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A new species of fossil guenon (Cercopithecini, Cercopithecidae) from the Early Pleistocene Lower Ngaloba Beds, Laetoli, Tanzania
Abstract
The living guenons (Cercopithecini, Cercopithecidae) are speciose and widely distributed across sub-Saharan Africa but are poorly represented in the fossil record. In addition, the craniodental and skeletal similarity of the guenons has hampered the identification of fragmentary material, likely obscuring the taxonomic diversity represented in the fossil record. Here, we describe a new fossil guenon specimen (LAET 75-3703) from the Lower Ngaloba Beds, Laetoli in Tanzania, dated to ∼1.7–1.2 Ma and preserving the lower face and mandible. Comparison to 278 extant guenon specimens, representing all six extant genera, identified several informative traits for distinguishing between the morphologically similar Chlorocebus and Cercopithecus, and these support the attribution of LAET 75-3703 to Chlorocebus. A discriminant function analysis of seven craniodental indices on a subsample of Chlorocebus and Cercopithecus was robust with an overall correct classification rate of 80.4%, and it classified LAET 75-3703 as a member of Chlorocebus with a posterior probability of 92.7%. LAET 75-3703 shares with Chlorocebus the presence of small ‘thumbprint’ depressions on the maxilla; a tall, narrow, and diamond-shaped nasal aperture; a relatively longer and shallower face; relatively buccolingually broader molars; and a shallow mandible that decreases in depth posteriorly. In addition, LAET 75-3703 is distinguished from all extant guenons, including other species of Chlorocebus, in having a very small P³ relative to M¹ area. As such, LAET 75-3703 is assigned to a new species, Chlorocebus ngedere sp. nov. This specimen represents the first cercopithecin from Laetoli, as well as the oldest fossil cercopithecin confidently attributed to a modern genus.
... The lower Ngaloba Beds from Laetoli, Tanzania, have yielded a recently named species of guenon, Chlorocebus ngedere ($1.7-1.2 Ma; Arenson et al., 2022). There are also a handful of isolated teeth from Olduvai/Oldupai Gorge and Loboi (Leakey, 1988). ...
... Depending on the researcher's definition of semi-terrestrial, some species of cercopithecin have been considered as both arboreal and semi-terrestrial (e.g., Cardini & Elton, 2008vs. Arenson et al., 2020, or both semi-terrestrial and terrestrial (e.g., Arenson et al., 2020and Arenson et al., 2022vs. Gebo & Sargis, 1994and Cardini & Elton, 2008. ...
Objectives
The goals of this study were to describe and interpret two new fossil assemblages of cercopithecin monkeys ( n = 328), one from the Faro Daba beds (ca. 100,000 years) and the other one from the Chai Baro beds (>158,000 years old), in the Afar Rift of Ethiopia.
Materials and Methods
We describe the two assemblages and compare them to extant cercopithecin species and the smaller fossil assemblage from Asbole, Ethiopia (ca. 600 ka). We use a population‐based approach to the taxonomy given the unusually large number of specimens. Craniodental and postcranial anatomy are presented. Evidence of locomotor habitus is described and evaluated in a framework of hybridization and postcranial plasticity.
Results
We attribute all cercopithecin specimens from both beds to cf. Chlorocebus and conclude that the Faro Daba and Chai Baro assemblages likely sample single species at each time horizon. Subtle differences between the two assemblages, mostly in postcranial morphology, are insufficient to justify separation at the species level.
Discussion
The large sample sizes and unique preservational aspects of these two assemblages open a new window into the recent evolution of guenons. Our data indicate that these fossil populations may be ancestral to the cercopithecins currently living in the Afar region of Ethiopia.
... However, Chlorocebus ngederethe, the oldest fossil cercopithecin classified to the genus Chlorocebus, is characterized by six infraorbital foramina on the left and five on the right positioned just below the inferior plane of the orbit (Arenson et al., 2022). It is not known whether the ancestors of modern Chlorocebus were characterized by a greater number of infraorbital foramina than other cercopithecids, or whether this is the result of intraspecific variability. ...
Knowledge of the nonhuman primate morphology and anatomy related to craniofacial mechanoreception is essential for a fundamental understanding of the incidents that have occurred during the evolution of craniofacial features. The present study focuses on the variability in the number of infraorbital foramina and associated anatomical structures such as the infraorbital canal (IOC) and the infraorbital groove (IOG), as they are considered to play an important role in the behavioral ecology of these animals. A total of 19 skulls of Chlorocebus aethiops were analyzed. The number of infraorbital foramina was assessed macroscopically using a magnifying glass and a small diameter probe. Three dimensional (3D) projections and morphometric analysis of the infraorbital foramina, IOCs, and IOGs were performed using microcomputed tomography (micro-CT) for two skulls that represent one of the most common morphological types. Regardless of sex and body side, the most common morphological type observed in the studied species is the presence of three infraorbital foramina. The IOC takes a funnel or pinched shape. 3D projections were made to assess the course of the infraorbital vascular and nerve bundles in selected individuals. The results indicate a high morphological diversity within the species, although there appears to be a consistent distribution pattern of infraorbital neurovascular bundles in species of the Cercopithecidae family. The use of X-ray micro-CT allowed 3D visualization of the maxillary region to determine the variability of the infraorbital foramina and to track the division of the infraorbital neurovascular bundle in the case of the most common macroscopic expression of the number of the infraorbital foramen in C. aethiops, as well as the morphometric of the IOCs and IOGs which are related to mechanoreception of the primate's snout.
