons (Papio)

Baboons (Papio, s.s.) comprise a series of parapatric allotaxa (subspecies or closely related species) widely distributed in sub-Saharan Africa. Despite extensive studies of their ecology, morphology, and behavior, disagreement about their phylogenetic relationships continues, as expressed in the current coexistence of at least three major, competing taxonomic treatments. To help resolve this situation, we sequenced approximately 900 bases of mitochondrial DNA of 40 individuals from five of the widely recognized "major" allotaxa. Total sequence diversity (>5%) is high compared to most primate species. Major mitochondrial clades correspond to recognized allotaxa, with the important exception that haplotypes from yellow and olive baboons form a single, monophyletic clade within which the two allotaxa do not comprise mutually exclusive clusters. The major clades fall unambiguously into the pattern: (chacma (Guinea (hamadryas (yellow + olive)))). This phylogeny does not support taxonomies that oppose hamadryas to all other baboons ("desert" vs. "savanna"), but is compatible with the view that all definable allotaxa should be recognized as coordinates, either as "phylogenetic" species or "biological" subspecies. The close relationship and unsegregated distribution of haplotypes from Kenyan and Tanzanian yellow and olive baboons are unexplained, but may reflect introgression across the documented hybrid zone. The overall phylogeny, when combined with paleontological data, suggests a southern African origin for extant Papio baboons, with all extant lineages sharing a common mitochondrial ancestor at approximately 1.8 Ma.     

Progressions of adult male chacma baboons (Papio ursinus) in the moremi wildlife reserve

It has been suggested that the sociospatial organization of baboon progressions has a protective function in which the most physically powerful troop members, the adult males, play a key role. This theory implies regularities in adult male progression order for different species of savannah baboons with similar social systems. Quantitative progression data are available from two such similar baboon species, olive and yellow, but not from the third, chacma. The order of movement of 15 adult male chacma baboons was determined from 40 progressions observed at the Moremi Wildlife Reserve, Botswana. The chacma males were most often found in the front sixth of progressions, next most often in the second sixth, and about equally often from there to the rear. As expected from the protection theory, this frontal positioning is consistent with available quantitative data from other species of savannah baboons.     

Capture-release field observations of free-ranging chacma baboons,Papio ursinus,focusing on the behaviour of the sub-adult male segment of the baboon social unit

An adult female and three age-graded male chacma baboons,Papio ursinus, were captured and then artificially introduced into a recipient troop of free-ranging baboons of the same species. Two of the transplanted individuals, the youngest juvenile male and the sub-adult male, were accepted into the troop while the oldest juvenile male and the adult female were aggressively chased off by the sub-adult and adult males of the troop, and they subsequently returned more than 10 km to their home troop. Acceptance of the first two individuals was dependent on the gradual reduction of aggressive behaviour of the sub-adult males. This suggested that successful troop transfers in the wild, occurring more frequently than traditionally believed, may be at least partially contingent on the behaviour of the sub-adult male segment of the baboon social unit. Supported by a Graduate Research Grant from the University of Cape Town.     

Patterns of Inheritance of Mating Signals in Sailfin and Shortfin Mollies (Poeciliidae: Poecilia: Mollienesia)

Divergence in mating signals is a primary factor leading to reproductive isolation, and thus, speciation. However, the genetic changes underlying such divergence are poorly understood, especially in vertebrates. We used two species of poeciliid fishes, Poecilia velifera and P. mexicana , to explore the link between genes and mating behaviors that has resulted in pre-mating reproductive isolation between these species. Using backcross hybrids created from the F1 male offspring of reciprocal interspecific crosses between a sailfin molly ( P. velifera ) and a shortfin molly ( P. mexicana ), we examined the effects of Y-linkage and autosomal contributions on the expression of two male mating behaviors: courtship displays and gonopodial thrusts. The F1 hybrid males displayed a strong influence of sire on courtship display rates, with F1 males sired by the sailfin species showing courtship display rates that were up to three times higher than the rates of displays performed by F1 males sired by the shortfin species. These results suggest a Y-linked genetic effect on the expression of courtship display behavior. Comparisons between backcross hybrid males with sailfin Y-chromosomes or shortfin Y-chromosomes suggested that the interaction of autosomal genes also influences the inheritance of courtship display rates. Sailfin autosomal genes significantly increased the probability of performing courtship displays for hybrid males, and increased display rate for males from the sailfin Y-chromosome line. Autosomal genes had less of an impact on gonopodial thrusting behavior, however, thrust rates did significantly decrease with an increasing proportion of sailfin autosomes in males from the shortfin Y-chromosome line. These results suggest that the inheritance of species differences in mating signals between shortfin and sailfin mollies involves both genes found on the Y-chromosome and autosomal gene influences on their expression.     

