New mitogenomic lineages in Papio baboons and their phylogeographic implications.

OBJECTIVES: Incomplete and/or biased sampling either on a taxonomic or geographic level can lead to delusive phylogenetic and phylogeographic inferences. However, a complete taxonomic and geographical sampling is often and for various reasons impossible, particularly for widespread taxa such as baboons (Papio spp.). Previous studies on baboon phylogeography identified several sampling gaps, some of which we fill by investigating additional material including samples from museum specimens. MATERIALS AND METHODS: We generated 10 new mitochondrial genomes either via conventional PCR and subsequent Sanger sequencing from two blood samples or via high-throughput shotgun sequencing from degraded DNA extracted from eight museum specimens. Phylogenetic relationships and divergence times among baboon lineages were determined using maximum-likelihood and Bayesian inferences. RESULTS: We identified new mitochondrial lineages in baboons from Central Africa (Chad, the Central African Republic), from the Mahale, and the Udzungwa Mountains (Tanzania), with the latter likely representing a case of mitochondrial capture from sympatric kipunjis (Rungwecebus kipunji). We also found that the mitochondrial clades of olive baboons found in Ivory Coast and Tanzania extend into Niger and the Democratic Republic of Congo, respectively. Moreover, an olive baboon from Sierra Leone carries a mitochondrial haplotype usually found in Guinea baboons, suggesting gene flow between these two species. DISCUSSION: The extension of the geographic sampling by including samples from areas difficult to visit or from populations that are most likely extirpated has improved the geographic and temporal resolution of the mitochondrial phylogeny of baboons considerably. Our study also shows the great value of museum material for genetic analyses even when DNA is highly degraded.

Ecological niche modeling of the genus Papio.

OBJECTIVE: Ecological niche modeling (ENM) has been used to assess how abiotic variables influence species distributions and diversity. Baboons are broadly distributed throughout Africa, yet the degree of climatic specialization is largely unexplored for individual taxa. Also, the influence of climate on baboon phylogenetic divergence is unknown. In this study, we constructed ENMs to investigate how niches vary across Papio species to understand how climatic variables have influenced their biogeography and mode of speciation. MATERIALS AND METHODS: We used Maxent to generate ENMs by collating locality data for six Papio species and climate information from WorldClim. In addition, we examined the degree of niche overlap among all possible pairs of taxa, which can provide insight into patterns of species diversity. Lastly, we conducted a Mantel test to assess the relationship between niche overlap and estimated time since divergence. RESULTS: Our models performed moderately to extremely well, with a mean area under the curve value of 0.868. The species with the best models include P. papio and P. kindae, whereas P. hamadryas had the poorest models. We found that most species pairs exhibited significantly different niches. Lastly, we found no significant correlation between niche overlap and divergence times. DISCUSSION: Niche models had good predictive power, which indicates Papio species distributions are correlated with climatic variables to varying degrees. Significantly little niche overlap and incomplete geographic boundaries suggests these models generally support a parapatric speciation scenario for the genus Papio.

Alu Insertion Polymorphisms as Evidence for Population Structure in Baboons.

Male dispersal from the natal group at or near maturity is a feature of most baboon (Papio) species. It potentially has profound effects upon population structure and evolutionary processes, but dispersal, especially for unusually long distances, is not readily documented by direct field observation. In this pilot study, we investigate the possibility of retrieving baboon population structure in yellow (Papio cynocephalus) and kinda (Papio kindae) baboons from the distribution of variation in a genome-wide set of 494 Alu insertion polymorphisms, made available via the recently completed Baboon Genome Analysis Consortium. Alu insertion variation in a mixed population derived from yellow and olive (Papio anubis) baboons identified each individual's proportion of heritage from either parental species. In an unmixed yellow baboon population, our analysis showed greater similarity between neighboring than between more distantly situated groups, suggesting structuring of the population by male dispersal distance. Finally (and very provisionally), an unexpectedly sharp difference in Alu insertion frequencies between members of neighboring social groups of kinda baboons suggests that intergroup migration may be more rare than predicted in this little known species.

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.

Pleistocene aridification cycles shaped the contemporary genetic architecture of Southern African baboons.