Despite recent advances in chronometric techniques (e.g., Uranium-Lead [U-Pb], cosmogenic nuclides, electron spin resonance spectroscopy [ESR]), considerable uncertainty remains regarding the age of many Plio-Pleistocene hominin sites, including several in South Africa. Consequently, biochronology remains important in assessments of Plio-Pleistocene geochronology and provides direct age estimates of the fossils themselves. Historically, cercopithecid monkeys have been among the most useful taxa for biochronology of early hominins because they are widely present and abundant in the African Plio-Pleistocene record. The last major studies using cercopithecids were published over 30 y ago. Since then, new hominin sites have been discovered, radiometric age estimates have been refined, and many changes have occurred in cercopithecid taxonomy and systematics. Thus, a biochronological reassessment using cercopithecids is long overdue. Here, we provide just such a revision based on our recent study of every major cercopithecid collection from African Plio-Pleistocene sites. In addition to correlations based on shared faunal elements, we present an analysis based on the dentition of the abundant cercopithecid Theropithecus oswaldi , which increases in size in a manner that is strongly correlated with geological age ( r ² ∼0.83), thereby providing a highly accurate age-estimation tool not previously utilized. In combination with paleomagnetic and U-Pb data, our results provide revised age estimates and suggest that there are no hominin sites in South Africa significantly older than ∼2.8 Ma. Where conflicting age estimates exist, we suggest that additional data are needed and recall that faunal estimates have ultimately proved reliable in the past (e.g., the age of the KBS Tuff).
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.
Research Highlights
• Camera trap videos support that two described species, Cercopithecus dryas and Cercopithecus salongo, are conspecific.
• Male dryas monkeys develop a red subcaudal patch, blue perineum, and white caudal ruff that forms an elaborate display, similar to the red, white, and blue displays of savanna monkeys.
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 Eyasi Plateau Paleontological Expedition (EPPE) Laetoli specimen database contains 13716 records of plant and animal fossils (ca. 28248 specimens) collected by EPPE field teams working at Laetoli, Tanzania between 1998 and 2005. This dataset is a digital version of the original hard-copy specimen catalog, and it documents the discovery, stratigraphic provenience and taxonomic diversity of Plio-Pleistocene fauna and flora in northern Tanzania between 4.4 Ma and >200 ka. Laetoli is renowned for the discovery of important hominin fossils, including the lectotype for Australopithecus afarensis, one of our early hominin ancestors, the first record of Paranthropus aethiopicus outside Kenya-Ethiopia, and an early record of our own species Homo sapiens. This database is one of the few publicly available palaeoanthropological fossil datasets and serves as an example for expanding open access to primary fossil occurrence data in palaeoanthropology. The taxonomic identifications appearing in this dataset are the original field identifications and are provisional. Any taxonomic analysis employing this dataset should refer to updated taxonomic identifications published by specialists.
Genomic data can be a powerful tool for inferring ecology, behaviour 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 behaviour and possibly less than 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 around 1.4 million years ago with additional bi-directional 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 recognised. 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 recognised. We thus provide an example of how genomic data can directly improve our understanding of highly elusive species.
Although modern guenons are diverse and abundant in Africa, the fossil record of this group is surprisingly sparse. In 2012 the West Turkana Paleo Project team recovered two associated molar teeth of a small primate from the Pliocene site of Kanapoi, West Turkana, Kenya. The teeth are bilophodont and the third molar lacks a hypoconulid, which is diagnostic for Cercopithecini. The teeth are the same size as those of extant Miopithecus, which is thought to be a dwarfed guenon, as well as a partial mandible preserving two worn teeth, previously recovered from Koobi Fora, Kenya, which was also tentatively identified as a guenon possibly allied with Miopithecus. Tooth size and proportions, as well as analysis of relative cusp size and shearing crest development clearly separate the fossil from all known guenons. Based on the Kanapoi material, we erect a new genus and species, Nanopithecus browni gen. et sp. nov. The small size of the specimen suggests either that dwarfing occurred early in the lineage, or at least twice independently, depending on the relationship of the new species with extant Miopithecus. Further, the distinctive habitat and geographic separation from Miopithecus suggests that the origin of small body size is not uniquely linked to the current habitat of Miopithecus, and possibly that relatives of extant Miopithecus were much more widely distributed in the past. This in turn argues caution in using extant biogeography in models of the origins of at least some guenons.