Cranial ontogeny of Papio baboons (Papio hamadryas)

Cranial form in subspecies of Papio baboons (Papio hamadryas) varies in relation to size, geography, and sex. However, knowledge about this variation is based mainly on adults, precluding direct assessments of the evolutionary factors that are ultimately responsible for adult shape variation. Consequently, this study tests hypotheses about the development of size and shape differences among subspecies of Papio baboons, anticipating limited evolutionary divergences in the ontogenetic pathways leading to adult endpoints. Geometric morphometric and bivariate allometric analyses are used to explore developmental size and shape variation. Allometric scaling in adult Papio baboons occurs because both sexes and all subspecies follow similar developmental pathways to a variety of adult forms. However, complex allometry contributes to form differences, producing potentially important shape differences that emerge during development. Modest shape differences that are statistically independent of size distinguish chacma baboons (P. h. ursinus) from other forms. A small-headed subspecies, the Kinda baboon (P. h. kindae), also presents a distinctive ontogeny, and may provide insights into the evolution of size change in this species. Variation among subspecies that is statistically independent of size involves the rostrum, zygomatic breadths, and cranial flexion. These features may be related to diet, but the precise biomechanical correlates of baboon form variation remain unclear.     

Population genetic insights into the social organization of Guinea baboons (Papio papio): Evidence for female‐biased dispersal

Sex differences in philopatry and dispersal have important consequences on the genetic structure of populations, social groups, and social relationships within groups. Among mammals, male dispersal and female philopatry are most common and closely related taxa typically exhibit similar dispersal patterns. However, among four well‐studied species of baboons, only hamadryas baboons exhibit female dispersal, thus differing from their congenerics, which show female philopatry and close‐knit female social relationships. Until recently, knowledge of the Guinea baboon social system and dispersal pattern remained sparse. Previous observations suggested that the high degree of tolerance observed among male Guinea baboons could be due to kinship. This led us to hypothesize that this species exhibits male philopatry and female dispersal, conforming to the hamadryas pattern. We genotyped 165 individuals from five localities in the Niokolo‐Koba National Park, Senegal, at 14 autosomal microsatellite loci and sequenced a fragment of the mitochondrial hypervariable region I (HVRI) of 55 individuals. We found evidence for higher population structuring in males than in females, as expected if males are the more philopatric sex. A comparison of relatedness between male–male and female–female dyads within and among communities did not yield conclusive results. HVRI diversity within communities was high and did not differ between the sexes, also suggesting female gene flow. Our study is the first comprehensive analysis of the genetic population structure in Guinea baboons and provides evidence for female‐biased dispersal in this species. In conjunction with their multilevel social organization, this finding parallels the observations for human hunter‐gatherers and strengthens baboons as an intriguing model to elucidate the processes that shaped the highly cooperative societies of Homo. Am. J. Primatol. 77:878–889, 2015. © 2015 The Authors. American Journal of Primatology Published by Wiley Periodicals Inc.     

Diurnal variations in serum testosterone concentrations of captive adult male chacma baboons (Papio ursinus)

Captive adult male chacma baboons (Papio ursinus) housed with natural lighting exposure and blood sampled at 3-hr intervals showed significant diurnal variations in serum testosterone concentrations. Low mean concentrations were found at 0800 hr approximately 1 hr after sunrise and mean concentrations were their highest at 2000 hr approximately 1 ¼ hr after sunset.     

Fecal cortisol levels in free-ranging female chacma baboons: relationship to dominance, reproductive state and environmental factors

Savannah baboons are one of the few mammalian species that do not exhibit seasonal reproduction patterns and are therefore ideally suited to study the effect of female reproductive states (cycling, pregnant, lactating) on cortisol levels independent of seasonal factors. Fecal samples from 10 free-ranging female chacma baboons (Papio hamadryas ursinus), collected during a period of 17 months, were analyzed using a steroid-extraction method. Reproductive state had a significant effect on fecal cortisol, with lowest levels found in estrous females. Fertility was not related to fecal cortisol levels; we found no significant differences between samples collected on conceptive and nonconceptive cycles. Environmental factors explained most of the variance of fecal cortisol levels. Cortisol measures were strongly correlated with seasonal differences such as daylight duration, temperature and the amount of time that baboons spent resting. We measured higher cortisol levels during winter months and suggest that this could be related to shorter resting periods and to the cold minimum ambient temperatures at this study site. Finally, we found no relationship between social rank nor the rate of agonistic interactions with basal fecal cortisol levels.     

