Genetic assessment of an isolated endemic Samango monkey (Cercopithecus albogularis labiatus) population in the Amathole Mountains, Eastern Cape Province, South Africa.

The endemic Samango monkey subspecies (Cercopithecus albogularis labiatus) inhabits small discontinuous Afromontane forest patches in the Eastern Cape, KwaZulu-Natal midlands and southern Mpumalanga Provinces in South Africa. The subspecies is affected by restricted migration between forest patches which may impact on gene flow resulting in inbreeding and possible localized extinction. Current consensus, based on habitat quality, is that C. a. labiatus can be considered as endangered as the small forest patches they inhabit may not be large enough to sustain them. The aim of this study was to conduct a molecular genetic investigation to determine if the observed isolation has affected the genetic variability of the subspecies. A total of 65 Samango monkeys (including juveniles, subadults and adults) were sampled from two localities within the Hogsback area in the Amathole Mountains. Nuclear and mitochondrial DNA variation was assessed using 17 microsatellite markers and by sequencing the hypervariable 1 region (HVR1). Microsatellite data generated was used to determine population structure, genetic diversity and the extent of inbreeding. Sequences of the HVR1 were used to infer individual origins, haplotype sharing and haplotype diversity. No negative genetic factors associated with isolation such as inbreeding were detected in the two groups and gene flow between groups can be regarded as fairly high primarily as a result of male migration. This was in contrast to the low nuclear genetic diversity observed (H o = 0.45). A further reduction in heterozygosity may lead to inbreeding and reduced offspring fitness. Translocations and establishment of habitat corridors between forest patches are some of the recommendations that have emerged from this study which will increase long-term population viability of the subspecies.

X Chromosome Introgression and Recombination in the cephus Group of Cercopithecus Monkeys.

A representative of Cercopithecus erythrotis was surveyed at a 9.3-kb region of the X chromosome. The data were compared against homologous sequences of closely related Cercopithecus monkeys including C. cephus, a species recently shown to have 2 polymorphic X-chromosomal lineages. Direct sequence comparisons and subsequent phylogenetic analyses revealed that synapomorphies in the first 4.3 kb cluster C. erythrotis with one C. cephus lineage, while synapomorphies in the latter 5.0 kb join it with the second C. cephus lineage. This pattern very likely reflects an ancestral episode of introgression from C. cephus into C. erythrotis followed by a recombination event. Similar groups of synapomorphies occur at different phylogenetic depths within the C. erythrotis/C. cephus/C. ascanius radiation and reveal new details in the evolutionary history of this 3-species clade.

Morphoarchitectural variation in South African fossil cercopithecoid endocasts.

Despite the abundance of well-preserved crania and natural endocasts in the South African Plio-Pleistocene cercopithecoid record, which provide direct information relevant to the evolution of their endocranial characteristics, few studies have attempted to characterize patterns of external brain morphology in this highly successful primate Superfamily. The availability of non-destructive penetrating radiation imaging systems, together with recently developed computer-based analytical tools, allow for high resolution virtual imaging and modeling of the endocranial casts and thus disclose new perspectives in comparative paleoneurology. Here, we use X-ray microtomographic-based 3D virtual imaging and quantitative analyses to investigate the endocranial organization of 14 cercopithecoid specimens from the South African sites of Makapansgat, Sterkfontein, Swartkrans, and Taung. We present the first detailed comparative description of the external neuroanatomies that characterize these Plio-Pleistocene primates. Along with reconstruction of endocranial volumes, we combine a semi-automatic technique for extracting the neocortical sulcal pattern together with a landmark-free surface deformation method to investigate topographic differences in morphostructural organization. Besides providing and comparing for the first time endocranial volume estimates of extinct Plio-Pleistocene South African cercopithecoid taxa, we report additional information regarding the variation in the sulcal pattern of Theropithecus oswaldi subspecies, and notably of the central sulcus, and the neuroanatomical condition of the colobine taxon Cercopithecoides williamsi, suggested to be similar for some aspects to the papionin pattern, and discuss potential phylogenetic and taxonomic implications. Further research in virtual paleoneurology, applied to specimens from a wider geographic area, is needed to clarify the polarity, intensity, and timing of cortical surface evolution in cercopithecoid lineages.

New insights into samango monkey speciation in South Africa.

