Sex chromosome phylogenetics indicate a single transition to terrestriality in the guenons (tribe Cercopithecini)

This is the first molecular study to trace the evolutionary transition in substrate preference across a primate radiation. We surveyed 20 guenons (tribe Cercopithecini) and 4 outgroup taxa for two Y-chromosomal genes, TSPY ( approximately 2240 bp) and SRY ( approximately 780 bp), and one X-chromosomal intergenic region ( approximately 1600 bp) homologous to a fragment of human Xq13.3. Parsimony and maximum likelihood analyses of the sex chromosomal datasets consistently cluster the three terrestrial taxa, Cercopithecus aethiops, Cercopithecus lhoesti, and Erythrocebus patas, into a group that is reciprocally monophyletic with a clade of arboreal Cercopithecus spp. Given that the common ancestor of the two clades was most likely an arboreal taxon, this phylogenetic pattern suggests the transition to terrestriality occurred only once among the extant guenons. This pattern also indicates that the genus Cercopithecus is paraphyletic, as presently defined, and calls for taxonomic revision so that the nomen describes a strictly monophyletic group. We outline four acceptable taxonomic schemes and suggest that the most appropriate is to reassign C. aethiops, C. lhoesti, and E. patas to the resurrected genus Chlorocebus. Finally, while the phylogeny and taxonomy of terrestrial guenons were the focus of this study, the X-chromosome sequences presented here represent the first molecular evidence to unambiguously place Allenopithecus nigroviridis as the basal lineage of the tribe Cercopithecini.     

Odontometric variation within and between taxonomic levels of cercopithecidae: Implications for interpetations of fossil samples

This study examines metric variation of the post-canine permanent dentition of four monkey groups (savannah and forest baboons, savannah and forest guenons) represented by 1,840 individuals.Papio, Mandrillus, Cercopithecus aethiops, andC. mitis each display marked within-group variation in tooth size. Taxonomic status and/or sexual composition of a sample does not correspond to a particular magnitude of variation. Therefore, the use of the coefficient of variation to assess either the specific or sexual composition of fossil samples is untenable.     

The comparative gross anatomy of the arteria cerebri media in the green monkey (Cercopithecus aethiops) and olive monkey (Papio anubis)

The gross anatomy of the arteria cerebri media inCercopithecus aethiops andPapio anubis was studied and compared statistically. Several features appeared to be species characteristic. InCercopithecus aethiops the first branch, r. striati, arose directly from the main artery, however, inPapio anubis, r. striati arose from r. orbitales the second major branch. InCercopithecus aethiops, r. orbitales and r. frontales arose by a common trunk from the a. cerebri media and inPapio anubis these two branches had separate origins. In both species r. temporales arose from two trunks, on either side of the a. sulcus centralis. Each trunk of r. temporales divided into two or three branches inCercopithecus aethiops and three or four branches inPapio anubis. The last portion of the a. cerebri media, r. parietales, divided into two trunks inCercopithecus aethiops and continued as a single trunk inPapio anubis. In the former, r. parietales sent one or two branches to the sulcus intraparietalis and sulcus lunatus while sending one branch to the gyrus postcentralis. In the latter, r. parietales sent two or three branches to the sulcus intraparietalis, three or four to the sulcus lunatus and one to the gyrus postcentralis.     

Better to Live with Allogenerics Than to Live Alone? The Case of Single Male Cercopithecus pogonias in Troops of Colobus satanas

We report the integration of single male crowned guenons (Cercopithecus pogonias) into troops of black colobus (Colobus satanas). We observed one male Cercopithecus pogonias in three troops of Colobus satanas on 30% of observation days (n = 231). Activities of single males guenons did not differ significantly from those of the colobus with which they associated. Moreover, both species performed simultaneously the same activities more often than expected by chance. Interspecific grooming occurred on several occasions. Furthermore, single male guenons spent as much in time social activities when part of a colobus troop, as they typically do when part of a conspecific group. Unlike solitary male crowned guenons, which are silent, a male that is integrated into a troop of colobus is vocal and emits social alarm calls to which colobus monkeys respond. During the single file movements of colobus troops, single male crowned guenons were integrated in the core of the troop and used the same branches at the same height with the colobus. Thus, the life of a single male crowned guenon with black colobus was social. We suggest that the main benefits that he gained is the possibility to live in a social context. Social interactions could be the key element to explain why single males Cercopithecus pogonias join troops of monkeys so different from their natal groups.     

