Complex Evolutionary History With Extensive Ancestral Gene Flow in an African Primate Radiation.

Understanding the drivers of speciation is fundamental in evolutionary biology, and recent studies highlight hybridization as an important evolutionary force. Using whole-genome sequencing data from 22 species of guenons (tribe Cercopithecini), one of the world's largest primate radiations, we show that rampant gene flow characterizes their evolutionary history and identify ancient hybridization across deeply divergent lineages that differ in ecology, morphology, and karyotypes. Some hybridization events resulted in mitochondrial introgression between distant lineages, likely facilitated by cointrogression of coadapted nuclear variants. Although the genomic landscapes of introgression were largely lineage specific, we found that genes with immune functions were overrepresented in introgressing regions, in line with adaptive introgression, whereas genes involved in pigmentation and morphology may contribute to reproductive isolation. In line with reports from other systems that hybridization might facilitate diversification, we find that some of the most species-rich guenon clades are of admixed origin. This study provides important insights into the prevalence, role, and outcomes of ancestral hybridization in a large mammalian radiation.

The Genome of the Endangered Dryas Monkey Provides New Insights into the Evolutionary History of the Vervets.

Genomic data can be a powerful tool for inferring ecology, behavior, and conservation needs of highly elusive species, particularly, when other sources of information are hard to come by. Here, we focus on the Dryas monkey (Cercopithecus dryas), an endangered primate endemic to the Congo Basin with cryptic behavior and possibly <250 remaining adult individuals. Using whole-genome sequencing data, we show that the Dryas monkey represents a sister lineage to the vervets (Chlorocebus sp.) and has diverged from them ∼1.4 Ma with additional bidirectional gene flow ∼750,000-∼500,000 years ago that has likely involved the crossing of the Congo River. Together with evidence of gene flow across the Congo River in bonobos and okapis, our results suggest that the fluvial topology of the Congo River might have been more dynamic than previously recognized. Despite the presence of several homozygous loss-of-function mutations in genes associated with sperm mobility and immunity, we find high genetic diversity and low levels of inbreeding and genetic load in the studied Dryas monkey individual. This suggests that the current population carries sufficient genetic variability for long-term survival and might be larger than currently recognized. We thus provide an example of how genomic data can directly improve our understanding of highly elusive species.

Morphological analysis of new Dryas Monkey specimens from the Central Congo Basin: Taxonomic considerations and an emended diagnosis.

OBJECTIVES: The little known guenon Cercopithecus dryas has a controversial taxonomic history with some recognizing two taxa (C. dryas and C. salongo) instead of one. New adult specimens from the TL2 region of the central Congo Basin allow further assessment of C. dryas morphology and, along with CT scans of the juvenile holotype, provide ontogenetically stable comparisons across all C. dryas and "C. salongo" specimens for the first time. MATERIALS AND METHODS: The skins and skulls of two newly acquired C. dryas specimens, male YPM MAM 16890 and female YPM MAM 17066, were compared to previously described C. dryas and "C. salongo" specimens, along with a broader guenon comparative sample (cranial sample n = 146, dental sample n = 102). Qualitative and quantitative assessments were made on the basis of commonly noted pelage features as well as craniodental characters in the form of shape ratios and multivariate discriminant analyses. RESULTS: All C. dryas specimens, including the TL2 adults, are comparatively small in overall cranial size, have relatively small I1 s, and display tall molar cusps; these osteological characters, along with pelage features, are shared with known "C. salongo" specimens. Discriminant analyses of dental features separate C. dryas/salongo specimens from all other guenons. DISCUSSION: In addition to pelage-based evidence, direct osteological evidence suggests "C. salongo" is a junior synonym of C. dryas. Combined with molecular analyses suggesting C. dryas is most closely related to Chlorocebus spp., we emend the species diagnosis and support its transfer to Chlorocebus or possibly a new genus to reflect its distinctiveness.

A natural history of Chlorocebus dryas from camera traps in Lomami National Park and its buffer zone, Democratic Republic of the Congo, with notes on the species status of Cercopithecus salongo.