The samango monkey is South Africa's only exclusively forest dwelling primate and represents the southernmost extent of the range of arboreal guenons in Africa. The main threats to South Africa's forests and thus to the samango are linked to increasing land-use pressure and increasing demands for forest resources, resulting in deforestation, degradation and further fragmentation of irreplaceable habitats. The species belongs to the highly polytypic Cercopithecus nictitans group which is sometimes divided into two species C. mitis and C. albogularis. The number of subspecies of C. albogularis is also under debate and is based only on differences in pelage colouration and thus far no genetic research has been undertaken on South African samango monkey populations. In this study we aim to further clarify the number of samango monkey subspecies, as well as their respective distributions in South Africa by combining molecular, morphometric and pelage data. Overall, our study provides the most comprehensive view to date into the taxonomic description of samango monkeys in South Africa. Our data supports the identification of three distinct genetic entities namely; C. a. labiatus, C. a. erythrarchus and C. a. schwarzi and argues for separate conservation management of the distinct genetic entities defined by this study.

Seven novel MHC class I alleles identified in Cercopithecus mitis.

We report here the identification of three Cemi-A and four Cemi-B novel alleles of Cercopithecus mitis.

Ubiquitous Hepatocystis infections, but no evidence of Plasmodium falciparum-like malaria parasites in wild greater spot-nosed monkeys (Cercopithecus nictitans).

Western gorillas (Gorilla gorilla) have been identified as the natural reservoir of the parasites that were the immediate precursor of Plasmodium falciparum infecting humans. Recently, a P. falciparum-like sequence was reported in a sample from a captive greater spot-nosed monkey (Cercopithecus nictitans), and was taken to indicate that this species may also be a natural reservoir for P. falciparum-related parasites. To test this hypothesis we screened blood samples from 292 wild C. nictitans monkeys that had been hunted for bushmeat in Cameroon. We detected Hepatocystis spp. in 49% of the samples, as well as one sequence from a clade of Plasmodium spp. previously found in birds, lizards and bats. However, none of the 292 wild C. nictitans harbored P. falciparum-like parasites.

Full-length genome sequence of a simian immunodeficiency virus from a wild-captured sun-tailed monkey in Gabon provides evidence for a species-specific monophyletic SIVsun lineage.

Since the first characterization of SIVsun (L14 strain) from a sun-tailed monkey (Cercopithecus solatus) in Gabon in 1999, no further information exists about the evolutionary history and geographic distribution of this lentivirus. Here, we report the full-length molecular characterization of a second SIVsun virus (SIVsunK08) naturally infecting a wild-caught sun-tailed monkey. The SIVsunK08 strain was most closely related to SIVsunL14 and clustered with members of the SIVmnd-1/SIVlhoest group. SIVsunK08 shared identical functional motifs in the LTR, Gag and Env proteins with SIVsunL14. Our data indicate that C. solatus is naturally infected with a monophyletic SIVsun strain.

Polyspecific associations of Cercopithecus campbelli and C. petaurista with C. diana: what are the costs and benefits?

Polyspecific associations (PSA) are common in many African primate communities, including the diurnal primates at Taï Forest, Côte d'Ivoire. In this paper I use data on the PSA of two forest guenons, Campbell's (Cercopithecus campbelli) and lesser spot-nosed monkeys (C. petaurista), with Diana monkeys (C. diana) and other primates to clarify interspecific relationships during 17 months including a 3-month low-fruit period. I analyzed association in relation to fruit availability and measured forest strata use for C. campbelli and C. petaurista when alone and in associations with and without C. diana. I also measured predator risk and reactions to potential predators. C. campbelli and C. petaurista had high association rates with C. diana monkeys, and fruit availability did not influence association rates. C. campbelli and C. petaurista used higher strata when in association with C. diana than when alone, but they used even higher strata when associated with other primates without C. diana. This suggested that C. diana competitively exclude C. campbelli and C. petaurista from higher strata. There were relatively large numbers of potential predators, and C. diana were usually the first callers to threatening stimuli, suggesting that antipredator benefits of association with C. diana outweighed the competitive costs. C. campbelli spent more time in association with C. diana than C. petaurista did and appeared to be more reliant on C. diana for antipredator benefits. C. petaurista were less reliant on C. diana because of a cryptic strategy and may have associated less in some months because of high chimpanzee (Pan troglodytes) presence.

A novel simian immunodeficiency virus isolated from a Schmidt's guenon (Cercopithecus ascanius schmidti).