Non-antagonistic relations between wild bonobos and two species of guenons

Interspecific relations between wild bonobos (Pan paniscus) and two species of guenons (Cercopithecus wolfi andC. ascanius) were studied at Wamba in the Central Zaire Basin from September 1989 to January 1990. Data on the guenons were collected while following parties of bonobos or when searching for them. The guenons were observed directly 59 times during the study period. In about half of these observations, the guenons were found within 20 m from the bonobo parties. The encounters between the bonobos and the guenons sometimes lasted over an hour. The guenons mainly initiated the encounters by approaching the bonobos. During the encounters, no aggressive interactions were observed between the bonobos and the guenons. Evidence of hunting by wild bonobos has been restricted to small mammals, and there has been no evidence of hunting of primates by wild bonobos. These findings and the results of the present study strongly suggest that wild bonobos do not hunt sympatric primates.     

Variation in guenon skulls (I): species divergence, ecological and genetic differences

Guenons are the most diverse clade of African monkeys. They have varied ecologies, include arboreal and terrestrial species, and can be found in nearly every region of sub-Saharan Africa. Species boundaries are often uncertain, with a variable number of species and subspecies mostly recognised on the basis of their geographic distribution and pelage. If guenon soft tissue patterns show high variability, the same does not seem to hold for skull morphology. Guenon skulls are traditionally considered relatively undifferentiated and homogeneous. However, patterns of variation in skulls have never been examined using a large number of specimens sampled across the breadth of species diversity. Thus, in the present study, skulls of adult guenons and two outgroup species are analysed using three-dimensional geometric morphometrics. Three-dimensional coordinates of 86 anatomical landmarks were measured on 1,315 adult specimens belonging to all living guenon species except Cercopithecus dryas. Species are well-discriminated using shape but the best discrimination occurs when species have either a long evolutionary history (e.g., Allenopithecus nigroviridis) or represent extremes of size variation (Miopithecus sp. and Erythrocebus patas). Interspecific phenetic relationships reflect size differences. Four main clusters are found that mainly correspond to four size groups: the smallest species (Miopithecus sp.), the largest species (E. patas plus the study outgroups), a group of medium-small arboreal guenons, and a group of medium-large arboreal and terrestrial guenons. Correlations between interspecific shape distances and interspecific differences in size are higher than between shape distances and genetic distances. However, if only the component of interspecific shape variation which is not correlated to evolutionary allometry is used in the comparison with genetic distances, correlations are up to 1.4 times larger than those including allometric shape. The smallest correlations are those between shape and ecological distances, which is consistent with the lack of clusters clearly reflecting broad ecological specialisations (e.g., arboreality versus terrestriality). Thus, size, which is generally considered more evolutionarily labile than shape, seems to have played a major role in the evolution of the guenons. The incongruence between interspecific shape differences and phylogeny might be explained by a large proportion of shape changes having occurred along allometric trajectories that tend to be conserved within this clade.     

Positional Behavior of Cercopithecus petaurista

I studied the positional behavior and habitat use of Cercopithecus petaurista, the lesser spot-nosed monkey, in the Ivory Coast's Taï Forest for 15 months. I compare these data with similar information collected on sympatric groups of Cercopithecus diana and C. campbelli in order to examine further the relationships between locomotion, posture, support use, stratal use, body size, diet, activity patterns and foraging behavior. Spot-nosed monkeys are predominantly quadrupedal primates that frequent the top layer of the understory during all maintenance activities. Locomotion is characteristically slow and cautious; travel takes place on branches and boughs while foraging occurs on twigs and branches. Postural behavior of Cercopithecus petaurista reflects their reliance on more ubiquitously distributed, less mobile food items. The relationship between body size, climbing, leaping and support use among Taï guenons is weak; interspecific differences are more likely functions of strata use and overall behavioral characteristics, e.g. crypticity. I also compare the locomotion and support use of Cercopithecus petaurista with that of C. ascanius from Uganda's Kibale Forest (Gebo and Chapman, 1995a) in order to assess the behavioral similarity of members of the same superspecies. Although overall support use is quite similar, the monkeys differ significantly in frequencies of quadrupedism, leaping and climbing. I present possible reasons for and implications of these differences.     

