Genetic evidence reveals temporal change in hybridization patterns in a wild baboon population

The process and consequences of hybridization are of interest to evolutionary biologists because of the importance of hybridization in understanding reproductive isolation, speciation, and the influence of introgression on population genetic structure. Recent studies of hybridization have been enhanced by the advent of sensitive, genetic marker-based techniques for inferring the degree of admixture occurring within individuals. Here we present a genetic marker-based analysis of hybridization in a large-bodied, long-lived mammal over multiple generations. We analysed patterns of hybridization between yellow baboons (Papio cynocephalus) and anubis baboons (Papio anubis) in a well-studied natural population in Amboseli National Park, Kenya, using genetic samples from 450 individuals born over the last 36 years. We assigned genetic hybrid scores based on genotypes at 14 microsatellite loci using the clustering algorithm implemented in STRUCTURE 2.0, and assessed the robustness of these scores by comparison to pedigree information and through simulation. The genetic hybrid scores showed generally good agreement with previous morphological assessments of hybridity, but suggest that genetic methods may be more sensitive for identification of low levels of hybridity. The results of our analysis indicate that the proportion of hybrids in the Amboseli population has grown over time, but that the average proportion of anubis ancestry within hybrids is gradually decreasing. We argue that these patterns are probably a result of both selective and nonselective processes, including differences in the timing of life-history events for hybrid males relative to yellow baboon males, and stochasticity in long-distance dispersal from the source anubis population into Amboseli.     

Immigration of aPapio anubis male into a group ofPapio cynocephalus baboons and

The 1982 observation of the immigration of an adult male olive baboon, Papio anubis,into a group of yellow baboons, Papio cynocephalus,in Amboseli National Park, Kenya, constitutes the first confirmed report of interbreeding between the two species within the Amboseli baboon population. We document the social aspects of the immigration and describe subsequent sightings of anubisbaboons in Amboseli that confirm the existence of a previously unrecognized hybrid zone in Kenya.     

Immigration and hybridization patterns of yellow and anubis baboons in and around Amboseli, Kenya

In 1986, Samuels and Altmann reported evidence for a hybrid zone between Papio anubis and Papio cynocephalus in Amboseli, Kenya, in a baboon population that has been the subject of long-term study since 1971 [Samuels & Altmann, International Journal of Primatology 7:131-138, 1986]. In the current report we document ongoing patterns of hybridization in Amboseli between anubis and yellow baboons. In July 2000, we exhaustively scored living members of study groups for their degree of hybridity, using seven phenotypic characteristics (five in juveniles). We also scored all former members of study groups on the basis of photographic records, field notes, and observer recollections. A total of five anubis males and 11 males with hybrid phenotypes have immigrated into study groups over the course of the long-term study, and immigrations by hybrid males have increased in frequency over time. Further, the increasing frequency of hybrid phenotypes among animals born into study groups indicates that anubis and hybrid males have successfully reproduced in study groups. However, hybrid phenotypes and anubis immigrations were limited to groups in the southwestern portion of the Amboseli basin, with no hybrids occurring in the six eastern groups. Finally, we present evidence that anubis and hybrid males in Amboseli exhibit patterns of natal dispersal that are different from those of yellow males in Amboseli: males with anubis or hybrid phenotypes were significantly more likely to immigrate as juveniles or young subadults than were yellow males.     

Age at maturity in wild baboons: genetic, environmental and demographic influences

The timing of early life-history events, such as sexual maturation and first reproduction, can greatly influence variation in individual fitness. In this study, we analysed possible sources of variation underlying different measures of age at social and physical maturation in wild baboons in the Amboseli basin, Kenya. The Amboseli baboons are a natural population primarily comprised of yellow baboons (Papio cynocephalus) that occasionally hybridize with anubis baboons (Papio anubis) from outside the basin. We found that males and females differed in the extent to which various factors influenced their maturation. Surprisingly, we found that male maturation was most strongly related to the proportion of anubis ancestry revealed by their microsatellite genotypes: hybrid males matured earlier than yellow males. In contrast, although hybrid females reached menarche slightly earlier than yellow females, maternal rank and the presence of maternal relatives had the largest effects on female maturation, followed by more modest effects of group size and rainfall. Our results indicate that a complex combination of demographic, genetic, environmental, and maternal effects contribute to variation in the timing of these life-history milestones.     