In recent years, hybridization has gained recognition as an important creative force in primate evolution. The exchange of genetic material between species provides genetic novelty on which evolutionary forces, such as natural selection, may act. The guenon radiation (Tribe Cercopithecini) is known for numerous cases of contemporary hybridization—in the wild and captivity—between broadly sympatric species. Interspecific hybrids are viable, and field studies report fertile hybrid females. Despite being a well-documented phenomenon, hybridization among wild guenons is relatively rare and sporadic. An exception is the long-standing hybridization between Cercopithecus mitis doggetti and C. ascanius schmidti in Gombe National Park, Tanzania, where hybrids comprise a significant proportion of the breeding population. Here, I used mitochondrial loci to conduct a genetic survey of the Gombe population and examine the extent and direction of gene flow between the parental species. I extracted DNA from noninvasive fecal samples of unhabituated individuals (N = 144 individuals) with known phenotype and provenance. All parental phenotypes and hybrid individuals were identified in the field based on species specific pelage colors and patterns. Phylogenetic analyses of DNA sequences from inside and outside the hybrid zone show Gombe’s population of C. mitis doggetti is distinct from neighboring conspecific populations in having mitochondrial DNA of C. ascanius schmidti. All animals surveyed from the hybrid zone have one of two haplotypes of C. ascanius schmidti unique to Gombe. These results provide evidence of asymmetric introgressive hybridization between sympatric guenon species, a likely consequence of colonization patterns of the parental species during range expansions. The spatial distribution patterns of the two haplotypes imply that Gombe is a site of both historic and contemporary hybridization between sympatric guenons. The discovery of gene flow and ongoing hybridization between clearly defined species, ecologically distinct enough to coexist in broad sympatry, provides an ideal system to investigate speciation mechanisms in primate adaptive radiations. © 2018 Springer Science+Business Media, LLC, part of Springer Nature
Vervet monkeys are among the most widely distributed nonhuman primates, show considerable phenotypic diversity, and have long been an important biomedical model for a variety of human diseases and in vaccine research. Using whole-genome sequencing data from 163 vervets sampled from across Africa and the Caribbean, we find high diversity within and between taxa and clear evidence that taxonomic divergence was reticulate rather than following a simple branching pattern. A scan for diversifying selection across taxa identifies strong and highly polygenic selection signals affecting viral processes. Furthermore, selection scores are elevated in genes whose human orthologs interact with HIV and in genes that show a response to experimental simian immunodeficiency virus (SIV) infection in vervet monkeys but not in rhesus macaques, suggesting that part of the signal reflects taxon-specific adaptation to SIV.
Complete mitochondrial (mtDNA) genomes have proved to be useful in reconstructing primate phylogenies with higher resolution and confidence compared to reconstructions based on partial mtDNA sequences. Here, we analyse complete mtDNA genomes of African green monkeys (genus Chlorocebus), a widely distributed primate genus in Africa representing an interesting phylogeographical model for the evolution of savannah species. Previous studies on partial mtDNA sequences revealed nine major clades, suggesting several cases of para- and polyphyly among Chlorocebus species. However, in these studies, phylogenetic relationships among several clades were not resolved, and divergence times were not estimated. We analysed complete mtDNA genomes for ten Chlorocebus samples representing major mtDNA clades to find stronger statistical support in the phylogenetic reconstruction than in the previous studies and to estimate divergence times. Our results confirmed para- and polyphyletic relationships of most Chlorocebus species, while the support for the phylogenetic relationships between the mtDNA clades increased compared to the previous studies. Our results indicate an initial west–east division in the northern part of the Chlorocebus range with subsequent divergence into north-eastern and southern clades. This phylogeographic scenario contrasts with that for another widespread African savannah primate genus, the baboons (Papio), for which a dispersal from southern Africa into East and West Africa was suggested.
We describe a genome reference of the African green monkey or vervet (Chlorocebus aethiops). This member of the Old World monkey (OWM) superfamily is uniquely valuable for genetic investigations of simian immunodeficiency virus (SIV), of which it is the most abundant natural host species, and of a wide range of health-related phenotypes assessed in Caribbean vervets (C. a. sabaeus), whose numbers have expanded dramatically since Europeans introduced small numbers of their ancestors from West Africa during the colonial era. We use the reference to characterize the genomic relationship between vervets and other primates, the intrageneric phylogeny of vervet subspecies, and genome-wide structural variations of a pedigreed C. a. sabaeus population. Through comparative analyses with human and rhesus macaque, we characterize at high resolution the unique chromosomal fission events that differentiate the vervets and their close relatives from most other catarrhine primates, in whom karyotype is highly conserved. We also provide a summary of transposable elements and contrast these with the rhesus macaque and human. Analysis of sequenced genomes representing each of the main vervet subspecies supports previously hypothesized relationships between these populations, which range across most of sub-Saharan Africa, while uncovering high levels of genetic diversity within each. Sequence-based analyses of major histocompatibility complex (MHC) polymorphisms reveal extremely low diversity in Caribbean C. a. sabaeus vervets, as compared to vervets from putatively ancestral West African regions. In the C. a. sabaeus research population we discover the first structural variations that are in some cases predicted to have a deleterious effect; future studies will determine
Significance
The primate subfamily Cercopithecinae represents the most diverse and successful living Old World primate group, with a current distribution throughout Africa and Asia. However, how and when these monkeys dispersed out of Africa is not well understood. This paper is significant in its description of a ∼6.5–8.0 million-y-old fossil guenon from Arabia representing the earliest cercopithecine (and only guenon) yet known outside of Africa. Furthermore, this specimen extends the guenon fossil record by at least 2.3 million y and may represent the earliest known cercopithecine as well. Because Old World monkeys appear to have dispersed out of Africa sometime during the Late Miocene, the Arabian fossils also have implications for dispersal scenarios in Old World monkey biogeography and evolution.
The phylogeny of Old World monkeys has remained unresolved in part because of a lack of resolution in the Cercopithecinae. Competing morphological hypotheses have had Allen's swamp monkey (Allenopithecus nigroviridis) and the talapoins (Miopithecus spp.) as basal branches of either the tribe Cercopithecini or the tribe Papionini. Previous molecular analyses have not adequately addressed the issue. To better understand the evolutionary history of these primates, we sequenced and subjected to phylogenetic analysis ∼3.1 kb of 2 loci (TSPY and SRY) from the non-recombining portion of the Y-chromosome. Individuals from the genera Allenopithecus, Miopithecus, Erythrocebus, Chlorocebus, and Cercopithecus were surveyed and their sequences compared with those previously published for the Papionini and Colobinae. The results suggest Allenopithecus and Miopithecus are more closely related to the Cercopithecini than Papionini. Our data also support the hypothesis that within the Cercopithecini, Erythrocebus and Chlorocebus share a close evolutionary relationship, distinct from the other members of the tribe.