Detection of Mycobacterium tuberculosis infection in chacma baboons (Papio ursinus) using the QuantiFERON-TB Gold (In-Tube) assay

Background  Early diagnosis of simian tuberculosis (TB) is vital to prevent transmission of this disease. We evaluated the ability of the QuantiFERON-TB Gold (In-Tube Method) assay (QFG-IT) to detect TB in chacma baboons ( Papio ursinus ).
Methods  Fifty-one baboons were tested using the Tuberculin Skin Test (TST) and the QFG-IT. Baboons testing positive, and animals exposed to infected individuals, were euthanised and subjected to necropsy. Selected tissues were processed for histopathology, mycobacterial culture and genetic speciation.
Results  Tuberculosis was confirmed in one TST positive/QFG-IT positive animal and one TST negative/QFG-IT positive animal. One TST positive/QFG-IT negative animal and five TST negative/QFG-IT negative animals were confirmed uninfected following necropsy.
Conclusion  The QFG-IT correctly detected TB in two baboons, including one TST negative individual and correctly identified six baboons as uninfected, including one TST positive individual. The QFG-IT shows promise as a sensitive, specific test for TB in chacma baboons.     

Out of the mouths of baboons: stress,life history,and dental development in the Awash National Park hybrid zone,Ethiopia

The techniques of dental histology provide a method for reconstructing much of the life history of an individual, as accentuated increments visible in polarized light microscopy record incidents of physiological stress during the formation of dental tissues. Combined with counts of the normal periodic growth increments, they provide a means of reconstructing the chronology of dental development, age at death, and the ages at which stress occurs. In this study, we determine age at death and reconstruct the chronology of dental development in two male anubis baboons from Uganda and two female baboons from the Awash National Park hybrid zone. For the female baboons, we used the dates of death and rainfall records for the region to determine date of birth, ages at periods of physiological stress, dates at which these stresses occurred, and rainfall amounts for those months.Ages determined histologically for each specimen are comparable to ages estimated from dental emergence schedules and dental scores for wild baboons. Crown formation times are longer than those reported in radiographic studies of captive yellow baboons. Age at initiation of crown formation is similar to that reported for radiographic studies, but ages at completion of crown formation are consistently later. The pattern of stresses is similar in the two female baboons, suggesting that individual life history intersects with local ecology to produce a pattern of accentuated increments occurring during the weaning process and at the onset of menarche, as well as during the first postweaning dry and rainy periods.     

Female perineal swelling and its effects on male sexual arousal: An apparent sexual releaser in the chacma baboon (Papio ursinus)

The function of the periodic perineal swelling that females of some primate species show in relation to their menstrual cycle has long puzzled many scientists. A role in female attractiveness was suspected, but fluctuations in female behaviors concomitant to these changes in female appearance have always prevented its assessment. By attaching a plastic reproduction of a fully swollen perineum to ovariectomized female chacma baboons, it has finally been demonstrated that the sexual swelling hasan important function in the sexual communication of this species. It induces sexual arousal in male conspecifics. The way the perineal swelling acts and other characteristic aspects of this feature appear to qualify it as a releaser for sexual behavior.     

Greeting movements among adult males in a colony of baboons:Papio hamadryas,P. cynocephalus and their hybrids

Seven greeting movements performed by four adult males belonging to a colony of baboons (Papio hamadryas, P. cynocephalus and their hybrids) were described. The hamadryas male has more number and more refined repertoire of movements than the yellow baboons, what would mean that the greeting movements possess a species-specific nature. This characteristic is expressed also by the existence of some inappropriate responses of the yellow baboons to the greeting of the hamadryas male. The differences in the greeting movements between both species would be explained as characteristic consequences of their social system organization. The hybrid male, having acquired a system organization similar to that of the hamadryas male, has acquired the same signal code, too, according to this system. The hybridization tendency would be adaptive in those colonies or troops with mixed species.     