Genetic structure in a dynamic baboon hybrid zone corroborates behavioural observations in a hybrid population

Behaviour and genetic structure are intimately related: mating patterns and patterns of movement between groups or populations influence the movement of genetic variation across the landscape and from one generation to the next. In hybrid zones, the behaviour of the hybridizing taxa can also impact the incidence and outcome of hybridization events. Hybridization between yellow baboons and anubis baboons has been well documented in the Amboseli basin of Kenya, where more anubis-like individuals tend to experience maturational and reproductive advantages. However, it is unknown whether these advantages are reflected in the genetic structure of populations surrounding this area. Here, we used microsatellite genotype data to evaluate the structure and composition of baboon populations in southern Kenya. Our results indicate that, unlike for mitochondrial DNA, microsatellite-based measures of genetic structure concord with phenotypically based taxonomic distinctions and that the currently active hybrid zone is relatively narrow. Isolation with migration analysis revealed asymmetric gene flow in this region from anubis populations into yellow populations, in support of the anubis-biased phenotypic advantages observed in Amboseli. Populations that are primarily yellow but that receive anubis gene flow exhibit higher levels of genetic diversity than yellow populations far from the introgression front. Our results support previous work that indicates a long history of hybridization and introgression among East African baboons. Specifically, it suggests that anubis baboons are in the process of gradual range expansion into the range of yellow baboons, a pattern potentially explained by behavioural and life history advantages that correlate with anubis ancestry.     

Demography of Amboseli baboons, 1963–1983

Repeated censuses of a population of yellow baboons (Papio cynocephalus) in Amboseli National Park, Kenya, revealed a decrease from over 2,500 animals in 1963–1964 to 123 individuals in 1979, or from a density of about 73 to 1.8 baboons per km² over a 15-year period. Median group size decreased from 43 in 1964 to 27 in 1979. The largest and smallest groups declined the most; groups near the median have maintained fairly stable size and age distributions. The population seemed to have stabilized by 1983 at approximately 150 animals in six groups (median group size 28; density 2.2/km²). Although baboon population and group size appeared to be stable during 1963–1964, the age distribution and demographic parameters (age-specific mortality and natality for one social group) during that year indicate that the population decline had already started. The rate of population decline was greatest in the 1964–1969 period and remained appreciable during the next 5 years. The decline of the baboon population was paralleled by that of other Amboseli savannah woodland mammalian species and took place during a period of very high mortality of fever trees (Acacia xanthophloea) and extensive invasion of the area by halophytes, a transition brought on by rising ground water and consequent elevation of the soil salinity zone. In this and several other primate populations, mortality of infants and juveniles appears to be the demographic variable most sensitive to environmental change.     

A note on the activities of a solitary male baboon

This paper describes the behavior and activity patterns of a solitary adult male yellow baboon (Papio cynocephalus) living in the Amboseli National Park, Kenya. Social events surrounding the male's departure from his group, his contacts with other baboons while solitary, and events surrounding his return to the group are described in detail. The distribution of the male's time among several activity states, called histime budget, the average duration of these activities and the autocorrelation of activity states are analyzed and compared to the same measures of activity taken on group living males. The information presented indicates that a solitary male, even when injured, is not necessarily destined to die or to have a low reproductive potential.     

The Ap-Bp blood groups of baboons

Four isoimmunized baboons each produced isoantibodies defining a number of blood factors of baboon blood of which two, A^p and B^p, have been most intensively studied. The two blood factors determine the A^P-B^P blood group system which, judging from its serological behavior, may be the baboon analogue of the human M-N system and the chimpanzee V-A-B system. Tests for A^P-B^P types of 592 baboons showed striking differences in the distributions of the four types among the four sub-species, Papio cynocephalus, Papio anubis, Papio ursinus (South Africa) and Papio papio (Senegal). The baboon A^P-B^P types could also be demonstrated by tests on the red cells of geladas (Theropithecus gelada). If one assumes inheritance by multiple allelic genes, then the existence of only a single gene O^p need be invoked for Papio ursinus, three alleles O^p, A^p and B^p for Papio cynocephalus and Papio anubis, but four alleles for Papio papio including an allele, very frequent in that subspecies, which determines an agglutinogen having both blood factors A^p and B^p.     