Mumba Rockshelter in northern Tanzania presents one of the richest and most complete archaeological sequences in East Africa for the Middle Stone Age through the Iron Age. Past excavations of the shelter revealed an extremely rich lithic and faunal assemblage, but were problematic, either because of poor excavation and recording methods (in the 1930s), or because the materials were never fully studied (in the 1979/1981 excavations). In both cases, excavators had concluded that the shelter contained a deposit without visible separation between archaeological levels. Re-excavation of Mumba, using modern techniques for recording spatial data, show that the previous geological and archaeological sub-divisions of the shelter deposits need much revision. The results of the excavation have implications for the interpretation of the “transitional” Mumba Industry in the Pleistocene levels and for the concurrence of ceramic traditions in the Holocene levels.
This paper describes cercopithecid craniodental and postcranial fossils recovered by L. S. B. Leakey at Kanam East, Kenya during the early 1930s. These fossil monkeys have been generally assumed to have been derived from early Pliocene horizons, but their exact geographical and stratigraphical provenience is unknown. Although the question of the evolutionary significance of these specimens must await the recovery of more securely dated material from Kanam East, some general conclusions can be drawn concerning their taxonomic affinities and paleobiology. Based on comparative studies of the craniodental material, at least three extant genera are represented—Colobus,Lophocebus, andCercopithecus. The postcranial fossils include a number of hindlimb specimens, as well as the manubrium of a sternum and a caudal vertebra. Identification of the postcranial remains to particular genera is not possible, but they are similar in morphology to modern arboreal and semiterrestrial cercopithecid monkeys of small to medium size. It is evident that Kanam East had a diverse cercopithecid community, similar to those found today in forested and woodland habitats, and this may be of some significance in reconstructing the paleoecology of the site. Because the fossil record of most extant cercopithecid genera is rather sparse at Plio-Pleistocene sites in Africa, Kanam East represents one of only a few sites that has yielded material that can be assigned toColobus,Lophocebus, orCercopithecus. The fossil monkeys from the site, therefore, provide additional evidence to help reconstruct the paleobiology, as well as the patterns of species diversity and community structure that characterized the cercopithecid radiation during the Plio-Pleistocene.
Guenons (tribe Cercopithecini) are one of the most diverse groups of primates. They occupy all of sub-Saharan Africa and show
great variation in ecology, behavior, and morphology. This variation led to the description of over 60 species and subspecies.
Here, using next-generation DNA sequencing (NGS) in combination with targeted DNA capture, we sequenced 92 mitochondrial genomes
from museum-preserved specimens as old as 117 years. We infer evolutionary relationships and estimate divergence times of
almost all guenon taxa based on mitochondrial genome sequences. Using this phylogenetic framework, we infer divergence dates
and reconstruct ancestral geographic ranges. We conclude that the extraordinary radiation of guenons has been a complex process
driven by, among other factors, localized fluctuations of African forest cover. We find incongruences between phylogenetic
trees reconstructed from mitochondrial and nuclear DNA sequences, which can be explained by either incomplete lineage sorting
or hybridization. Furthermore, having produced the largest mitochondrial DNA data set from museum specimens, we document how
NGS technologies can “unlock” museum collections, thereby helping to unravel the tree-of-life. [Museum collection; next-generation
DNA sequencing; primate radiation; speciation; target capture.]
African green monkeys (Chlorocebus) represent a widely distributed and morphologically diverse primate genus in sub-Saharan Africa. Little attention has been paid to their genetic diversity and phylogeny. Based on morphological data, six species are currently recognized, but their taxonomy remains disputed. Here, we aim to characterize the mitochondrial (mt) DNA diversity, biogeography and phylogeny of African green monkeys. We analyzed the complete mitochondrial cytochrome b gene of 126 samples using feces from wild individuals and material from zoo and museum specimens with clear geographical provenance, including several type specimens. We found evidence for nine major mtDNA clades that reflect geographic distributions rather than taxa, implying that the mtDNA diversity of African green monkeys does not conform to existing taxonomic classifications. Phylogenetic relationships among clades could not be resolved suggesting a rapid early divergence of lineages. Several discordances between mtDNA and phenotype indicate that hybridization may have occurred in contact zones among species, including the threatened Bale monkey (Chlorocebus djamdjamensis). Our results provide both valuable data on African green monkeys' genetic diversity and evolution and a basis for further molecular studies on this genus. Am. J. Primatol. 00:1-11, 2013. © 2013 Wiley Periodicals, Inc.
Baboons (genus Papio) are an interesting phylogeographical primate model for the evolution of savanna species during the Pleistocene. Earlier studies, based on partial mitochondrial sequence information, revealed seven major haplogroups indicating multiple para- and polyphylies among the six baboon species. The most basal splits among baboon lineages remained unresolved and the credibility intervals for divergence time estimates were rather large. Assuming that genetic variation within the two studied mitochondrial loci so far was insufficient to infer the apparently rapid early radiation of baboons we used complete mitochondrial sequence information of ten specimens, representing all major baboon lineages, to reconstruct a baboon phylogeny and to re-estimate divergence times. Our data confirmed the earlier tree topology including the para- and polyphyletic relationships of most baboon species; divergence time estimates are slightly younger and credibility intervals narrowed substantially, thus making the estimates more precise. However, the most basal relationships could not be resolved and it remains open whether (1) the most southern population of baboons diverged first or (2) a major split occurred between southern and northern clades. Our study shows that complete mitochondrial genome sequences are more effective to reconstruct robust phylogenies and to narrow down estimated divergence time intervals than only short portions of the mitochondrial genome, although there are also limitations in resolving phylogenetic relationships. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.