Life history and the competitive environment: trajectories of growth,maturation, and reproductive output among chacma baboons

The social environment is a key feature influencing primate life histories. Chacma baboons (Papio hamadryas ursinus) are a female-bonded species with a strict linear dominance hierarchy. In this species, the allocation of energy to competing demands of growth and reproduction is hypothesized to vary as a function of competitive ability, which in turn increases with social rank. Since growth rate is a major component of life history models, measures of age-specific growth were used to analyze variation in life history traits across social ranks. Weights of 42 immature baboons were obtained without sedation or baiting from a troop of well-habituated chacma baboons in the Okavango Delta, Botswana. Using demographic and weight data from this wild population, five main findings emerged: 1) Weight for age and growth rate of infant and juvenile females are positively associated with maternal rank. 2) Male growth is not influenced by maternal rank. 3) Female growth shows smaller variation across feeding conditions than male growth. 4) Low-ranking adult females continue investment in offspring through prolonged lactation until they reach a weight comparable to that of high-ranking infants. 5) The benefit of rank to reproductive success shown in this study is 0.83 additional offspring. Reproductive span determined predominantly by age at maturation contributes 27-38% to the difference in expected number of offspring by rank, vs. 62-73% due to reproductive rate. These findings have major implications for understanding the role of social environment in phenotypic plasticity of life history traits, and in the evolution of primate life histories.     

Predation by a troop of olive baboons (Papio anubis)

During 1970–1971, a troop of 49 olive baboons was observed in a partially protected area in Kenya, not far from the village of Gilgil. The baboons were seen to catch and eat 47 small animals, a rate of predation far higher than has been reported for any other nonhuman primate. Prey animals included hares, small antelope and the neonatal young of larger antelope. Adult male baboons caught and ate all but three of the prey animals. Adult females caught hares three times, but only once was a female able to keep and eat most of the animal she had caught. There was no significant seasonal variation in the occurrence of this behavior. The baboons appeared to search out prey deliberately and to come upon it by accident. No instances of cooperative hunting or voluntary sharing were seen. Both incidence and form of this predatory behavior may be influenced by learned, local tradition.     

Genetics of sex determination in flowering plants

Most flowering plant species are hermaphroditic, but a small number of species in most plant families are unisexual (i.e., an individ-ual will produce only male or female gametes). Because species with unisexual flowers have evolved repeatedly from hermaphroditic progenitors, the mechanisms controlling sex determination in flowering plants are extremely diverse. Sex is most strongly determined by genotype in all species but the mechanisms range from a single controlling locus to sex chromosomes bearing several linked locirequired for sex determination. Plant hormones also influence sex expression with variable effects from species to species. Here, we review the genetic control of sex determination from a number of plant species to illustrate the variety of extant mechanisms. We emphasize species that are now used as models to investigate the molecular biology of sex determination. We also present our own investigations of the structure of plant sex chromosomes of white campion (Silene latifolia - Melan-drium album). The cytogenetic basis of sex determination in white campion is similar to mammals in that it has a male-specific Y-chromosome that carries dominant male determining genes. If one copy of this chromosome is in the genome, the plant is male. Otherwise it is female. Like mammalian Y-chromosomes, the white campion Y-chromosome is rich in repetitive DNA. We isolated repetitive sequences from microdissected Y-chromosomes of white campion to study the distribution of homologous repeated sequences on the Y-chromosome and the other chromosomes. We found the Y to be especially rich in repetitive sequences that were generally dispersed over all the white campion chromosomes. Despite its repetitive character, the Y-chromosome is mainly euchromatic. This may be due to the relatively recent evolution of the white campion sex chromosomes compared to the sex chromosomes of animals. © 1994 Wiley-Liss, Inc.     

Hybridization and population genetics of two macaque species in Sulawesi, Indonesia

This study investigates hybridization and population genetics of two species of macaque monkey in Sulawesi, Indonesia, using molecular markers from mitochondrial, autosomal, and Y-chromosome DNA. Hybridization is the interbreeding of individuals from different parental taxa that are distinguishable by one or more heritable characteristics. Because hybridization can affect population structure of the parental taxa, it is an important consideration for conservation management. On the Indonesian island of Sulawesi an explosive diversification of macaques has occurred; seven of 19 species in the genus Macaca live on this island. The contact zone of the subjects of this study, M. maura and M. tonkeana, is located at the base of the southwestern peninsula of Sulawesi. Land conversion in Sulawesi is occurring at an alarming pace; currently two species of Sulawesi macaque, one of which is M. maura, are classified as endangered species. Results of this study indicate that hybridization among M. maura and M. tonkeana has led to different distributions of molecular variation in mitochondrial DNA and nuclear DNA in the contact zone; mitochondrial DNA shows a sharp transition from M. maura to M. tonkeana haplotypes, but nuclear DNA from the parental taxa is homogenized in a narrow hybrid zone. Similarly, within M. maura divergent mitochondrial DNA haplotypes are geographically structured but population subdivision in the nuclear genome is low or absent. In M. tonkeana, mitochondrial DNA haplotypes are geographically structured and a high level of nuclear DNA population subdivision is present in this species. These results are largely consistent with a macaque behavioral paradigm of female philopatry and obligate male dispersal, suggest that introgression between M. maura and M. tonkeana is restricted to the hybrid zone, and delineate one conservation management unit in M. maura and at least two in M. tonkeana.     