Distribution and Habitat Associations of Baboons (Papio hamadryas) in Central Eritrea

At least three diurnal primate taxa are still present in Eritrea, NE Africa: hamadryas baboons (Papio hamadryas hamadryas), olive baboons (Papio h. anubis) and grivet monkeys (Chlorocebus aethiops aethiops). However, information on status and distribution of primates and their habitats in Eritrea is outdated and incomplete. We conducted a primate survey, focussing on hamadryas baboons, to obtain data which will be integrated in a national wildlife management and conservation plan in Eritrea. We obtained information about the geographical distribution and abundance of baboons, their altitudinal range, habitat quality of their home-ranges, aggregation sizes at sleeping cliffs and predator presence. We described habitat quality via the Normalized Difference Vegetation Index (NDVI), a vegetation classification of Landsat MSS satellite data. Hamadryas and olive baboons are still present in Eritrea in ample numbers. Their geographical distributions in 1997 and 1998 did not deviate significantly from their historical distributions. An estimated 15,000 Papio hamadryas hamadryas lived in the 25,000-km² area of survey (0.58 baboons/km²). Population densities of hamadryas baboons in many parts of the survey area are higher than at Kummer's (1968) study site in Ethiopia. Hamadryas baboons live at all altitudes in four of five ecogeographical zones of Eritrea. Olive baboons replaced them in the western lowlands. Both baboon taxa tend to select better quality habitats, characterized by a higher normalized difference vegetation index (NDVI) than the average for the respective ecogeographical zones. Hamadryas baboons show a greater ecological plasticity than olive baboons, which are confined to riverbeds with extended gallery forest. By the end of 1999, a hybrid zone could not be confirmed.     

Alternation of sleeping groves by yellow baboons (Papio cynocephalus) as a strategy for parasite avoidance

The primary locus of contact between free-living yellow baboons (Papio cynocephalus) in the Amboseli National Park of Kenya and the infective stages of their intestinal parasites is believed to be soil beneath sleeping trees contaminated by the baboons' own fecal emissions. In this report, we present evidence both that infective ova and larvae of intestinal parasites are found at very high densities in the soil beneath sleeping groves and that Amboseli baboons substantially reduce their contact with this reservoir of parasites by alternating periods of a few consecutive nights' use of any particular grove with much longer periods of avoidance of that grove. Although many factors other than the presence of parasite larvae also influence choice of sleeping groves, we propose as a working hypothesis that the temporal pattern of sleeping grove alternation shown by Amboseli baboons reflects a subtle behavioral strategy for parasite avoidance.     

Some developmental markers in yellow baboon infants of Mikumi National Park,Tanzania

Infants of known birthdates were sampled from a population of yellow baboons (Papio cynocephalus) in Mikumi National Park, Tanzania, to ascertain the reliability of several maturational changes which could be used to age infants whose birthdates are unknown. The transition from the infant's black natal coat to the uniform yellow or tan adult pelage proved extremely variable, with completion varying from 7 to 19 months. The transition from the pink skin of the newborn to the completely grey adult pigmentation was much less variable. Skin on the hands and feet and on the paracallosal area was completely grey in all individuals by 8 months, while skin on the face and ears changed more gradually and was entirely grey by 12 months. These data are in substantial agreement with maturational markers established for yellow baboon infants in Amboseli National Park, Kenya, despite differences in habitat and age-sex structure between the two populations.     

Female Reproductive Parameters of Tana River Yellow Baboons

We describe the female reproductive parameters of yellow baboons at the Tana River National Primate Reserve, Kenya. We present data on menarche, cycle length, pregnancy, birth, postpartum amenorrhea, interbirth interval, and infant survival. We also briefly compare our data to those reported for yellow baboon females at the Amboseli Reserve, Kenya. Our results indicate statistically significant differences in some of these reproductive parameters between the two sites.     

