Genome-wide ancestry and introgression in a Zambian baboon hybrid zone.

Hybridization in nature offers unique insights into the process of natural selection in incipient species and their hybrids. In order to evaluate the patterns and targets of selection, we examine a recently discovered baboon hybrid zone in the Kafue River Valley of Zambia, where Kinda baboons (Papio kindae) and grey-footed chacma baboons (P. ursinus griseipes) coexist with hybridization. We genotyped baboons at 14,962 variable genome-wide autosomal markers using double-digest RADseq. We compared ancestry patterns from this genome-wide data set to previously reported ancestry from mitochondrial-DNA and Y-chromosome sources. We also fit a Bayesian genomic cline model to scan for genes with extreme patterns of introgression. We show that the Kinda baboon Y chromosome has penetrated the species boundary to a greater extent than either mitochondrial DNA or the autosomal chromosomes. We also find evidence for overall restricted introgression in the JAK/STAT signalling pathway. Echoing results in other species including humans, we find evidence for enhanced and/or directional introgression of immune-related genes or pathways including the toll-like receptor pathway, the blood coagulation pathway, and the LY96 gene. Finally we show enhanced introgression and excess chacma baboon ancestry in the sperm tail gene ODF2. Together, our results elucidate the dynamics of introgressive hybridization in a primate system while identifying genes and pathways possibly under selection.

Evolution of DNA Methylation in Papio Baboons.

Changes in gene regulation have long been thought to play an important role in primate evolution. However, although a number of studies have compared genome-wide gene expression patterns across primate species, fewer have investigated the gene regulatory mechanisms that underlie such patterns, or the relative contribution of drift versus selection. Here, we profiled genome-scale DNA methylation levels in blood samples from five of the six extant species of the baboon genus Papio (4-14 individuals per species). This radiation presents the opportunity to investigate DNA methylation divergence at both shallow and deeper timescales (0.380-1.4 My). In contrast to studies in human populations, but similar to studies in great apes, DNA methylation profiles clearly mirror genetic and geographic structure. Divergence in DNA methylation proceeds fastest in unannotated regions of the genome and slowest in regions of the genome that are likely more constrained at the sequence level (e.g., gene exons). Both heuristic approaches and Ornstein-Uhlenbeck models suggest that DNA methylation levels at a small set of sites have been affected by positive selection, and that this class is enriched in functionally relevant contexts, including promoters, enhancers, and CpG islands. Our results thus indicate that the rate and distribution of DNA methylation changes across the genome largely mirror genetic structure. However, at some CpG sites, DNA methylation levels themselves may have been a target of positive selection, pointing to loci that could be important in connecting sequence variation to fitness-related traits.

Philopatry at the frontier: A demographically driven scenario for the evolution of multilevel societies in baboons (Papio).

The baboons (Papio sp.) exhibit marked interspecies variation in social behavior. The thesis presented here argues, first, that male philopatry is a crucial factor, arguably the crucial factor, underlying the other distinctive features (one-male units, multilevel society) shared by hamadryas and Guinea baboons, but not other species of Papio. The second suggestion is that male philopatry as a population norm was not an adaptation to a particular habitat or set of ecological circumstances but evolved in the common ancestor of hamadryas and Guinea baboons as a response to natural selection in the demographic context peculiar to the frontier of a rapidly expanding population. Other derived features of social structure (male-male tolerance, some facultative female dispersal) subsequently evolved to accommodate male philopatry. The mitochondrial genetic population structure of extant baboons preserves a footprint of the initial expansion of 'modern' Papio. Immediately after the expansion, male-philopatric, multilevel populations with a general physical and behavioral resemblance to Guinea baboons occupied the whole northern hemisphere range of the genus. Behavioral and physical autapomorphies of hamadryas baboons evolved in a subpopulation of this ancestral northern base, in response to a less productive habitat of the Horn of Africa. Subsequently, ancestral olive baboons 'reinvented' male dispersal. They and yellow baboons, another male-dispersing species, then replaced most of the male-philopatric northern populations, by male-driven introgression and nuclear swamping.