Plio-Pleistocene environmental change influenced the evolutionary history of many animal lineages in Africa, highlighting key roles for both climate and tectonics in the evolution of Africa's faunal diversity. Here, we explore diversification in the southern African chacma baboon Papio ursinus sensu lato and reveal a dominant role for increasingly arid landscapes during past glacial cycles in shaping contemporary genetic structure. Recent work on baboons (Papio spp.) supports complex lineage structuring with a dominant pulse of diversification occurring 1-2Ma, and yet the link to palaeoenvironmental change remains largely untested. Phylogeographic reconstruction based on mitochondrial DNA sequence data supports a scenario where chacma baboon populations were likely restricted to refugia during periods of regional cooling and drying through the Late Pleistocene. The two lineages of chacma baboon, ursinus and griseipes, are strongly geographically structured, and demographic reconstruction together with spatial analysis of genetic variation point to possible climate-driven isolating events where baboons may have retreated to more optimum conditions during cooler, drier periods. Our analysis highlights a period of continuous population growth beginning in the Middle to Late Pleistocene in both the ursinus and the PG2 griseipes lineages. All three clades identified in the study then enter a state of declining population size (Nef) through to the Holocene; this is particularly marked in the last 20,000 years, most likely coincident with the Last Glacial Maximum. The pattern recovered here conforms to expectations based on the dynamic regional climate trends in southern Africa through the Pleistocene and provides further support for complex patterns of diversification in the region's biodiversity.

Neutral nuclear variation in Baboons (genus Papio) provides insights into their evolutionary and demographic histories.

Baboons (genus Papio) are distributed over most of sub-Saharan Africa and in the southern portion of the Arabian Peninsula. Six distinct morphotypes, with clearly defined geographic distributions, are recognized (the olive, chacma, yellow, Guinea, Kinda, and hamadryas baboons). The evolutionary relationships among baboon forms have long been a controversial issue. Phylogenetic analyses based on mitochondrial DNA sequences revealed that the modern baboon morphotypes are mitochondrially paraphyletic or polyphyletic. The discordance between mitochondrial lineages and morphology is indicative of extensive introgressive hybridization between ancestral baboon populations. To gain insights into the evolutionary relationships among morphotypes and their demographic history, we performed an analysis of nuclear variation in baboons. We sequenced 13 noncoding, putatively neutral, nuclear regions, and scored the presence/absence of 18 polymorphic transposable elements in a sample of 45 baboons belonging to five of the six recognized baboon forms. We found that the chacma baboon is the sister-taxon to all other baboons and the yellow baboon is the sister-taxon to an unresolved northern clade containing the olive, Guinea, and hamadryas baboons. We estimated that the diversification of baboons occurred entirely in the Pleistocene, the earliest split dating ∼1.5 million years ago, and that baboons have experienced relatively large and constant effective population sizes for most of their evolutionary history (∼30,000 to 95,000 individuals).

Ectocranial suture fusion in primates: pattern and phylogeny.

Patterns of ectocranial suture fusion among Primates are subject to species-specific variation. In this study, we used Guttman Scaling to compare modal progression of ectocranial suture fusion among Hominidae (Homo, Pan, Gorilla, and Pongo), Hylobates, and Cercopithecidae (Macaca and Papio) groups. Our hypothesis is that suture fusion patterns should reflect their evolutionary relationship. For the lateral-anterior suture sites there appear to be three major patterns of fusion, one shared by Homo-Pan-Gorilla, anterior to posterior; one shared by Pongo and Hylobates, superior to inferior; and one shared by Cercopithecidae, posterior to anterior. For the vault suture pattern, the Hominidae groups reflect the known phylogeny. The data for Hylobates and Cercopithecidae groups is less clear. The vault suture site termination pattern of Papio is similar to that reported for Gorilla and Pongo. Thus, it may be that some suture sites are under larger genetic influence for patterns of fusion, while others are influenced by environmental/biomechanic influences.

Calibrated tree priors for relaxed phylogenetics and divergence time estimation.