A novel simian immunodeficiency virus (SIV) was characterized from a Schmidt's guenon (Cercopithecus ascanius schmidti), which was housed in a local zoo. The virus infection was detected during a routine serological screening for antibodies that were cross-reactive with SIVmac antigens. Infection with an immunodeficiency virus was confirmed using an INNO-LIA HIV Confirmation assay. Using DNA isolated from a blot clot, a 1895 nt partial pol sequence was amplified and sequenced. Phylogenetic analysis showed that this virus, designated SIVschm, shares a distant relationship with SIVgsn, isolated from greater spot-nosed monkeys, and is one of the most divergent SIVs identified to date.

Characterization of a novel simian immunodeficiency virus (SIVmonNG1) genome sequence from a mona monkey (Cercopithecus mona).

A novel simian immunodeficiency virus (SIV) sequence has been recovered from RNA extracted from the serum of a mona monkey (Cercopithecus mona) wild born in Nigeria. The sequence was obtained by using novel generic (degenerate) PCR primers and spans from two-thirds into the gag gene to the 3' poly(A) tail of the SIVmonNG1 RNA genome. Analysis of the open reading frames revealed that the SIVmonNG1 genome codes for a Vpu protein, in addition to Gag, Pol, Vif, Vpr, Tat, Rev, Env, and Nef proteins. Previously, only lentiviruses infecting humans (human immunodeficiency virus type 1 [HIV-1]) and chimpanzees (SIVcpz) were known to have a vpu gene; more recently, this has also been found in SIVgsn from Cercopithecus nictitans. Overall, SIVmonNG1 most closely resembles SIVgsn: the env gene sequence groups with HIV-1/SIVcpz env sequences, whereas the pol gene sequence clusters closely with the pol sequence of SIVsyk from Cercopithecus albogaris. By bootscanning and similarity plotting, the first half of pol resembles SIVsyk, whereas the latter part is closer to SIVcol from Colobus guereza. The similarities between the complex mosaic genomes of SIVmonNG1 and SIVgsn are consistent with a shared or common lineage. These data further highlight the intricate nature of the relationships between the SIVs from different primate species and will be helpful for unraveling these associations.

Variation in seed handling by two species of forest monkeys in Rwanda.

We examined temporal variability in the handling and dispersal of seeds by two sympatric species of monkeys, the arboreal blue monkey (Cercopithecus mitis doggetti) and the more terrestrial mountain monkey (C.l'hoesti). Ten months of data on phenological patterns and foraging behavior, including details of seed handling based on scan sampling data, were combined with dung sample data to examine patterns of seed handling. The systematic scan sampling observations showed that blue monkeys and mountain monkeys alternated between acting predominately as seed droppers, seed predators, and seed defecators depending on fruit resource availability. All the mountain monkey dung samples examined contained intact seeds, and 94% of the blue monkey dung samples contained intact seeds. Both monkey species defecated a greater number of seeds per dung sample and larger-sized seeds than found elsewhere for Cercopithecus monkeys. We found a mean of 2.33 and 6.43 seeds > 2 mm in blue and mountain monkey dung samples, respectively. The mountain monkeys dispersed relatively higher numbers of seeds and frequented open, disturbed forest, suggesting that terrestrial forest monkeys have been overlooked as potentially important seed dispersal agents. The variability in the ways seeds were handled was dependent on the array of available food resources and may suggest that the monkeys exert weak selective pressures on fruit traits.

Phylogenetic, paleodemographic, and taphonomic implications of Victoriapithecus deciduous teeth from Maboko, Kenya.