Hybridization in human evolution: Insights from other organisms.

During the late Pleistocene, isolated lineages of hominins exchanged genes thus influencing genomic variation in humans in both the past and present. However, the dynamics of this genetic exchange and associated phenotypic consequences through time remain poorly understood. Gene exchange across divergent lineages can result in myriad outcomes arising from these dynamics and the environmental conditions under which it occurs. Here we draw from our collective research across various organisms, illustrating some of the ways in which gene exchange can structure genomic/phenotypic diversity within/among species. We present a range of examples relevant to questions about the evolution of hominins. These examples are not meant to be exhaustive, but rather illustrative of the diverse evolutionary causes/consequences of hybridization, highlighting potential drivers of human evolution in the context of hybridization including: influences on adaptive evolution, climate change, developmental systems, sex-differences in behavior, Haldane's rule and the large X-effect, and transgressive phenotypic variation.

Dopamine pathway is highly diverged in primate species that differ markedly in social behavior.

In the endeavor to associate genetic variation with complex traits, closely related taxa are particularly fruitful for understanding the neurophysiological and genetic underpinnings of species-specific attributes. Similarity to humans has motivated research into nonhuman primate models, yet few studies of wild primates have investigated immediate causal factors of evolutionarily diverged social behaviors. Neurotransmitter differences have been invoked to explain the distinct behavioral suites of two baboon species in Awash, Ethiopia, which differ markedly in social behavior despite evolutionary propinquity. With this natural experiment, we test the hypothesis that genomic regions associated with monoamine neurotransmitters would be highly differentiated, and we identify a dopamine pathway as an outlier, highlighting the system as a potential cause of species-specific social behaviors. Dopamine levels and resultant variation in impulsivity were likely under differential selection in the species due to social system structure differences, with either brash or circumspect social behavior advantageous to secure mating opportunities depending on the social backdrop. Such comparative studies into the causes of the behavioral agendas that create and interact with social systems are of particular interest, and differences in temperament related to boldness and associated with dopamine variation likely played important roles in the evolution of all social, behaviorally complex animals, including baboons and humans.

Morphological variation in the genus Chlorocebus: Ecogeographic and anthropogenically mediated variation in body mass, postcranial morphology, and growth.

OBJECTIVES: Direct comparative work in morphology and growth on widely dispersed wild primate taxa is rarely accomplished, yet critical to understanding ecogeographic variation, plastic local variation in response to human impacts, and variation in patterns of growth and sexual dimorphism. We investigated population variation in morphology and growth in response to geographic variables (i.e., latitude, altitude), climatic variables (i.e., temperature and rainfall), and human impacts in the vervet monkey (Chlorocebus spp.). METHODS: We trapped over 1,600 wild vervets from across Sub-Saharan Africa and the Caribbean, and compared measurements of body mass, body length, and relative thigh, leg, and foot length in four well-represented geographic samples: Ethiopia, Kenya, South Africa, and St. Kitts & Nevis. RESULTS: We found significant variation in body mass and length consistent with Bergmann's Rule in adult females, and in adult males when excluding the St. Kitts & Nevis population, which was more sexually dimorphic. Contrary to Rensch's Rule, although the South African population had the largest average body size, it was the least dimorphic. There was significant, although very small, variation in all limb segments in support for Allen's Rule. Females in high human impact areas were heavier than those with moderate exposures, while those in low human impact areas were lighter; human impacts had no effect on males. CONCLUSIONS: Vervet monkeys appear to have adapted to local climate as predicted by Bergmann's and, less consistently, Allen's Rule, while also responding in predicted ways to human impacts. To better understand deviations from predicted patterns will require further comparative work in vervets.

Comparison of vitamin D metabolites in wild and captive baboons.