The use of fossil evidence to calibrate divergence time estimation has a long history. More recently, Bayesian Markov chain Monte Carlo has become the dominant method of divergence time estimation, and fossil evidence has been reinterpreted as the specification of prior distributions on the divergence times of calibration nodes. These so-called "soft calibrations" have become widely used but the statistical properties of calibrated tree priors in a Bayesian setting hashave not been carefully investigated. Here, we clarify that calibration densities, such as those defined in BEAST 1.5, do not represent the marginal prior distribution of the calibration node. We illustrate this with a number of analytical results on small trees. We also describe an alternative construction for a calibrated Yule prior on trees that allows direct specification of the marginal prior distribution of the calibrated divergence time, with or without the restriction of monophyly. This method requires the computation of the Yule prior conditional on the height of the divergence being calibrated. Unfortunately, a practical solution for multiple calibrations remains elusive. Our results suggest that direct estimation of the prior induced by specifying multiple calibration densities should be a prerequisite of any divergence time dating analysis.

Introgressive hybridization in southern African baboons shapes patterns of mtDNA variation.

Species, as main evolutionary units have long been considered to be morphological entities with limited hybridization potential. The occurrence of taxa which maintain morphological distinctness despite extensive hybridization is an interesting phenomenon. To understand the evolution of these taxa, descriptions of contemporary morphological and genetic variation are essential, also to reconstruct sound phylogenies. Baboons, with their wide geographic range, variant morphotypes, and extensive hybridization offer an intriguing model for those studies. We focus on the complex situation in southern Africa that, in contrast to east Africa, has been neglected in terms of baboon hybridization history. We aim to clarify the distribution and identify possible overlapping zones between different, previously described mitochondrial (mt) DNA clades of baboons that do not match with the ranges of traditionally recognized species. On the basis of the widespread sampling and mitochondrial cytochrome b gene sequencing, we constructed a phylogenetic tree that separates representatives of the two southern African baboon species, yellow and chacma baboons, into six clades: southern, northern and eastern chacmas, Kinda baboons and southern and Luangwa yellow baboons. The ranges of the chacma clades come into close contact or overlap in two regions in the Republic of South Africa and Namibia. Our phylogenetic reconstruction reveals mitochondrial paraphyly for chacma and yellow baboons, which is probably caused by introgressive hybridization and subsequent nuclear swamping, whereby males of the chacma morphotype population from the south invaded the yellow morphotype population in the north bringing their morphotype into a population that maintained its yellow baboon mtDNA.

Having a Jolly good time--together! Evolution by cooperative interaction.

What's in a word? "Hybridization" is easy to say (for professors) but carries surprisingly deep meaning from an evolutionary viewpoint. Cliff Jolly's research contributions have included important work and thought on the nature of baboon diversity and interactions. Hybridization among baboon subspecies reflects compatible genes for many different physical and behavioral traits, essentially all traits, each of them complex. Modern developmental genetics has shown that a few general principles characterize the phenogenetic logic by which genes assemble embryos and maintain the complex traits and abilities of organisms, including behavior. How cooperative viability is maintained while complex adaptive traits evolve and populations diverge is a question we can begin to answer more definitively than has been possible before. A careful look leads us to challenge the nature of the Darwinian explanations that have been the standard for more than a century.

Is the new primate genus rungwecebus a baboon?

BACKGROUND: In 2005, a new primate species from Tanzania, the kipunji, was described and recognized as a member of the mangabey genus Lophocebus. However, molecular investigations based upon a number of papionins, including a limited sample of baboons of mainly unknown geographic origin, identified the kipunji as a sister taxon to Papio and not as a member of Lophocebus. Accordingly, the kipunji was separated into its own monotypic genus, Rungwecebus. METHODOLOGY/PRINCIPAL FINDINGS: We compare available mitochondrial and nuclear sequence data from the voucher specimen of Rungwecebus to other papionin lineages, including a set of geographically proximal (parapatric) baboon samples. Based on mitochondrial sequence data the kipunji clusters with baboon lineages that lie nearest to it geographically, i.e. populations of yellow and chacma baboons from south-eastern Africa, and thus does not represent a sister taxon to Papio. Nuclear data support a Papio+Rungwecebus clade, but it remains questionable whether Rungwecebus represents a sister taxon to Papio, or whether it is nested within the genus as depicted by the mitochondrial phylogeny. CONCLUSIONS/SIGNIFICANCE: Our study clearly supports a close relationship between Rungwecebus and Papio and might indicate that the kipunji is congeneric with baboon species. However, due to its morphological and ecological uniqueness Rungwecebus more likely represents a sister lineage to Papio and experienced later introgressive hybridization. Presumably, male (proto-)kipunjis reproduced with sympatric female baboons. Subsequent backcrossing of the hybrids with kipunjis would have resulted in a population with a nuclear kipunji genome, but which retained the yellow/chacma baboon mitochondrial genome. Since only one kipunji specimen was studied, it remains unclear whether all members of the new genus have been impacted by intergeneric introgression or rather only some populations. Further studies with additional Rungwecebus samples are necessary to elucidate the complete evolutionary history of this newly-described primate genus.