The natural history and taxonomic status of two central African primates, Cercopithecus dryas and Cercopithecus salongo have long been in question. Recent studies confirmed that C. dryas is a basal member of the savanna monkey clade, and that it prefers dense undergrowth in lowland rainforest. While these studies advanced our knowledge of this enigmatic species, key aspects of its natural history remain poorly documented. Furthermore, the lack of a field study that documents pelage patterns of both sexes and different age classes of C. dryas has led to a disagreement over the validity of C. salongo as a sister taxon to C. dryas. Using the results of two multi-strata camera trap surveys in Lomami National Park (Democratic Republic of the Congo) and its buffer zone, we conducted a third survey in the understory of degraded forest to accumulate videos of C. dryas/salongo. We used these videos to test the hypothesis that C. dryas and C. salongo are synonymous, and to assess the species' group composition, density, behavior and vocalizations. Camera traps revealed an ontogenetic change in pelage pattern that supports the view that C. salongo is the adult of C. dryas. Videos revealed that adult males develop a blue perineum and scrotum, and a red subcaudal patch, similar to other savanna monkeys. We provide a preliminary assessment of C. dryas' group composition, density, behavior, and vocalizations. This long-overlooked monkey is an exceptional member of the Chlorocebus clade, and all aspects of its biology require further investigation.

Skeletal morphology of the lesula (Cercopithecus lomamiensis) and the evolution of guenon locomotor behavior.

OBJECTIVES: The guenons (tribe Cercopithecini) are a diverse and primarily arboreal radiation of Old World monkeys from Africa. However, preliminary behavioral observations of the lesula (Cercopithecus lomamiensis), a little-known guenon species described in 2012, report it spending substantial amounts of time on the ground. New specimens allow us to present the first description of lesula postcranial morphology and apply a comparative functional morphology approach to supplement our knowledge of its locomotor behavior. MATERIALS AND METHODS: To infer the substrate use preferences of the lesula, 22 postcranial variables correlated with locomotion were assessed in a sample of 151 adult guenon specimens, including two C. lomamiensis. Using multivariate statistical analyses, we predict the amount of time the lesula spends on the ground relative to the comparative sample. RESULTS: Results suggest that the lesula spends nearly half its time on the ground, and the two available individuals were classified as semiterrestrial and terrestrial with strong support. Comparisons with two outgroup cercopithecid taxa (Colobus guereza and Macaca mulatta) demonstrate that, as a group, guenons retain signals of a generalized, semiterrestrially adapted postcranium compared to specialized arboreal cercopithecids. DISCUSSION: These results corroborate preliminary behavioral observations of the lesula as a semiterrestrial to terrestrial primate and imply multiple evolutionary transitions in substrate use among the guenon radiation. A broader view of cercopithecoid evolution suggests that a semiterrestrial ancestor for extant guenons is more parsimonious than an arboreal one, indicating that the arboreal members of the group are probably recently derived from a more semiterrestrial ancestor.

The efficacy of sex-chromosomal markers in studies of Cercopithecus hybridization: Discovery of a captive hybrid and applications in wild populations.

We demonstrate the utility of previously described molecular methods for identifying hybrid Cercopithecus monkeys. Using phylogenetic analyses and DNA sequence comparisons at X-chromosomal and Y-chromosomal loci, we have identified a hybrid animal in the Cheyenne Mountain Zoo (USA)--an identification that was not known a priori but was later confirmed by review of zoo records. The molecular techniques employed here are of great use to studies of the genus Cercopithecus because, unlike most mammals, these monkeys frequently form polyspecific associations, and recent deforestation is likely to have driven otherwise low-level hybridization to higher frequencies which may reduce the fitness of threatened populations. Y-chromosomal markers are especially informative because they provide working hypotheses for (1) the primary mechanism of hybridization (i.e., species A males × species B females) and, by extension; (2) the major direction of gene flow.

Camera Traps Uncover the Behavioral Ecology of an Endemic, Cryptic Monkey Species in the Congo Basin.

Guenons are the most diverse clade of African primates, and many species living within the core of the Congo Basin rainforest are still understudied. The recently described guenon species, Cercopithecus lomamiensis, known as lesula, is a cryptic, semi-terrestrial species endemic to the central Congo Basin in the Democratic Republic of the Congo. The recent IUCN Red List Assessment recognizes lesula's risk of extinction in the wild as Vulnerable. The objective of our study was to use camera traps to expand knowledge on the behavioral ecology of lesula. We conducted three systematic, terrestrial camera trap (CT) surveys within Lomami National Park and buffer zone (Okulu: 2013; Losekola: 2014; E15: 2015). We accumulated 598 independent events of lesula over 5960 CT days from 92 CTs. Typical of Cercopithecus species, camera trap videos reveal that lesula has a diurnal activity pattern, birth seasonality, a group size of up to 32 individuals, and social organization with female philopatry and male dispersal. Results also suggest that lesula are highly terrestrial, distinguishing them from other Cercopithecus species, which are mostly arboreal. Our study provides new information about the behavioral ecology of this little-studied primate, generating species-specific knowledge of a threatened species for successful conservation planning.

The history, taxonomy, and geographic origins of an introduced African monkey in the southeastern United States.