Vitamin D adequacy is essential for multiple physiologic processes. With limited exposure to sunlight for vitamin D3 synthesis, captive primates are supplemented with vitamin D3 (cholecalciferol). Vitamin D metabolite data from wild primates living indigenously could suggest optimum levels. The purpose of this study was to: 1) to explore whether baboons, a speciose genus whose members have significant exposed skin, coat color variation and wide geographical distribution, mirrors the skin pigmentation-vitamin D relationship found in humans; 2) compare vitamin D metabolite levels in wild and captive members of the same or similar baboon species; and 3) apply a recently developed method currently used in humans for measuring multiple vitamin D metabolites as a panel to explore if/how these metabolites can inform us on vitamin D sufficiency. Serum samples from males of three baboon species in the wild: Papio anubis (olive baboon, dark exposed skin), P. cynocephalus (yellow baboon, brown exposed skin), and P. hamadryas (hamadryas baboon, pink exposed skin), were compared with vitamin D supplemented captive olive baboons with sun exposure. Liquid chromatography/tandem mass spectrometry (LC/MS/MS) measured vitamin D and its main metabolites. Cholecalciferol, 25 hydroxyvitamin D2&3 (25(OH)D2&3 ), and 24,25 dihydroxyvitamin D2&3 (24,25(OH)2 D2&3 ), showed significant differences by species. The levels of cholecalciferol due to supplements in the captive olive baboons did not convert to higher 25(OH)D3 while the wild olive baboons exhibited the lowest levels for both cholecalciferol and 25(OH)D3 . Further metabolic conversion of 25(OH)D3 to 24,25(OH)2 D3 indicated that all baboons had more similar conversion ratios and these were within the same range found for humans that are depicted as having adequate vitamin D levels. This study provided evidence that exposed skin color does influence vitamin D3 levels, with lower levels in darker skinned species, but these differences are eliminated in the downstream metabolite conversion indicating strong regulatory control.

Zoonotic Potential of Simian Arteriviruses.

Wild nonhuman primates are immediate sources and long-term reservoirs of human pathogens. However, ethical and technical challenges have hampered the identification of novel blood-borne pathogens in these animals. We recently examined RNA viruses in plasma from wild African monkeys and discovered several novel, highly divergent viruses belonging to the family Arteriviridae. Close relatives of these viruses, including simian hemorrhagic fever virus, have caused sporadic outbreaks of viral hemorrhagic fever in captive macaque monkeys since the 1960s. However, arterivirus infection in wild nonhuman primates had not been described prior to 2011. The arteriviruses recently identified in wild monkeys have high sequence and host species diversity, maintain high viremia, and are prevalent in affected populations. Taken together, these features suggest that the simian arteriviruses may be "preemergent" zoonotic pathogens. If not, this would imply that biological characteristics of RNA viruses thought to facilitate zoonotic transmission may not, by themselves, be sufficient for such transmission to occur.

A Darwinian species definition and its implications.

A review of the vast literature on the epistemology and ontology of "species" is far beyond the capacity of both the writer and the length-allotment of this essay, limiting it to a somewhat dogmatic presentation of personal opinions, few of them original. Also prohibited by the prescribed word limit is an account of species concepts considered but not adopted; in many cases, their omission does not do justice to their intellectual content.

Male-driven grooming bouts in mixed-sex dyads of Kinda baboons (Papio kindae).

The behavior of the Central African Kinda baboon (Papio kindae) is not well documented. Having previously noted distinctive grooming behavior in several Kinda baboon populations, we investigated the topic more systematically in the Kafue National Park, Zambia. We recorded the duration and details of male-female dyadic interactions (approaches, withdrawals and time spent grooming) in the early morning and late afternoon. Such interactions were more often initiated by the male and terminated by the female partner. The male groomed the female more often, and longer, than she groomed him, regardless of the female's reproductive state or the presence of an infant. The bias towards male grooming was stronger in morning than evening interactions. These behaviors, whose function is not immediately obvious, and which are unlike those previously reported in baboons, further exemplify the distinctiveness of the taxon.

Genome-wide coancestry reveals details of ancient and recent male-driven reticulation in baboons.