Inferring Plio-Pleistocene southern African biochronology from facial affinities in Parapapio and other fossil papionins.

Buried in the same South African cave deposits as Australopithecus, fossil papionins have been referred to Parapapio (Pp. whitei, Pp. broomi, Pp. jonesi, Pp. antiquus), Papio (P. izodi, P. angusticeps, P. h. robinsoni), Theropithecus (e.g., T. darti), Gorgopithecus, or Dinopithecus on the basis of postcanine tooth size and descriptive morphology of the muzzle. The morphological patterns of variation that these papionins demonstrate can help to place the Australopithecus fossils into a biochronological context and provide valuable information for reconstructing regional Plio-Pleistocene turnover. To document these patterns of variation across fossil-bearing sites, we explore morphometric affinities within Parapapio, and between Parapapio and other Plio-Pleistocene taxa (Dinopithecus ingens, Papio angusticeps, Papio izodi, and Theropithecus darti) by analyzing a sample of interlandmark distances derived from 3-D coordinate data of the most complete fossil papionin specimens available. Bivariate and multivariate analyses show that Pp. whitei exhibits as much variation between sites and between individuals as Pp. broomi and Pp. whitei combined. Diversity in Parapapio at Makapansgat and Sterkfontein may suggest substantial time depth to the caves. Theropithecus darti, Dinopithecus ingens, Papio angusticeps, Pp. whitei from Bolt's Farm (BF 43), and Pp. jonesi from Sterkfontein (STS 565) differ considerably from one another. Other Parapapio specimens across sites form a separate cluster with P. izodi from Taung, suggesting a Pliocene age for this site.

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.

Ontogeny and homoplasy in the papionin monkey face.

Recent molecular research has provided a consistent estimate of phylogeny for the living papionin monkeys (Cercocebus, Lophocebus, Macaca, Mandrillus, Papio, and Theropithecus). This phylogeny differs from morphological phylogenies regarding the relationships of the mangabeys (Cercocebus and Lophocebus) and baboons (Mandrillus, Papio, and Theropithecus). Under the likely assumption that the molecular estimate is correct, the incongruence between the molecular and morphological data sets indicates that the latter include numerous homoplasies. Knowledge of how these homoplasies emerge through development is important for understanding the morphological evolution of the living papionins, and also for reconstructing the phylogenetic relationships and adaptations of their fossil relatives. Accordingly, we have used geometric morphometric techniques and the molecular phylogeny to investigate the ontogeny of a key area of morphological homoplasy in papionins, the face. Two analyses were carried out. The first compared allometric vectors of Cercocebus, Lophocebus, Macaca, Mandrillus, and Papioto determine which of the facial resemblances among the genera are homoplasic and which are plesiomorphic. The second analysis focused on early post-natal facial form in order to establish whether the facial homoplasies exhibited by the adult papionins are to some degree present early in the post-natal period or whether they develop only later in ontogeny. The results of our analyses go some way to resolving the debate over which papionin genera display homoplasic facial similarities. They strongly suggest that the homoplasic facial similarities are exhibited by Mandrillus and Papio and not by Cercocebus and Lophocebus, which share the putative primitive state with Macaca. Our results also indicate that Mandrillus and Papio achieve their homoplasic similarities in facial form not through simple extension of the ancestral allometric trajectory but through a combination of an extension of allometry into larger size ranges and a change in direction of allometry away from the ancestral trajectory. Thus, the face of Mandrillus is not simply a hypermorphic version of the face of its sister taxon, Cercocebus, and the face of Papio is not merely a scaled-up version of the face of its sister taxon, Lophocebus. Lastly, our results show that facial homoplasy is not restricted to adult papionins; it is also manifest in infant and juvenile papionins. This suggests that the homoplasic facial similarities between Mandrillus and Papio are unlikely to be a result of sexual selection.