Phylogenetic relationships, divergence times, and patterns of biogeographic descent among primate species are both complex and contentious. Here, we generate a robust molecular phylogeny for 70 primate genera and 367 primate species based on a concatenation of 69 nuclear gene segments and ten mitochondrial gene sequences, most of which were extracted from GenBank. Relaxed clock analyses of divergence times with 14 fossil-calibrated nodes suggest that living Primates last shared a common ancestor 71-63 Ma, and that divergences within both Strepsirrhini and Haplorhini are entirely post-Cretaceous. These results are consistent with the hypothesis that the Cretaceous-Paleogene mass extinction of non-avian dinosaurs played an important role in the diversification of placental mammals. Previous queries into primate historical biogeography have suggested Africa, Asia, Europe, or North America as the ancestral area of crown primates, but were based on methods that were coopted from phylogeny reconstruction. By contrast, we analyzed our molecular phylogeny with two methods that were developed explicitly for ancestral area reconstruction, and find support for the hypothesis that the most recent common ancestor of living Primates resided in Asia. Analyses of primate macroevolutionary dynamics provide support for a diversification rate increase in the late Miocene, possibly in response to elevated global mean temperatures, and are consistent with the fossil record. By contrast, diversification analyses failed to detect evidence for rate-shift changes near the Eocene-Oligocene boundary even though the fossil record provides clear evidence for a major turnover event ("Grande Coupure") at this time. Our results highlight the power and limitations of inferring diversification dynamics from molecular phylogenies, as well as the sensitivity of diversification analyses to different species concepts.
Y-chromosomal patterns agree with earlier karyotypic studies in depicting a close relationship among patas, vervets, and l’Hoest’s
monkeys distinct from other members of the Cercopithecini. This relationship is suggested to be one of shared ancestry, rather
than one due to past hybridization. Thus, on the working assumption that the earliest guenons were arboreal, terrestriality
appears to have originated only once among the extant cercopithecins. Consequently, taxonomic revision is necessary as relates
to the three terrestrial taxa: Erythrocebus patas, Cercopithecus aethiops, and C. lhoesti.
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.
The Olduvai Gorge Coring Project drilled a total of 611.72 m of core (575.48 m recovered) of mostly fluvio- lacustrine and fan-delta volcaniclastic Pleistocene strata at three sites in the Olduvai Basin, Tanzania, in 2014. We have developed a chronostratigraphic framework for three of the cores based on 40Ar/39Ar dating of core and outcrop volcanic and volcaniclastic units, core paleomagnetic stratigraphy, and tephrochemical correlation between cores and from core to outcrop. This framework is then used to constrain Bayesian stratigraphic age models which permit age estimates for desired core levels with realistic confidence intervals. The age models reveal that the deepest core level reached at 245 mbs is ~2.24 Ma, ~210 kyr older than the oldest strata exposed at Olduvai Gorge. Strata net accretion rates in this early phase of basin history were relatively rapid (57–69 cm/ kyr), but decreased within ~250 kyr to ~15 cm/kyr in Lower Bed I. Rates rebounded partially in Upper Bed I, but subsequently declined to < 10 cm/kyr by Middle to Upper Pleistocene. The age models also provide new estimates for the basal contacts of upper Olduvai Gorge stratigraphic units that have been previously difficult to calibrate: Bed III at 1.14 ± 0.05 (95% confidence interval), Bed IV at 0.93 ± 0.08, Masek at 0.82 ± 0.06, and Ndutu at 0.50 ± 0.04 Ma. Finally, based on recently acquired seismic imaging identifying basement another 135 m beneath the bottom of the deepest core, extrapolation of net accretion rates suggests that sedimentation began at this site in the Olduvai Basin at ~2.5 Ma.
The taxonomy and number of Cercopithecus monkey radiation events in southern Africa are still debated. To date, genetic studies have largely been limited to single specimens per taxon and a scattered geographical distribution. A recent study focusing on South African Cercopithecus monkeys showed that populations can be divided into three distinct genetic entities. Our current study aims to add new mtDNA and microsatellite data from a coastal population (Vamizi Island) in Mozambique to compare to existing data from South Africa. Our additional data allowed analysis of the number and timing of radiation events of Cercopithecus monkeys in southern Africa. Here we propose the occurrence of a single, north-south radiation event during the mid-Pleistocene along the Afromontane forest belt and that after the Last Glacial Maximum, samango populations reradiated into (re)established coastal forests on a more local scale. Our population genetic data support this pattern for both Mozambican, as well as South African samango monkey populations. By including mtDNA sequence data from Cercopithecus across Africa, we also discuss the hypothesis that the ‘Kingdon Line’ may explain the divergence of two major species in Africa within the C. mitis/nictitans group: C. albogularis and C. mitis.
Old World monkeys (Cercopithecoidea) are the most successful and diverse group of living non-human primates in terms of the number of species, behavioural repertoires and ecology. They have much to teach us about the processes of evolution and the principles of ecology, and are among our closest living relatives. This volume presents a broad, technical account of cercopithecoid biology including molecular, behavioural and morphological approaches to phylogeny, population structure, allometry, fossil history, functional morphology, ecology, cognitive capabilities, social behaviour and conservation. It will be the definitive reference on this group for professionals and graduate students in primatology, animal behaviour, paleontology, morphology, systematics and physical anthropology, but will also be useful to senior undergraduates.