Class I MHC expression in the yellow baboon

MHC class I molecules play a crucial role in the immune response to pathogens and vaccines and in self/non-self recognition. Therefore, characterization of MHC class I gene expression of Papio subspecies is a prerequisite for studies of immunology and transplantation in the baboon (papio hamadryas). To elucidate MHC class I expression and variation within Papio subspecies and to further investigate the evolution of A and B loci in Old World primates, we have characterized the expressed class I repertoire of the yellow baboon (Papio hamadryas cynocephalus) by cDNA library screening. A total of nine distinct MHC class I cDNAs were isolated from a spleen cDNA library. The four A alleles and four B alleles obtained represent four distinct loci indicating that a duplication of the A and B loci has taken place in the lineage leading to these Old World primates. No HLA--C homologue/orthologue was found. In addition a single, nonclassical homologue of HLA--E was characterized. Examination of nucleotide and extrapolated protein sequences indicates that alleles at the two B loci are much more diversified than the alleles at the A loci. One of the A loci in particular appears to display very limited polymorphism in both Papio hamadryas cynocephalus and Papio hamadryas anubis subspecies. The failure to detect a homologue of HLA--C in the baboon provides additional evidence for the more recent origin of this locus in the pongidae and hominidae: Further comparative analysis with MHC sequences among the primate species reveals specific patterns of divergence and conservation within class I molecules of the yellow baboon.     

Complete rectal prolapse in wild anubis baboons (Papio anubis)

This report describes two cases of rectal prolapse in wild anubis baboons (Papio anubis), with one spontaneous resolution. Both occurred after individuals consumed low‐water, high‐fibre dried maize during provisioning prior to capture, while one also experienced distress during capture.     

Ecology and age,but not genetic ancestry,predict fetal loss in a wild baboon hybrid zone

Objectives

Pregnancy failure represents a major fitness cost for any mammal, particularly those with slow life histories such as primates. Here, we quantified the risk of fetal loss in wild hybrid baboons, including genetic, ecological, and demographic sources of variance. We were particularly interested in testing the hypothesis that hybridization increases fetal loss rates. Such an effect would help explain how baboons may maintain genetic and phenotypic integrity despite interspecific gene flow.

Materials and Methods

We analyzed outcomes for 1020 pregnancies observed over 46 years in a natural yellow baboon-anubis baboon hybrid zone. Fetal losses and live births were scored based on records of female reproductive state and the appearance of live neonates. We modeled the probability of fetal loss as a function of a female's genetic ancestry (the proportion of her genome estimated to be descended from anubis [vs. yellow] ancestors), age, number of previous fetal losses, dominance rank, group size, climate, and habitat quality using binomial mixed effects models.

Results

Female genetic ancestry did not predict fetal loss. Instead, the risk of fetal loss is elevated for very young and very old females. Fetal loss is most robustly predicted by ecological factors, including poor habitat quality prior to a home range shift and extreme heat during pregnancy.

Discussion

Our results suggest that gene flow between yellow and anubis baboons is not impeded by an increased risk of fetal loss for hybrid females. Instead, ecological conditions and female age are key determinants of this component of female reproductive success.     