Skeletal and dental morphology supports diphyletic origin of baboons and mandrills.

Numerous biomolecular studies from the past 20 years have indicated that the large African monkeys Papio, Theropithecus, and Mandrillus have a diphyletic relationship with different species groups of mangabeys. According to the results of these studies, mandrills and drills (Mandrillus) are most closely related to the torquatus-galeritus group of mangabeys placed in the genus Cercocebus, whereas baboons (Papio) and geladas (Theropithecus) are most closely related to the albigena-aterrimus mangabeys, now commonly placed in the genus Lophocebus. However, there has been very little morphological evidence linking mandrills on the one hand and baboons and geladas on the other with different groups of mangabeys. In a study of mangabey locomotion and skeletal anatomy, we have identified features of the postcranial skeleton and the dentition that support the molecular phylogeny and clearly link mandrills with Cercocebus and Papio with Lophocebus. Moreover, the features linking Cercocebus and Mandrillus accord with ecological studies of these species indicating that these two genera are a cryptic clade characterized by unique adaptations for gleaning insects, hard nuts, and seeds from the forest floor.

A comparison of TSPY genes from Y-chromosomal DNA of the great apes and humans: sequence, evolution, and phylogeny.

The genes for testis-specific protein Y (TSPY) were sequenced from chimpanzee (Pan troglodytes), gorilla (Gorilla gorilla), orangutan (Pongo pygmaeus), and baboon (Papio hamadryas). The sequences were compared with each other and with the published human sequence. Substitutions were detected at 144 of the 755 nucleotide positions compared. In overviewing five sequences, one deletion in human, four successive nucleotide insertions in orangutan, and seven deletions/insertions in baboon sequence were noted. The present sequences differed from that of human by 1.9% (chimpanzee), 4.0% (gorilla), 8.2% (orangutan), and 16.8% (baboon), respectively. The phylogenetic tree constructed by the neighbor-joining method suggests that human and chimpanzee are more closely related to each other than either of them is to gorilla, and this result is also supported by maximum likelihood and strict consensus maximum parsimony trees. The number of nucleotide substitutions per site between human and chimpanzee, gorilla, and orangutan for TSPY intron were 0.024, 0.048, and 0.094, respectively. The rates of nucleotide substitutions per site per year were higher in the TSPY intron than in the TSPY exon, and higher in the TSPY intron than in the ZFY (Zinc Finger Y) intron in human and apes.

X-linked glucose-6-phosphate dehydrogenase (G6PD) and autosomal 6-phosphogluconate dehydrogenase (6PGD) polymorphisms in baboons.

Electrophoretic polymorphisms of glucose-6-phosphate dehydrogenase (G6PD) and 6-phosphogluconate dehydrogenase (6PGD) were examined in captive colonies of five subspecies of baboons (Papio hamadryas). Phenotype frequencies and family data verified the X-linked inheritance of the G6PD polymorphism. Insufficient family data were available to confirm autosomal inheritance of the 6PGD polymorphism, but the electrophoretic patterns of variant types (putative heterozygotes) suggested the codominant expression of alleles at an autosomal locus. Implications of the G6PD polymorphism are discussed with regard to its utility as a marker system for research on X-chromosome inactivation during baboon development and for studies of clonal cell proliferation and/or cell selection during the development of atherosclerotic lesions in the baboon model.

Mannose-6-phosphate isomerase polymorphism in baboon erythrocytes.

Although erythrocytic mannose-6-phosphate isomerase (MPI) has been reported to be undetectable in mammals, we have demonstrated that sufficient activity is present in some species to enable its electrophoretic analysis. A survey of MPI from 2656 baboons revealed four allelic isozymes which segregated codominantly in pedigreed families. The gene frequencies differed significantly among five subspecies of baboons. However, the MPI*C allele had the highest frequency in all subspecies, ranging from 0.830 to 1.000. MPI phenotypes from erythrocytes and liver of the same individual were identical, indicating that the erythrocytic enzyme is specified by the same gene locus as the liver enzyme.