Recent fieldwork at Kanapoi has expanded the sample of fossil cercopithecids, facilitating a re-appraisal of their taxonomy. The assemblage now includes at least one species of cercopithecin, two papionins, and two colobines. The guenon Nanopithecus browni is similar in dental size to extant Miopithecus. We tentatively re-affirm the identification of Parapapio cf. ado and confirm the presence of Theropithecus. The colobines include a small form tentatively attributed to Kuseracolobus and a second larger species. The Kanapoi fossils represent the oldest occurrences of guenons in Africa and of the important genus Theropithecus, the most abundant and widespread primate in the Neogene of Africa. In the assemblage, Parapapio cf. ado is the most abundant form, comprising the majority of specimens. All of the other taxa are comparatively rare. Colobines make up a small part of the Kanapoi fossil assemblage compared to most other contemporary sites, including Allia Bay, Kenya, where, like Kanapoi, Australopithecus anamensis has been found. The presence of Theropithecus is consistent with the presence of some relatively open habitat at Kanapoi. While the ecological preferences of the small cercopithecin are unknown, most guenons are associated with relatively wooded habitats, as are most colobines, suggesting the availability of at least some wooded areas.
Baboons (Papio hamadryas) are among the most successful extant primates, with a minimum of six distinctive forms throughout Sub-Saharan Africa. However, their presence in the fossil record is unclear. Three early fossil taxa are generally recognized, all from South Africa: Papio izodi, Papio robinsoni and Papio angusticeps. Because of their derived appearance, P. angusticeps and P. robinsoni have sometimes been considered subspecies of P. hamadryas and have been used as biochronological markers for the Plio-Pleistocene hominin sites where they are found. We reexamined fossil Papio forms from across Africa with an emphasis on their distinguishing features and distribution. We find that P. robinsoni and P. angusticeps are distinct from each other in several cranial features, but overlap extensively in dental size. Contrary to previous assessments, no diagnostic cranio-mandibular material suggests these two forms co-occur, and dental variation at each site is comparable to that within P. h. ursinus, suggesting that only one form is present in each case. P izodi, however, may co-occur with P. robinsoni, or another Papio form, at Sterkfontein Member 4. P izodi appears more primitive than P. robinsoni and P. angusticeps. P. robinsoni is slightly distinct from P. hamadryas subspecies in its combination of features while P. angusticeps might be included within one of the modern P. hamadryas varieties (i.e., P. h. angusticeps). No definitive Papio fossils are currently documented in eastern Africa until the Middle Pleistocene, pointing to southern Africa as the geographic place of origin for the genus. These results have implications for Plio-Pleistocene biochronology and baboon evolution.
Detailed analyses and comparisons of postcranial specimens of Plio-Pleistocene cercopithecids provide an opportunity to examine the recent evolutionary history and locomotor diversity in Old World monkeys. Studies examining the positional behavior and substrate preferences of fossil cercopithecids are also important for reconstructing the paleoenvironments of Plio-Pleistocene hominin sites. Here we describe a new fossil cercopithecid tibia (EP 1100/12) from the Australopithecus afarensis-bearing Upper Laetolil Beds (∼3.7 Ma) of Laetoli in northern Tanzania. The fossil tibia is attributed to cf. Rhinocolobus sp., which is the most common colobine at Laetoli. In addition to qualitative comparisons, the tibial shape of EP 1100/12 was compared to that of 190 extant cercopithecids using three-dimensional landmarks. Discriminant function analyses of the shape data were used to assess taxonomic affinity and shape variation relating to positional behavior. EP 1100/12 clustered with extant colobines, particularly the large-bodied genera Nasalis and Rhinopithecus. Comparisons reveal that EP 1100/12 belongs to a large-bodied monkey that engaged in arboreal pronograde quadrupedalism. These findings add further support to previous inferences that woodland and forest environments dominated the paleoenvironment of the Upper Laetolil Beds, which supported the diverse community of cercopithecids at Laetoli. The inferred paleoecology and the presence of large-bodied arboreally-adapted monkeys at Laetoli show that A. afarensis had access to a range of diverse habitats, including woodlands and forests. This supports the possibility that A. afarensis, with its potential range of positional capabilities, was able to utilize arboreal settings for food acquisition and refuge from predators.
The baboons of the genus Papio [excluding the gelada (Theropithecus) and (pace Delson, 1975), the mandrills, and drills (Mandrillus)] comprise a cluster of para-patric populations spread across most of the Ethiopian faunal zone. The present paper uses baboon diversity to explore some aspects of species definition and diagnosis, without attempting a comprehensive revision of the group or an exhaustive exploration of the species concept. The baboons are well suited to this purpose, because the various phenotypically distinct “forms” (which I call subspecies) have some but not all of the attributes commonly used to define one or another variant of the species concept. Another advantage is their quasi-continuous distribution, mostly undivided by extrinsic barriers that would avoid the problem of delineating natural units yet including some populations that are geographically isolated but not phenetically distinct, which illustrate the problems of definition raised by extrinsic isolation.