The origins and taxonomy of the introduced vervet monkey population in Dania Beach, Florida has been unconfirmed due to a lack of documentation and genetic research. Our goal was to determine the introduction history, species identification, and geographic origins of the monkeys. Through interviews, historical archives, and popular media, we traced the monkeys to an escape from the Dania Chimpanzee Farm in 1948. The facility imported primates from Africa for medical research purposes. Historical archives suggest the monkeys were caught in Sierra Leone. We tested the hypothesis of West African origins using three genetic markers: one mitochondrial DNA gene (cytochrome b) and two fragments from the Y-chromosome, the sex-determining gene and the zinc-finger gene. We ran Bayesian and maximum-likelihood analyses to reconstruct phylogenetic trees. Results from all loci confirmed the species identification is Chlorocebus sabaeus. We found no variation among the sampled individuals and found the cytochrome b haplotype to be a complete match to a C. sabaeus sample from Senegal. Phylogenetic analyses showed strong support for the Dania Beach mitochondrial and Y-chromosome lineages to group within a monophyletic C. sabaeus clade endemic to West Africa. Our study provides critical baseline information to the scientific community about a little-known population of Chlorocebus monkeys that have adapted to a novel environment in the southeastern United States.

Bat Predation by Cercopithecus Monkeys: Implications for Zoonotic Disease Transmission.

The relationship between bats and primates, which may contribute to zoonotic disease transmission, is poorly documented. We provide the first behavioral accounts of predation on bats by Cercopithecus monkeys, both of which are known to harbor zoonotic disease. We witnessed 13 bat predation events over 6.5 years in two forests in Kenya and Tanzania. Monkeys sometimes had prolonged contact with the bat carcass, consuming it entirely. All predation events occurred in forest-edge or plantation habitat. Predator-prey relations between bats and primates are little considered by disease ecologists, but may contribute to transmission of zoonotic disease, including Ebolavirus.

Lesula: a new species of Cercopithecus monkey endemic to the Democratic Republic of Congo and implications for conservation of Congo's central basin.

In June 2007, a previously undescribed monkey known locally as "lesula" was found in the forests of the middle Lomami Basin in central Democratic Republic of Congo (DRC). We describe this new species as Cercopithecus lomamiensis sp. nov., and provide data on its distribution, morphology, genetics, ecology and behavior. C. lomamiensis is restricted to the lowland rain forests of central DRC between the middle Lomami and the upper Tshuapa Rivers. Morphological and molecular data confirm that C. lomamiensis is distinct from its nearest congener, C. hamlyni, from which it is separated geographically by both the Congo (Lualaba) and the Lomami Rivers. C. lomamiensis, like C. hamlyni, is semi-terrestrial with a diet containing terrestrial herbaceous vegetation. The discovery of C. lomamiensis highlights the biogeographic significance and importance for conservation of central Congo's interfluvial TL2 region, defined from the upper Tshuapa River through the Lomami Basin to the Congo (Lualaba) River. The TL2 region has been found to contain a high diversity of anthropoid primates including three forms, in addition to C. lomamiensis, that are endemic to the area. We recommend the common name, lesula, for this new species, as it is the vernacular name used over most of its known range.

X-chromosomal window into the evolutionary history of the guenons (Primates: Cercopithecini).

Molecular studies of the guenons suggest that the arboreal Cercopithecus species form a monophyletic group within the tribe Cercopithecini. However, the evolutionary relationships among these arboreal congeners remain poorly resolved. The present work marks the first attempt to reconstruct the history of this group through the phylogenetic analysis of long nuclear sequences. We surveyed 19 guenons and seven outgroup taxa for a approximately 9.3kb fragment of X-chromosomal DNA homologous to a portion of human Xq13.3. Parsimony and maximum likelihood analyses of these sequences consistently recover two strongly-supported patterns within the arboreal Cercopithecus clade: (1) a clustering of members of the cephus and mitis species groups, and (2) a monophyletic aggregate including the mona, neglectus, and diana species groups. Although guenons occasionally hybridize in the wild, interbreeding forms of different species groups do not cluster together as sister-taxa in the X-chromosomal tree, suggesting that the two clades inferred here are not reticulate patterns due to recent gene flow. These clades are most likely the result of either ancestral hybridization or true phylogenetic history. We advocate the latter explanation because the same two aggregates (cephus/mitis and mona/neglectus/diana) are recovered, albeit with weak support, by a number of earlier analyses. Finally, X-chromosomal divergence dates are estimated for a number of nodes in the guenon radiation. The divergence of guenon and papionin lineages at 11.5 (+/-1.3) MYA appears to be a particularly robust estimate since it is inferred from both mitochondrial and X-chromosomal studies, each using different fossil calibration points.