More than 240 milk teeth of Victoriapithecus macinnesi, representing all elements of the deciduous dentition, are described. Their morphology is intermediate between that of hominoids and cercopithecids. Unlike colobine and cercopithecine milk teeth, Victoriapithecus dp3s, dp4s, and at least 7 (14%) dp4s lack transverse distal loph(id)s and are not bilophodont. Victoriapithecus also differs from cercopithecids in having less elongated deciduous premolars, a dp3 metacone set mesial to a very small hypocone, a dp4 crista obliqua, and a dp4 hypoconulid. The deciduous canines and incisors of Victoriapithecus are like those of other cercopithecids in having an uneven distribution of enamel around a compressed (rather than cylindrical) root, but differ from cercopithecids and resemble hominoids in being more elongated. Since Colobinae and Cercopithecinae share features of the deciduous dentition that are derived relative to Victoriapithecus and hominoids, extant Old World monkeys are interpreted as representing the sister-taxon of the middle Miocene cercopithecoids. Due to a dramatic increase in the number of deciduous teeth found at Maboko Island, juvenile individuals represent a much larger proportion of recently excavated Victoriapithecus collections than is true of pre-1987 assemblages which mainly derive from sediment first excavated during the 1930s and 1940s. Age distribution differences between pre- and post-1987 samples indicate that paleontological collection procedures were more important than taphonomic biases in determining the paleodemographic profile of the Maboko fossils. Since the Victoriapithecus assemblage from Maboko is strikingly similar to that of fossil Theropithecus oswaldi from Olorgesailie in terms of the large number of specimens and high representation of juvenile and infant individuals, the latter can no longer be viewed as unique among cercopithecoid fossil assemblages. Rather than being related to a specific cause of death, such as selective hunting of T. oswaldi by Homo (Shipman et al. [1981] Curr. Anthropol. 22:257-268), the large number of cercopithecoids at both sites is attributed to the fact that both assemblages represent excavated samples and that the preferred habitats of the extinct monkeys were probably at or near the site of deposition. The greater number of young adult male than female canines in the apparently attritional Maboko Bed 5 assemblage, indicate that the social organization of V. macinnesi may have been similar to that of modern macaques, with males migrating out of their natal group and suffering higher death rates than females at puberty.

Terrestrial adaptations in the postcranial skeletons of guenons.

Arboreal and semiterrestrial guenons show similar osteological features of the limbs across a wide range of species, environments, and geography, while the more terrestrially committed guenons exhibit greater morphological divergence. An ecomorphological comparison of two sympatric guenons living in Kibale Forest, Uganda, reveals an array of anatomical adaptations for terrestriality in the limbs of Cercopithecus lhoesti similar to those found in Erythrocebus patas. In contrast, Cercopithecus aethiops, although also frequent users of the terrestrial environment, generally exhibit fewer morphological adaptations characteristic of a terrestrial lifestyle. It appears that significant morphological modification for terrestriality has occurred twice within the diverse radiation of living guenons with C. aethiops perhaps representing a third group in the making.

Quaternary environments and the evolution of primates in East Asia, with notes on two new specimens of fossil Cercopithecidae from China.

Primate faunas in East Asia since the mid-Tertiary have undergone a series of major changes in response to a complex sequence of environmental changes. As a consequence of the Himalayan orogeny and the rapid, episodic uplift of the Tibetan plateau, the climate of East Asia during the late Tertiary became monsoonal and thus more strongly seasonal. This led to the expansion of seasonal tropical forests and, in some areas, grasslands. During the Pleistocene, the climatic consequences of continued rapid uplift of the Tibetan plateau and other land masses (e.g. the Qinling mountains) were combined with those of glaciations, resulting in dramatic climatic oscillations between warm-humid and cold-dry phases. The contraction of tropical environments that began in the late Tertiary reached its peak at the last glacial maximum (LGM) and was responsible for the decline in the distribution and diversity of hominoids in East Asia. Cercopithecids, which were only minor elements of the late Tertiary primate faunas, colonized tropical, subtropical and temperate environments in the Pleistocene and were able to reradiate into those environments after the LGM. The abilities of monkeys to populate a wide range of terrestrial environments (eurytopy) contrast with those of apes, which are restricted to tropical forest environments (stenotopy).

Falsification of a single species hypothesis using the coefficient of variation: a simulation approach.

Dental variation remains an important criterion for assessing whether a morphologically homogeneous fossil primate sample includes more than one species. The Coefficient of Variation (CV) has commonly been used to compare variation in a fossil sample of unknown taxonomic composition with that of extant single-species samples, in order to determine whether more than one species might be present. However, statistical tests for differences between fossil and single species reference sample CVs often lack power, because fossil samples are usually small and confidence limits of the CV are consequently large. The present study presents a new methodology for using the CV to test the hypothesis that a sample represents only one species. Simulated sampling distributions of single-species and pooled-species CVs are generated based on variation observed in dental samples of extant Cercopithecus species. These simulated distributions are used to test a single-species hypothesis for 13 different combinations of two or three sympatric Cercopithecus species across four dental characteristics at different sample sizes. Two different ways to generate the reference value of the CV are used. Results show the proposed methodology has substantially greater power than previous methods for detecting multiple-species composition, while maintaining an acceptable Type I error rate. Results are also presented concerning the dependence of power on sample size and on the average difference between means in a pooled-species combination.