Body composition in baboons: Evaluating a morphometric method

The objective of this study was to determine whether noninvasive morphometric measurements of olive baboons (Papio cynocephalus anubis) can reliably predict lean body mass and fat mass in this species. Crown-rump length, triceps circumference, and skinfold measures at the neck, subscapular, suprailiac, and triceps sites were obtained prior to necropsy from 21 clinically normal infant baboons at 18 weeks of age and from 22 clinically normal adolescent baboons at 5 years of age. At necropsy, the lean body mass and body fat mass were measured using gravimetric methods. Pearson's correlations and regression analysis were used to test the relationship between direct measures of lean and fat mass obtained at necropsy with calculated estimates based on morphometric measures obtained prior to death. Our null hypothesis was that the morphometric measures (individually or in combination) were not related to direct measures of fat mass or lean mass. Non-linear and multiple regression estimators, by age and gender, were derived and provided increased predictability. Our results indicate that (1) morphometric measures can accurately predict lean body mass in male and female baboons; (2) morphometric measures used to predict lean body mass change with age; (3) morphometric measures are strongly associated with body fat mass at 18 weeks of age but are not as strongly associated with body fat mass in 5-year-old baboons; (4) triceps circumference provides the best single indicator of lean body mass for both genders and age periods; (5) baboons are like humans in that adolescent females tend to accumulate body fat while males of the same age tend to develop lean mass; and (6) combinations of these morphometric measurements explain between 70% and 100% of the variability and can be used to estimate lean and fat mass in baboons.     

Inter- and intrahabitat dietary variability of chacma baboons (Papio ursinus) in South African savannas based on fecal delta13C, delta15N, and %N

Baboons are dietary generalists, consuming a wide range of food items in varying proportions. It is thus difficult to quantify and explain the dietary behavior of these primates. We present stable carbon (delta(13)C) and nitrogen (delta(15)N) isotopic data, and percentage nitrogen (%N), of feces from chacma baboons (Papio ursinus) living in two savanna environments of South Africa: the mountainous Waterberg region and the low-lying Kruger National Park. Baboons living in the more homogeneous landscapes of the Waterberg consume a more isotopically heterogeneous diet than their counterparts living in Kruger Park. Grasses and other C(4)-based foods comprise between approximately 10-20% (on average) of the bulk diet of Kruger Park baboons. Carbon isotopic data from the Waterberg suggest diets of approximately 30-50% grass, which is higher than generally reported for baboons across the African savanna. Based on observations of succulent-feeding, we propose that baboons in the Waterberg consume a mix of C(4) grasses and CAM-photosynthesizing succulents in combined proportions varying between approximately 5-75% (average, approximately 35%). Fecal delta(15)N of baboons is lower than that of sympatric ungulates, which may be due to a combination of low levels of faunivory, foraging on subterranean plant parts, or the use of human foods in the case of Kruger Park populations. Fecal N levels in baboons are consistently higher than those of sympatric ungulate herbivores, indicating that baboons consume a greater proportion of protein-rich foods than do other savanna mammals. These data suggest that chacma baboons adapt their dietary behavior so as to maximize protein intake, regardless of their environment.     

A Recent Shift from Polygyny to Monogamy in Humans Is Suggested by the Analysis of Worldwide Y-Chromosome Diversity

Molecular genetic data contain information on the history of populations. Evidence of prehistoric demographic expansions has been detected in the mitochondrial diversity of most human populations and in a Y-chromosome STR analysis, but not in a previous study of 11 Y-chromosome SNPs in Europeans. In this paper, we show that mismatch distributions and tests of mutation/drift equilibrium based on up to 166 Y-chromosome SNPs, in 46 samples from all continents, also fail to support an increase of the male effective population size. Computer simulations show that the low nuclear versus mitochondrial mutation rates cannot explain these results. However, ascertainment bias, i.e., when only highly variable SNP sites are typed, may be concealing any Y SNPs evidence for a recent, but not an ancient, increase in male effective population sizes. The results of our SNP analyses can be reconciled with the expansion of male effective population sizes inferred from STR loci, and with mitochondrial evidence, by admitting that humans were essentially polygynous during much of their history. As a consequence, until recently only a few men may have contributed a large fraction of the Y-chromosome pool at every generation. The number of breeding males may have increased, and the variance of their reproductive success may have decreased, through a recent shift from polygyny to monogamy, which is supported by ethnological data and possibly accompanied the shift from mobile to sedentary communities.