Baboons (genus Papio ) are a morphologically and behaviorally diverse clade of catarrhine monkeys that have experienced hybridization between phenotypically and genetically distinct phylogenetic species. We used high coverage whole genome sequences from 225 wild baboons representing 19 geographic localities to investigate population genomics and inter-species gene flow. Our analyses provide an expanded picture of evolutionary reticulation among species and reveal novel patterns of population structure within and among species, including differential admixture among conspecific populations. We describe the first example of a baboon population with a genetic composition that is derived from three distinct lineages. The results reveal processes, both ancient and recent, that produced the observed mismatch between phylogenetic relationships based on matrilineal, patrilineal, and biparental inheritance. We also identified several candidate genes that may contribute to species-specific phenotypes. One-Sentence Summary: Genomic data for 225 baboons reveal novel sites of inter-species gene flow and local effects due to differences in admixture.

Genome-wide coancestry reveals details of ancient and recent male-driven reticulation in baboons.

Baboons (genus Papio) are a morphologically and behaviorally diverse clade of catarrhine monkeys that have experienced hybridization between phenotypically and genetically distinct phylogenetic species. We used high-coverage whole-genome sequences from 225 wild baboons representing 19 geographic localities to investigate population genomics and interspecies gene flow. Our analyses provide an expanded picture of evolutionary reticulation among species and reveal patterns of population structure within and among species, including differential admixture among conspecific populations. We describe the first example of a baboon population with a genetic composition that is derived from three distinct lineages. The results reveal processes, both ancient and recent, that produced the observed mismatch between phylogenetic relationships based on matrilineal, patrilineal, and biparental inheritance. We also identified several candidate genes that may contribute to species-specific phenotypes.

A global catalog of whole-genome diversity from 233 primate species.

The rich diversity of morphology and behavior displayed across primate species provides an informative context in which to study the impact of genomic diversity on fundamental biological processes. Analysis of that diversity provides insight into long-standing questions in evolutionary and conservation biology and is urgent given severe threats these species are facing. Here, we present high-coverage whole-genome data from 233 primate species representing 86% of genera and all 16 families. This dataset was used, together with fossil calibration, to create a nuclear DNA phylogeny and to reassess evolutionary divergence times among primate clades. We found within-species genetic diversity across families and geographic regions to be associated with climate and sociality, but not with extinction risk. Furthermore, mutation rates differ across species, potentially influenced by effective population sizes. Lastly, we identified extensive recurrence of missense mutations previously thought to be human specific. This study will open a wide range of research avenues for future primate genomic research.

Genomic signatures of high-altitude adaptation and chromosomal polymorphism in geladas.

Primates have adapted to numerous environments and lifestyles but very few species are native to high elevations. Here we investigated high-altitude adaptations in the gelada (Theropithecus gelada), a monkey endemic to the Ethiopian Plateau. We examined genome-wide variation in conjunction with measurements of haematological and morphological traits. Our new gelada reference genome is highly intact and assembled at chromosome-length levels. Unexpectedly, we identified a chromosomal polymorphism in geladas that could potentially contribute to reproductive barriers between populations. Compared with baboons at low altitude, we found that high-altitude geladas exhibit significantly expanded chest circumferences, potentially allowing for greater lung surface area for increased oxygen diffusion. We identified gelada-specific amino acid substitutions in the alpha-chain subunit of adult haemoglobin but found that gelada haemoglobin does not exhibit markedly altered oxygenation properties compared with lowland primates. We also found that geladas at high altitude do not exhibit elevated blood haemoglobin concentrations, in contrast to the normal acclimatization response to hypoxia in lowland primates. The absence of altitude-related polycythaemia suggests that geladas are able to sustain adequate tissue-oxygen delivery despite environmental hypoxia. Finally, we identified numerous genes and genomic regions exhibiting accelerated rates of evolution, as well as gene families exhibiting expansions in the gelada lineage, potentially reflecting altitude-related selection. Our findings lend insight into putative mechanisms of high-altitude adaptation while suggesting promising avenues for functional hypoxia research.