Behavior and serum cholesterol in a social group ofCercopithecus aethiops

This report describes the extent of associations between selected behaviors and serum cholesterol concentrations in vervets (Cercopithecus aethiops) living in a stable social group. Approximately 18% of the behaviors performed by males and 7% of behaviors performed by females demonstrated significant correlations with baseline serum cholesterol. Under conditions of dietary challenge, 11% of male behaviors and 8% of female behaviors exhibited significant correlations. Although there are sex differences in the identity of behaviors correlated with cholesterol concentrations, subordinate individuals have higher serum cholesterol levels.     

Correlates of Self-directed Behaviors in Captive <Emphasis Type="Italic">Cercopithecus aethiops</Emphasis>

Researchers have widely used self-directed behaviors (SDB) as a behavioral indicator of anxiety in nonhuman primates. We examined if SDB rates in captive vervets (Cercopithecus aethiops) were associated with 1) proximity to conspecifics in general, 2) relative dominance rank of proximity partners, and 3) postconflict situations. Subjects were members of a captive group of vervets at the Lisbon Zoo, Portugal. The group comprised 3 males and 7 females, which were focal sampled for 10.5 h each. Vervets did not engage in more SBD while in proximity of conspecifics than while alone, and individual SDB rates were not generally influenced by dominance ranks of neighbors. Yet, victims of conflicts significantly increased their SDB rates after agonistic episodes, which is consistent with the view that SDB rates are an index of anxiety in Cercopithecus aethiops.     

A case of patas-vervet hybrid in captivity

A female patas monkey (Erythrocebus patas) housed with two males of different species, Hamadryas baboon (Papio hamadryas), and vervet monkey (Cercopithecus aethiops pigerythrus), gave birth to a female offspring in a semi-open enclosure on June 11, 1975. Karyological analyses and electrophoretic examinations were carried out in order to determine the real father of the hybrid. From the results of these observations it was concluded that the father of the hybrid individual wasCercopithecus aethiops. Additionally, somatometric and hematological investigations were performed.     

Group size and group composition of the mona monkey (Cercopithecus mona) on the Island of Grenada,West Indies

Cercopithecus, the genus of guenons, is the largest of the African primate genera, and yet more than half of the species belonging to this group have never been the focus of a long-term field study. In this paper, I present data on group size and composition for a previously unstudied population of guenons on the Caribbean island of Grenada. The mona monkey, Cercopithecus mona, was introduced to Grenada from Africa approximately 200–300 years ago. Two types of social groups were found for Cercopithecus mona on Grenada: all-male groups consisting of two to four individuals and bisexual groups containing 5–32 individuals. All-male groups of Grenada mona monkeys contained any combination of juveniles, subadults, and/or adults. All-male groups were a common occurrence on Grenada but have never been reported for African C. mona and have been reported only in two other forest Cercopithecusspecies. Bisexual groups appeared to consist of one adult male, one to six adult females, subadult females, and juveniles and infants of both sexes. Even though no more than one adult male was ever seen in each bisexual group of monas on Grenada, other males were heard giving copulation calls simultaneously with resident adult male loud calls, suggesting that other males occasionally infiltrate bisexual groups. Am. J. Primatol. 43:167–173, 1997. © 1997 Wiley-Liss, Inc.     

Birth intervals ofCercopithecus monkeys of the kakamega forest,Kenya

Data on interbirth intervals are reported for two forest-living guenons,Cercopithecus mitis andC. ascanius, from a western Kenyan site. Measured intervals for females whose first offspring survived varied from 24 to 54 months (median 47,N=10) forC. mitis, and from 49 to 60 months (median 52,N=3) forC. ascanius. Intervals were shorter when the first of two offspring died. These results are supported by data on estimated intervals, in which the date of the first of two births was estimated, and incomplete intervals. Our measurements exceed previous estimates of interbirth intervals in wild populations and measured intervals of captive animals. Compared to closely related species inhabiting unpredictable and seasonal environments, these forest guenons breed very slowly indeed.     

