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.

Allele-specific gene expression in a wild nonhuman primate population.

Natural populations hold enormous potential for evolutionary genetic studies, especially when phenotypic, genetic and environmental data are all available on the same individuals. However, untangling the genotype-phenotype relationship in natural populations remains a major challenge. Here, we describe results of an investigation of one class of phenotype, allele-specific gene expression (ASGE), in the well-studied natural population of baboons of the Amboseli basin, Kenya. ASGE measurements identify cases in which one allele of a gene is overexpressed relative to the alternative allele of the same gene, within individuals, thus providing a control for background genetic and environmental effects. Here, we characterize the incidence of ASGE in the Amboseli baboon population, focusing on the genetic and environmental contributions to ASGE in a set of eleven genes involved in immunity and defence. Within this set, we identify evidence for common ASGE in four genes. We also present examples of two relationships between cis-regulatory genetic variants and the ASGE phenotype. Finally, we identify one case in which this relationship is influenced by a novel gene-environment interaction. Specifically, the dominance rank of an individual's mother during its early life (an aspect of that individual's social environment) influences the expression of the gene CCL5 via an interaction with cis-regulatory genetic variation. These results illustrate how environmental and ecological data can be integrated into evolutionary genetic studies of functional variation in natural populations. They also highlight the potential importance of early life environmental variation in shaping the genetic architecture of complex traits in wild mammals.

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 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.

Paternal effects on offspring fitness in a multimale primate society.

When females mate with multiple males, paternal care is generally expected to be negligible, because it may be difficult or impossible for males to discriminate their own offspring from those of other males, and because engaging in paternal care may reduce male mating opportunities. Consequently, males in multimale societies are not predicted to provide direct benefits to their offspring. We have recently demonstrated, however, that males in a typical multimale primate society (yellow baboons, Papio cynocephalus) discriminate their own offspring from those of other males and provide care to them in the form of repeated support during agonistic encounters. This observation raises the question of whether fathers enhance offspring fitness in this species. Here we use 30 years of data on age at maturity for 118 yellow baboons with known fathers. We show that the father's presence in the offspring's social group during the offspring's immature period accelerated the timing of physiological maturation in daughters. Sons also experienced accelerated maturation if their father was present during their immature period, but only if the father was high ranking at the time of their birth. Because age at reproductive maturity has a large impact on lifetime reproductive success, our results indicate a direct effect of paternal presence on offspring fitness. This relationship in turn suggests that the multiple roles that males play in multimale animal societies have not been sufficiently examined or appreciated and that paternal effects may be more pervasive than previously appreciated.

Inbreeding depression in non-human primates: a historical review of methods used and empirical data.

Offspring born to related parents may show reduced fitness due to inbreeding depression. Although evidence of inbreeding depression has accumulated for a variety of taxa during the past two decades, such analyses remain rare for primate species, probably because of their long generation time. However, inbreeding can have important fitness costs and is likely to shape life-history traits in all living species. As a consequence, selection should have favored inbreeding avoidance via sex-biased dispersal, extra-group paternity, or kin discrimination. In this paper, we review empirical studies on the effects of inbreeding on fitness traits or fitness correlates in primate species. In addition, we report the methods that have been used to detect inbreeding in primate populations, and their development with the improvement of laboratory techniques. We focus particularly on the advantages and disadvantages using microsatellite loci to detect inbreeding. Although the genetic data that are typically available (partial pedigrees, use of microsatellite heterozygosity as an estimate of genomewide inbreeding) tend to impose constraints on analyses, we encourage primatologists to explore the potential effects of inbreeding if they have access to even partial pedigrees or genetic information. Such studies are important because of both the value of basic research in inbreeding depression in the wild and the conservation issues associated with inbreeding, particularly in threatened species, which include more than half of the currently living primate species.

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.

Determinants of effective population size for loci with different modes of inheritance.

Here we report an assessment of the determinants of effective population size (N(e)) in species with overlapping generations. Specifically, we used a stochastic demographic model to investigate the influence of different life-history variables on N(e)/N (where N = population census number) and the influence of sex differences in life-history variables on N(e) for loci with different modes of inheritance. We applied an individual-based modeling approach to two datasets: one from a natural population of savannah baboons (Papio cynocephalus) in the Amboseli basin of southern Kenya and one from a human tribal population (the Gainj of Papua New Guinea). Simulation-based estimates of N(e)/N averaged 0.329 for the Amboseli baboon population (SD = 0.116, 95% CI = 0.172 - 0.537) and 0.786 for the Gainj (SD = 0.184, 95% CI = 0.498 - 1.115). Although variance in male fitness had a substantial impact on N(e)/N in each of the two primate populations, ratios of N(e) values for autosomal and sex-linked loci exhibited no significant departures from Poisson-expected values. In each case, similarities in sex-specific N(e) values were attributable to the unexpectedly high variance in female fitness. Variance in male fitness resulted primarily from age-dependent variance in reproductive success, whereas variance in female fitness resulted primarily from stochastic variance in survival during the reproductive phase.

Cross-species amplification, non-invasive genotyping, and non-Mendelian inheritance of human STRPs in Savannah baboons.