Mitochondrial evidence for the hybrid origin of the kipunji, Rungwecebus kipunji (Primates: Papionini).

Common baboons (Papio), gelada baboons (Theropithecus) and baboon-mangabeys (Lophocebus) are closely related African papionin monkeys. In 2005, the species Lophocebus kipunji was described from relict montane and submontane forests in Tanzania, based upon a single specimen and observations of living animals. Its initial assignment to Lophocebus was based on its overall morphology, but subsequent genetic studies suggesting that it was sister taxon to common baboons (Papio) led to its generic separation, as Rungwecebus. As a mangabey-like sister-taxon to Papio, Rungwecebus could be interpreted either as an arboreal derivative from a more terrestrial, baboon-like ancestor, or as a survivor of a mangabey-like common ancestor of the Lophocebus-Papio-Theropithecus clade. Here, we present a new, strongly-supported, mitochondrial DNA (mtDNA) phylogeny that includes Papio baboons from populations geographically close to the kipunji. Rather than supporting sister-taxon status, the new phylogeny not only situates the kipunji's mtDNA among Papio haplotypes, it clearly assigns it to a mitochondrial clade including geographically adjacent yellow baboons (Papio cynocephalus). This relationship suggests either that the kipunji is descended from a yellow baboon, and has converged on a mangabey-like morphology, or, much more likely, that it originated by hybridization between Papio cf.cynocephalus females and Lophocebus sp. males, about 0.65 Ma. We believe this to be the first case among mammals in which a natural occurrence of inter-generic hybridization can be shown to have resulted in a new, distinct, long-surviving taxon. More such cases can be anticipated as molecular evidence accumulates.

Alu insertion polymorphisms shared by Papio baboons and Theropithecus gelada reveal an intertwined common ancestry.

BACKGROUND: Baboons (genus Papio) and geladas (Theropithecus gelada) are now generally recognized as close phylogenetic relatives, though morphologically quite distinct and generally classified in separate genera. Primate specific Alu retrotransposons are well-established genomic markers for the study of phylogenetic and population genetic relationships. We previously reported a computational reconstruction of Papio phylogeny using large-scale whole genome sequence (WGS) analysis of Alu insertion polymorphisms. Recently, high coverage WGS was generated for Theropithecus gelada. The objective of this study was to apply the high-throughput "poly-Detect" method to computationally determine the number of Alu insertion polymorphisms shared by T. gelada and Papio, and vice versa, by each individual Papio species and T. gelada. Secondly, we performed locus-specific polymerase chain reaction (PCR) assays on a diverse DNA panel to complement the computational data. RESULTS: We identified 27,700 Alu insertions from T. gelada WGS that were also present among six Papio species, with nearly half (12,956) remaining unfixed among 12 Papio individuals. Similarly, each of the six Papio species had species-indicative Alu insertions that were also present in T. gelada. In general, P. kindae shared more insertion polymorphisms with T. gelada than did any of the other five Papio species. PCR-based genotype data provided additional support for the computational findings. CONCLUSIONS: Our discovery that several thousand Alu insertion polymorphisms are shared by T. gelada and Papio baboons suggests a much more permeable reproductive barrier between the two genera then previously suspected. Their intertwined evolution likely involves a long history of admixture, gene flow and incomplete lineage sorting.

Insights into the evolution of social systems and species from baboon studies.

Baboons, members of the genus Papio, comprise six closely related species distributed throughout sub-Saharan Africa and southwest Arabia. The species exhibit more ecological flexibility and a wider range of social systems than many other primates. This article summarizes our current knowledge of the natural history of baboons and highlights directions for future research. We suggest that baboons can serve as a valuable model for complex evolutionary processes, such as speciation and hybridization. The evolution of baboons has been heavily shaped by climatic changes and population expansion and fragmentation in the African savanna environment, similar to the processes that acted during human evolution. With accumulating long-term data, and new data from previously understudied species, baboons are ideally suited for investigating the links between sociality, health, longevity and reproductive success. To achieve these aims, we propose a closer integration of studies at the proximate level, including functional genomics, with behavioral and ecological studies.