With genomic data, alignments can be assembled that greatly increase the number of informative sites for analysis of molecular divergence dates. Here, we present an estimate of the molecular divergence dates for all of the major primate groups. These date estimates are based on a Bayesian analysis of approximately 59.8 kbp of genomic data from 13 primates and 6 mammalian outgroups, using a range of paleontologically supported calibration estimates. Results support a Cretaceous last common ancestor of extant primates (approximately 77 mya), an Eocene divergence between platyrrhine and catarrhine primates (approximately 43 mya), an Oligocene origin of apes and Old World monkeys (approximately 31 mya), and an early Miocene (approximately 18 mya) divergence of Asian and African great apes. These dates are examined in the context of other molecular clock studies.
Accurate divergence date estimates improve scenarios of primate evolutionary history and aid in interpretation of the natural history of disease-causing agents. While molecule-based estimates of divergence dates of taxa within the superfamily Hominoidea (apes and humans) are common in the literature, few such estimates are available for the Cercopithecoidea (Old World monkeys), the sister taxon of the hominoids in the primate infraorder Catarrhini. To help fill this gap, we have sequenced the entire mitochondrial DNA (mtDNA) genomes from a representative of three cercopithecoid tribes, Cercopithecini (Chlorocebus aethiops), Colobini (Colobus guereza), and Presbytini (Trachypithecus obscurus), and analyzed these new data together with other catarrhine mtDNA genomes available in public databases.
New fossil Cercopithecus material dated at 1.90 and 2.90 m. y. from the lower Omo basin, southwestern Ethiopia is described and compared to samples of modern C. aethiops and C. nictitans and to several other species discussed in the literature. All of the specimens described belong to the genus Cercopithecus. Assignment to species must await the recovery of further material.Copyright © 1972 S. Karger AG, Basel
The Middle Awash Valley, Afar, Ethiopia, contains a sedimentary sequence
that is > 1 km thick, spans much of the Neogene, and contains
vertebrate fossils throughout. Newly defined formations described here
are older and younger than the hominid-bearing Hadar Formation. The
Awash deposystem reflects deposition in an evolving triple junction.
Old World monkeys are some of the most common and visible components of the modern mammalian fauna of Africa, and are the dominant nonhuman primates in Africa today with respect to the overall numbers of species present and the number of ecological zones inhabited. What is rarely appreciated is that Old World monkeys have risen to a position of ecological dominance among primates only recently in geological time. During the early and middle Miocene, the Cercopithecoidea were well established in Africa, but not taxonomically diverse. The absence or near absence of monkey fossils from prolific early Miocene sites like Rusinga Island suggests that the animals were genuinely rare elements of the mammalian fauna at the time. The earliest African cercopithecoids belong to the Victoriapithecidae, an extinct family from the early to middle Miocene of eastern Africa that exhibit a mosaic of basal catarrhine and modern Old World monkeylike morphological features. This chapter describes the systematic paleontology of Cercopithecoidea.
Approximately 6000 cercopithecoid specimens have been recovered from Omo Group deposits of southwestern Ethiopia since 1967. The specimens range in completeness from fragmentary isolated teeth to nearly complete skeletons. The majority of the specimens consist, however, of isolated tecth, fragmentary jaw parts and limb bones. They range in age from c. 3·0 m.y. to c. 0·9 m.y.Both Colobinae and Cercopithecinae have been recovered, with the cercopithecines predominating. The colobine specimens fall into 4 size groups which probably represent taxonomic units. The smallest of the specimens have been assigned to genus Colobus. Of the two middle-sized groups, the smaller is rare and of unknown affinities, while the larger is probably a new genus and species. The largest of the specimens, similar in size to a modern savannah baboon, probably also represents a new genus and species.Six species of cercopithecines have been recovered. Specimens of Cercopithecus and Papio are rare as are those of two species of small Papionini of uncertain affinities. The majority of the specimens belong to the genus Theropithecus with both T. brumpti and T. oswaldi being represented.Cercopithecoid specimens are not evenly distributed through the deposits and preliminary analysis indicates that the differences in frequencies may be due to changes in the environment of the lower Omo basin through time.
Aim To examine and visualize clines in size and shape of Cercopithecus aethiops Linneus, 1758 (Primate, Cercopithecidae) skulls, and to investigate environmental factors which might best explain the observed variation.
Location Sub‐Saharan Africa.
Methods Eighty‐six three‐dimensional anatomical landmarks were used to describe 306 skulls of adult C. aethiops sampled over its entire distribution. Geometric morphometric methods for the quantitative analysis of form variation were applied. Size and shape variables were computed and regressed onto geographical coordinates and environmental variables (elevation, temperature, rainfall, moisture and Shannon rainfall diversity index) using both linear and curvilinear models. Components (geographical, environmental, spatially structured environmental and residual) of ecogeographical variation in skull form were partitioned using partial regression. A novel approach for summarizing and visualizing nonlinear patterns of clinal variation using surface rendering of three‐dimensional shapes is presented.
Results Clinal variation in size and shape was highly significant, and was best described by curvilinear models. There were strong similarities between females and males. The cline in size was especially pronounced, explaining up to about 40% of observed variation, and was mainly longitudinal rather than latitudinal. A major trend of clinal shape variation also occurred from west to east, and corresponded to an expansion of the face relative to the neurocranium in the west. In the east, skulls also tended to be deeper and with narrower zygomatic arches. Geography and the spatially structured environmental component were the major contributors to the explained variance in size in both sexes, but the proportion of variance explained by the latter was smaller in females. In contrast, geography and environment explained similar amounts of variation in shape and their contribution was about twice that of the spatially structured environmental component. About 60–80% of variation in skull form was not explained by any variable in the analysis. The main factors influencing skull size differed in females and males, with rainfall being very influential in males. Both female and male skull shapes were strongly affected by average annual rainfall.