Scalp EEG for the diagnosis of epilepsy and photosensitivity in the baboon

Spontaneous seizures have been observed in several baboon species housed at the Southwest National Primate Research Center (SNPRC), including Papio hamadryas anubis and cynocephalus/anubis, hamadryas/anubis, and papio/anubis hybrids. The goal of this study was to establish a noninvasive, reliable electroencephalographic technique to characterize epilepsy phenotypes and assess photosensitivity in these subspecies. Thirty baboons with witnessed seizures, and 15 asymptomatic baboons underwent scalp electroencephalograms (EEGs) with photic stimulation (PS). The sensitivity and specificity of surface EEG for identifying interictal epileptic discharges (IEDs) in baboons with witnessed seizures were examined. The morphology of IEDs, electroclinical features of seizures and responses to PS, reproducibility of EEG findings, and intrarater reliability were also evaluated. Twenty-three seizure baboons (77%) demonstrated IEDs, predominantly with frequencies of 4-6 Hz in 18 baboons and 2-3 Hz in six baboons. Two seizure animals had a mixture of 2-3-Hz and 4-6-Hz IEDs. All animals with 2-3-Hz IEDs were 3 years old or younger. Myoclonic seizures (MS) and generalized tonic-clonic seizures (GTCS) were recorded in 13 baboons (43%). PS activated IEDs in 15 baboons (50%) and seizures in nine baboons. The presence of IEDs or seizures was not associated with a particular gender or species (Fisher exact test, alpha=0.05). Seizures were more common in animals >3 years old, while PS-induced IEDs and seizures were more prevalent in P.h. anubis/cynocephalus crosses compared to P.h. anubis. In the asymptomatic controls, IEDs were recorded in five baboons (33%), and photoparoxysmal responses were observed in two (13%). Surface EEG is a sensitive and reliable instrument for characterizing the epilepsy encountered in Papio species. Electroclinically, the seizure animals had generalized epilepsy with photosensitivity. The variation in IED morphology may be age-related or it may reflect different epileptic phenotypes. Ketamine provoked IEDs and seizures in most seizure animals and only in a few asymptomatic baboons; therefore, it may enhance the sensitivity of surface EEG for detecting a predisposition to epilepsy.     

Baboons of the amboseli basin: Demographic stability and change

A cross-sectional demographic analysis of the entire baboon population of the Amboseli basin of southern Kenya was undertaken to complement the lon-gitudinal, intensive studies of a subpopulation. The present survey documented the extent and persistence of the influx of anubis baboons into the predominantly cynocephalus community and provided another example of the nonrandom dispersal patterns of cercopithecine males. In addition, the survey confirmed continued demographic stability of the basinwide baboon population and even growth in groups that had access to better feeding conditions, despite decline of the baboons' preferred habitat and expansion of human activities into wildlife areas. Conflicts with activities of humans, however, indicate that the present well-being of the Amboseli baboon population may be short-lived.     

Taste Preference Thresholds for Food-Associated Sugars in Baboons (Papio hamadryas anubis)

We aimed to determine taste preference thresholds for 5 food-associated sugars in Papio hamadryas anubis. In a 2-bottle preference test of brief duration (2 min) 4 subadult baboons significantly preferred concentrations as low as 10 mM sucrose, 20 mM fructose, lactose, and maltose, and 25 mM glucose over tap water. Presentation of suprathreshold sugar solutions led to marked concentration-dependent polydipsia. The results show that baboons are among the most sugar-sensitive nonhuman primates tested so far and, thus, support the assumption that Papio hamadryas anubis may use sweetness as a criterion for food selection.     

Fatal intragroup kidnapping in yellow baboons

The fatal kidnapping of a 5-day-old baboon (Papio cynocephalus) in Amboseli National Park, Kenya, is described. Although pulling and rough handling of primate infants by nonmothers are frequently observed, records of fatal intragroup kidnappings are rare. In the instance described here, the mother, a healthy, primiparous female, did not retrieve the infant from the kidnapper, a higher-ranking juvenile female of the same group, until he died 3 days later, presumably from starvation or dehydration. This incident is compared with other fatal intragroup kidnappings in nonhuman primates and related to adaptive interpretations.     

Systematic reconsideration and a revision of the nomenclature of Kenya baboons

Two populations of baboons in Kenya, often given different specific names, Papio doguera and Papio cynocephalus, were the subject of this investigation. We conducted a field study to determine if these two populations are the same or two different species. We located a zone of contact between the two putative species in the area of Simba Springs and Ithumba Hill. The population in this area was found to represent intergradation on the basis of field observations and detailed metric observations of the morphology. The morphology of this population appears to be intermediate between that of the two populations: the olive baboon, labeled Papio doguera, and the yellow baboon, labeled Papio cynocephalus. We confirmed the findings by statistical analyses of osteometric data. Since the specific separation of the two taxa studied in this investigation is invalid, both are placed in the prior nomen, Papio cynocephalus (Linnaeus, 1766) separating them on the subspecific level, P. c. doguera and P. c. cynocephalus.