The comparative genomics and complex population history of Papio baboons.

Recent studies suggest that closely related species can accumulate substantial genetic and phenotypic differences despite ongoing gene flow, thus challenging traditional ideas regarding the genetics of speciation. Baboons (genus Papio) are Old World monkeys consisting of six readily distinguishable species. Baboon species hybridize in the wild, and prior data imply a complex history of differentiation and introgression. We produced a reference genome assembly for the olive baboon (Papio anubis) and whole-genome sequence data for all six extant species. We document multiple episodes of admixture and introgression during the radiation of Papio baboons, thus demonstrating their value as a model of complex evolutionary divergence, hybridization, and reticulation. These results help inform our understanding of similar cases, including modern humans, Neanderthals, Denisovans, and other ancient hominins.

Characterization of Wild and Captive Baboon Gut Microbiota and Their Antibiotic Resistomes.

Environmental microbes have harbored the capacity for antibiotic production for millions of years, spanning the evolution of humans and other vertebrates. However, the industrial-scale use of antibiotics in clinical and agricultural practice over the past century has led to a substantial increase in exposure of these agents to human and environmental microbiota. This perturbation is predicted to alter the ecology of microbial communities and to promote the evolution and transfer of antibiotic resistance (AR) genes. We studied wild and captive baboon populations to understand the effects of exposure to humans and human activities (e.g., antibiotic therapy) on the composition of the primate fecal microbiota and the antibiotic-resistant genes that it collectively harbors (the "resistome"). Using a culture-independent metagenomic approach, we identified functional antibiotic resistance genes in the gut microbiota of wild and captive baboon groups and saw marked variation in microbiota architecture and resistomes across habitats and lifeways. Our results support the view that antibiotic resistance is an ancient feature of gut microbial communities and that sharing habitats with humans may have important effects on the structure and function of the primate microbiota. IMPORTANCE Antibiotic exposure results in acute and persistent shifts in the composition and function of microbial communities associated with vertebrate hosts. However, little is known about the state of these communities in the era before the widespread introduction of antibiotics into clinical and agricultural practice. We characterized the fecal microbiota and antibiotic resistomes of wild and captive baboon populations to understand the effect of human exposure and to understand how the primate microbiota may have been altered during the antibiotic era. We used culture-independent and bioinformatics methods to identify functional resistance genes in the guts of wild and captive baboons and show that exposure to humans is associated with changes in microbiota composition and resistome expansion compared to wild baboon groups. Our results suggest that captivity and lifestyle changes associated with human contact can lead to marked changes in the ecology of primate gut communities.

A computational reconstruction of Papio phylogeny using Alu insertion polymorphisms.

BACKGROUND: Since the completion of the human genome project, the diversity of genome sequencing data produced for non-human primates has increased exponentially. Papio baboons are well-established biological models for studying human biology and evolution. Despite substantial interest in the evolution of Papio, the systematics of these species has been widely debated, and the evolutionary history of Papio diversity is not fully understood. Alu elements are primate-specific transposable elements with a well-documented mutation/insertion mechanism and the capacity for resolving controversial phylogenetic relationships. In this study, we conducted a whole genome analysis of Alu insertion polymorphisms unique to the Papio lineage. To complete these analyses, we created a computational algorithm to identify novel Alu insertions in next-generation sequencing data. RESULTS: We identified 187,379 Alu insertions present in the Papio lineage, yet absent from M. mulatta [Mmul8.0.1]. These elements were characterized using genomic data sequenced from a panel of twelve Papio baboons: two from each of the six extant Papio species. These data were used to construct a whole genome Alu-based phylogeny of Papio baboons. The resulting cladogram fully-resolved relationships within Papio. CONCLUSIONS: These data represent the most comprehensive Alu-based phylogenetic reconstruction reported to date. In addition, this study produces the first fully resolved Alu-based phylogeny of Papio baboons.