Two incidents of venomous snakebite on juvenile blue and Sykes monkeys (Cercopithecus mitis stuhlmanni and C. m. albogularis)

Although rarely observed, predation is thought to be an important factor in the evolution of primate life histories and behavior. Here I describe two incidents of snake predation on Cercopithecus mitis guenons from Kenya. The first case involved a juvenile blue monkey (Cercopithecus mitis stuhlmanni) in the Kakamega Forest, which died following a bite by a Gaboon viper (Bitis gabonica gabonica). The snake’s attempts to ingest its prey were unsuccessful. In the second incident, a juvenile Sykes monkey (Cercopithecus mitis albogularis) at Gede Ruins National Monument died suddenly after suffering symptoms that are characteristic of bites inflicted by black mambas (Dendroaspis polylepis). In both cases circumstantial evidence suggests that attacks occurred during extended play sessions in dense vegetation on or near the ground. If so, the observations support the hypothesis that play may be a costly activity.     

Locomotor activity differences between sympatric patas monkeys (Erythrocebus patas) and vervet monkeys (Cercopithecus aethiops): Implications for the evolution of long hindlimb length in Homo

Homo erectus is notable for its taller stature and longer lower limbs relative to earlier hominids, but the selective pressures favoring such long limbs are unclear. Among anthropoid primates, patas monkeys (Erythrocebus patas) and extant hominids share several extreme characteristics involved with foraging and movement, including the relatively longest lower limb proportions, longest daily travel distances and largest home ranges for their body or group size, occupancy of some of the driest habitats, and very efficient thermoregulatory systems. We suggest that patas monkeys are an appropriate behavioral model with which to speculate on the selective pressures that might have operated on H. erectus to increase lower limb length. Here, in a comparison of the locomotor activities of patas monkeys and sympatric, closely related vervet monkeys (Cercopithecus aethiops), we provide evidence for the hypothesis that patas use their long stride more to increase foraging efficiency while walking than to run, either from predators or otherwise. Am J Phys Anthropol 105:199–207, 1998. © 1998 Wiley-Liss, Inc.     

Chromosome mapping of Miller-Diecker,Smith-Magenis and RARA loci in non-human primates: implications in the evolution of human chromosome 17

Molecular cytogenetics allows to verify chromosomal homologies previously hypothesised on the base of banding pattern comparison in different species. So far only the chromosome painting technique has been extensively used in studies of chromosomal evolution. This technique allows to detect only interchromosomal rearrangements. Human and Great Apes chromosomes basically differ by intrachromosomal rearrangements, in particular inversions; with chromosome painting it has just been possible to confirm the origin by fusion of human chromosome 2 and a reciprocal translocation in Gorilla, involving the homologous of chromosome 5 and 17. In order to verify intrachromosomal rearrangements in human chromosomal evolution, chromosome mapping of human loci in non-human primates is a useful approach. We mapped Miller-Diecker, Smith-Magenis and RARA loci localised on human chromosome 17, in Gorilla gorilla, Pongo pygmaeus, Macaca fascicularis and Cercopithecus aethiops. On the base of the obtained results it was possible to verify chromosomal rearrangements previously identified by banding, to achieve new informations about the controversial evolution of human chromosome 17, and to detect the occurrence of a paracentric inversion in the homologous in Cercopithecus aethiops.     

Banding patterns of the chromosomes of Erythrocebus patas (Schreber 1774) compared to other primate species

The karyotype of Erythrocebus patas was studied using G, Q and C bands and NOR staining and compared to those of Miopithecus talapoin, Macaca mulatta and Cercopithecus aethiops. The comparison shows a large number of homoeologies, but several chromosome pairs cannot be matched. The mechanisms that may have originated the karyotypes of these species are discussed.     

Comparative postcranial body shape and locomotion in Chlorocebus aethiops and Cercopithecus mitis