Twenty-nine human microsatellite primer pairs were screened for their utility in the cross-species amplification of baboon DNA derived from both blood and feces as part of a larger study to identify paternal half sisters in a population of wild baboons (Papio cynocephalus). Forty-one percent (12/29) of the human primers successfully amplified baboon DNA. Of these 12 primers, six amplified fragments that were both polymorphic and heterozygous (mean number of alleles = 6, mean heterozygosity = 87%) and yielded repeatable results. However, only five of these six simple tandem repeat polymorphisms (STRPs) showed patterns of Mendelian inheritance (i.e., mothers and offspring shared at least one allele at each locus), and were therefore useful for determining relatedness between individuals. Analysis of the sixth primer revealed non-Mendelian inheritance, i.e., three of the six known mother-daughter pairs had no shared alleles. This failure was probably due to non-specific fragment amplification, and may have resulted from a different STRP locus being amplified in mother and daughter. This finding highlights the importance of sampling DNA from known parent-offspring pairs when screening microsatellite primers for genetic studies. Multiple, independent replications of genotypes and Mendelian checks are both particularly important when using cross-species amplification or when using a low-quality source of DNA.

Paternal kin discrimination in wild baboons.

Mammals commonly avoid mating with maternal kin, probably as a result of selection for inbreeding avoidance. Mating with paternal kin should be selected against for the same reason. However, identifying paternal kin may be more difficult than identifying maternal kin in species where the mother mates with more than one male. Selection should nonetheless favour a mechanism of paternal kin recognition that allows the same level of discrimination among paternal as among maternal kin, but the hypothesis that paternal kin avoid each other as mates is largely untested in large mammals such as primates. Here I report that among wild baboons, Papio cynocephalus, paternal siblings exhibited lower levels of affiliative and sexual behaviour during sexual consortships than non-kin, although paternal siblings were not significantly less likely to consort than non-kin. I also examined age proximity as a possible social cue of paternal relatedness, because age cohorts are likely to be paternal sibships. Pairs born within two years of each other were less likely to engage in sexual consortships than pairs born at greater intervals, and were less affiliative and sexual when they did consort. Age proximity may thus be an important social cue for paternal relatedness, and phenotype matching based on shared paternal traits may play a role as well.

Hypercortisolism associated with social subordinance or social isolation among wild baboons.

BACKGROUND: The phenomena of basal hypercortisolism and of dexamethasone resistance have long intrigued biological psychiatrists, and much is still unknown as to the causes and consequences of such adrenocortical hyperactivity in various neuropsychiatric disorders. We have analyzed basal cortisol concentrations and adrenocortical responsiveness to dexamethasone in a population of wild baboons living in a national park in Kenya. We tested whether social subordinance in a primate is associated with dexamethasone resistance. Furthermore, we examined whether individual differences in adrenocortical measurements were predicted by the extent of social affiliation in these animals. METHODS: Seventy yellow baboons (Papio cynocephalus) were anesthetized and injected with 5 mg of dexamethasone; the cortisol response was monitored for 6 hours. The animals were of both sexes in a range of ages and had known ranks in the dominance hierarchies within their troops. Extensive behavioral data were available for a subset of 12 adult males who were anesthetized under circumstances that also allowed for the determination of basal cortisol concentrations. RESULTS: The socially subordinate baboons were less responsive to dexamethasone than were the dominant ones; as one manifestation of this, postdexamethasone cortisol values were more than 3 times higher in the dozen lowest-ranking animals compared with the dozen highest. In addition, socially isolated males had elevated basal cortisol concentrations and showed a trend toward relative dexamethasone resistance. CONCLUSIONS: Our findings indicate that social status and degree of social affilitation can influence adrenocortical profiles; specifically, social subordinance or social isolation were associated in our study with hypercortisolism or feedback resistance.

Behavior predicts genes structure in a wild primate group.

The predictability of genetic structure from social structure and differential mating success was tested in wild baboons. Baboon populations are subdivided into cohesive social groups that include multiple adults of both sexes. As in many mammals, males are the dispersing sex. Social structure and behavior successfully predicted molecular genetic measures of relatedness and variance in reproductive success. In the first quantitative test of the priority-of-access model among wild primates, the reproductive priority of dominant males was confirmed by molecular genetic analysis. However, the resultant high short-term variance in reproductive success did not translate into equally high long-term variance because male dominance status was unstable. An important consequence of high but unstable short-term variance is that age cohorts will tend to be paternal sibships and social groups will be genetically substructured by age.

Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group.

A very aggressive young adult male entered one of three long-term study groups of yellow baboons. Papio cynocephalus, approximately 3 weeks after an immobilization project began. The immigrant male's rate of agonistic encounters was appreciably higher than average, and these interactions disproportionately involved adult females as targets. Basal cortisol concentrations were higher and total lymphocyte counts lower for individuals immobilized during the immigration situation than for other individuals; these effects were greater for females than for males. Among animals whose endocrine data were obtained during the immigration period, some were specific targets of the immigrant male's aggression and others were not. Lymphocyte counts were significantly lower for those individuals who were victims of the male's aggression than for noninvolved individuals; a nonsignificant tendency toward higher basal cortisol concentrations for victims was observed as well. The immigrant male himself had a high basal cortisol concentration, a low lymphocyte count, and a testosterone concentration that was triple the average for adult males and almost double the second highest value in the population.