Main conclusions A strong spatial and environmental basis to variations in African vervet monkey skull form was evident. However, the observed pattern did not conform to predictions based on Bergmann's rule. Rainfall consistently emerged as an important predictor, which may contribute to intraspecific variation in the size and shape of vervet monkey skulls through its effect on habitat productivity.
New finds from Laetoli have allowed a more detailed assessment of the taxonomy and paleobiology of the fossil cercopithecids.
Most of the specimens consist of isolated teeth, jaw fragments and postcranial bones from the Upper Laetolil Beds (∼3.5–3.8
Ma), but four specimens are known from the Upper Ndolanya Beds (∼2.66 Ma) and a proximal humerus has been recovered from the
Lower Laetolil Beds (∼3.8–4.3 Ma). Four species are represented: Parapapio ado, Papionini gen. et sp. indet., cf. Rhinocolobus sp., and Cercopithecoides sp. Parapapio ado is the most common species. Based on dental size and proportions and facial morphology, Pp. ado can be distinguished from all other species of Parapapio. The postcranial specimens attributed to Pp. ado indicate that it was a slender and agile semi-terrestrial monkey. A few isolated teeth represent a second species of papionin,
larger in dental size than Pp. ado. Due to the paucity of the material, the taxon is left unassigned at the genus and species level. A distal humerus attributed
to this taxon indicates that it was large terrestrial cercopithecid. The most common species of colobine is referred to cf.
Rhinocolobus sp., based on its overall similarities to Rhinocolobus turkanaensis. The material can be distinguished from all fossil colobine species previously recognized from Africa, but without more complete
cranial specimens it is not possible to diagnose a new taxon. From the postcranial material it can be inferred that it was
generally adapted for arboreal quadrupedalism. The somewhat smaller species of colobine represents a previously undescribed
species of Cercopithecoides. The postcranial specimens attributed to this taxon indicate that it was fully arboreal. Analysis of the distribution of
the Laetoli cercopithecids provides provisional evidence of spatial patterning and temporal trends. For example, the dentition
of Parapapio exhibits a trend to increase in size during the course of the Upper Laetolil Beds. As at other late Miocene and early Pliocene
localities older than 3.5 Ma, the Laetoli cercopithecid community is characterized by the absence of Theropithecus and the relatively large proportion of colobines. After 3.5 Ma Theropithecus becomes the dominant cercopithecid at all East African localities, and the proportion of colobines declines accordingly.
Keywords
Parapapio
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Paracolobus
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Rhinocolobus
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Cercopithecoides
-Papionin-Colobines-Monkey-Pliocene-East Africa
Jolly (1993) stated that the degree of ecological niche separation among closely related taxa may help to distinguish their
evolutionary relationships since ecological divergence is often thought of as a characteristic of true biological species.
Based on qualitative data, Jolly (1993) hypothesized that there is little niche separation among savanna baboon forms and
therefore suggested that they are a single species. In addition, a recent study by Frost and colleagues (2003) found that
baboon cranial morphology covaried with latitude that also suggests a single species designation. This present study quantitatively
examined the ecological niche space of savanna baboons to test Jolly’s hypothesis and to examine how their ecological variation
varied with geography. To investigate this idea, previously published long-term data were accumulated from over twenty savanna
baboon populations. Variables from four categories were used to quantify their niche space: 1) Environment, 2) Diet, 3) Activity
budget, and 4) Social organization. A discriminant function and principal components analysis was conducted for each dataset,
and confirmed that savanna baboon subspecies inhabit significantly distinct environments, yet display a statistically non-significant
difference in their diet, activity budget, and social organization. In addition, a hierarchical cluster analysis revealed
that savanna baboon ecology followed a latitudinal cline. Therefore, the results of these analyses cannot falsify Jolly’s
hypothesis that there is little ecological niche separation among baboon taxa.
40Ar/39Ar dating of Pliocene tuffs from Laetoli, northern Tanzania, has refined the geochronological framework of the Laetolil Beds
and overlying strata. Dated units include the Lower and Upper Laetolil Beds (4.36−3.85 Ma and 3.85−3.63 Ma, respectively),
the Lower and Upper Ndolanya Beds (3.58 and 2.66 Ma, respectively), the Naibadad Beds (2.155−2.057 Ma), and the Olpiro Beds
(<2.057 Ma). Sedimentation rates of ∼50 cm/ka are obtained for the lower half of the Upper Laetolil Beds through Tuff 2, compared
to a rate of ∼15 cm/ka for the upper half (Tuff 4 to Tuff 8). Accumulation of the Upper Laetolil Beds required less than 220
ka, corresponding to a minimum overall sedimentation rate of 22 cm/ka. The new dates provide a more precise assessment of
the age of the fossil hominins at Laetoli. Australopithecus afarensis specimens from the Upper Laetolil Beds are constrained to 3.85−3.63 Ma, and a new interpolated age for the Footprint Tuff
(Tuff 7) is 3.66 Ma. The Paranthropus aethiopicus maxilla (Silal Artum) from the Upper Ndolanya Beds at 2.66 Ma is amongst the oldest known specimen attributable to this genus.
Keywords
40Ar/39Ar dating-Laetoli-Hominin-Pliocene-Tanzania-Laetolil Beds-Ndolanya Beds-Naibadad Beds-Olpiro Beds