Body weight and length, chest girth, and seven postcranial limb segment lengths are compared between two guenon species, Chlorocebus (Cercopithecus) aethiops (vervets) and Cercopithecus mitis (blue monkeys), exhibiting different habitual locomotor preferences. The subjects, all adults, were wild caught for a non-related research project (Turner et al. [1986] Genetic and morphological studies on two species of Kenyan monkeys, C. aethiops and C. mitis. In: Else JG, Lee PC, editors. Primate evolution, proceedings of the Xth International Congress of Primatology, Cambridge. London). The morphological results are interpreted within the context of previously published observations of primate locomotion and social organization. The sample is unique in that the body weight of each individual is known, allowing the effects of body-size scaling to be assessed in interspecific and intersexual comparisons. C. mitis has a significantly (P < 0.05) greater body weight and trunk length than C. aethiops. A shorter trunk may function to reduce spinal flexibility for ground-running in the latter. Proximal limb segments (arm and thigh) are significantly greater in C. mitis, reflecting known adaptations to committed arboreal quadrupedal locomotion. By contrast, relative distal limb segments (forearm, crus, and foot) are significantly longer in C. aethiops, concordant with a locomotor repertoire that includes substantial terrestrial quadrupedalism, in addition to arboreal agility, and also the requisite transition between ground and canopy. Although normally associated with arboreal monkeys, greater relative tail length occurs in the more terrestrial vervets. However, because vervets exploit both arboreal and terrestrial habitats, a longer tail may compensate for diminished balance during arboreal quadrupedalism resulting from the greater "brachial" and "crural" indices that enhance their ground quadrupedalism. Most interspecific differences in body proportions are explicable by differences in locomotor modalities. Some results, however, contradict commonly held "tenets" that relate body size and morphology exclusively to locomotion. Generally associated with terrestriality, sexual dimorphism (male/female) is greater in the more arboreal blue monkeys. A more intense, seasonal mating competition may account for this incongruity.     

Diet and dominance among female vervet monkeys (Cercopithecus aethiops)

Behavioral observations of free-ranging female vervet monkeys (Cercopithecus aethiops) suggest that priority of access to food enhances individual fitness. Seventeen adult females living in two social groups were observed for 26 months in the Samburu/Isiolo Game Reserves, northern Kenya. Priority of access to feeding and sitting sites was associated with significant differences in diet and reproduction. Food species distribution altered rank-related differences in diet. Rank-related differences in diet occurred when food items were clumped in distribution, but not when they were randomly distributed. The relation of individual food items to reproduction influenced rank-related differences in reproduction. Rank was significantly correlated with birth rate when a preferred food species was clumped in distribution.     

Comparative assessment of the ischial morphology of Victoriapithecus macinnesi

An almost complete primate ischium was recovered from middle Miocene (ca. 15 ma) deposits of Maboko Island (Kenya) in 1987. The specimen shows numerous similarities to the ischial morphology of extant cercopithecids and is attributed to Victoriapithecus macinnesi (Von Koenigswald, 1969), the early Old World monkey best known from Maboko Island. The Victoriapithecus ischium provides the first evidence of early Old World monkey pelvic girdle anatomy. The ischium is characterized by an obliquely oriented and broadly flaring tuberosity, a relatively small acetabulum with little ventrally directed curvature of its caudal portion, a long ischial body and a flange-like ischial spine positioned caudal to the rim of the acetabulum. In these features, Victoriapithecus most closely resembles the vervet monkey, Cercopithecus aethiops. The fossil specimen indicates that Victoriapithecus possessed ischial callosities, a mobile tail and adaptations for (possibly cursorial) quadrupedalism with an adducted posture of the thigh. The occurrence of ischial callosities in Victoriapithecus extends the documented antiquity of this feature in catarrhines by more than 12 million years and shows that the distinctive “sitting-sleeping” adaptations of Old World monkeys (Washburn, 1957) originated prior to the divergence of Colobinae and Cercopithecinae. Differences of developmental sequence and tissue composition indicate that the ischial pads of cercopithecids, hylobatids, and pongids may have arisen independently, through parallel evolution. Contrary to Strasser and Delson (1987), discontinuity of ischial callosities was probably the primitive condition for male cercopithecids.     

Effect of different primate species on germination of Ficus (Urostigma) seeds

We examined the germination of Ficus seeds (subgenus Urostigma) after defecation by six primate species (New World monkeys, Old World monkeys, and apes). Seeds from figs (control) and primate feces were placed in a thermostatically controlled chamber for 30 days. Seeds defecated by Alouatta palliata, A. pigra, and Cercopithecus aethiops showed significantly higher germination rates than control seeds. In addition, seeds from A. palliata feces germinated significantly faster than control seeds and seeds from C. aethiops and Pan troglodytes. These differences may be due to the different digestive characteristics of the six primate species. Zoo Biol 23:273–278, 2004. © 2004 Wiley‐Liss, Inc.