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Molecular characterization of a novel simian immunodeficiency virus lineage (SIVtal) from northern talapoins (Miopithecus ogouensis).

Simian immunodeficiency viruses (SIVs) are found in an extensive number of African primates, and humans continue to be exposed to these viruses by hunting and handling of primate bushmeat and following occupational exposures to captive nonhuman primates. Here, we report the molecular characterization of a new SIV lineage, SIVtal, from wild-caught and captive talapoin monkeys (Miopithecus ogouensis) from Cameroon and U.S. zoos, respectively. Phylogenetic tree analyses of a small fragment in the pol gene indicated that all SIVtal strains clustered together forming a single species-specific lineage. Full-length sequence analysis for two strains, SIVtal-00CM266 and SIVtal-01CM8023, from wild-caught animals in Cameroon confirmed that SIVtal was distinct from all primate lentiviruses isolated so far and represents a new SIV lineage. Phylogenetic analyses in different viral genes showed a significant clustering of the SIVtal lineage with the Cercopithecus-specific SIVs. In addition, SIVtal and Cercopithecus-specific SIVs share functional motifs in Gag and Env that distinguish them from other primate lentiviruses. Like SIVsyk and SIVdeb, a vpu gene homologue was also absent in SIVtal. Although northern talapoins belong to the Miopithecus genus, their SIVs belong to the Cercopithecus SIV lineage, suggesting evolution from a common ancestor or cross-species transmission between both primate genera.

Amino Acid Motifs↗

Cercopithecine Y-chromosome data provide a test of competing morphological evolutionary hypotheses.

We report here the results of the first molecular evolutionary analysis to include members of all 10 extant genera of cercopithecine monkeys. A total of 44 individuals were surveyed for approximately 2.2 kb of the testis-specific protein, Y-chromosome (TSPY). The TSPY sequences were subjected to parsimony analyses in PAUP 4.0, followed by tree comparison tests designed to assess existing morphological hypotheses of cercopithecine evolution. The results of these tests show that the present Y-chromosome dataset unambiguously supports: (1) monophyly of Macaca, (2) polyphyly of the mangabeys (Cercocebus and Lophocebus), (3) paraphyly of Cercopithecus, and (4) inclusion of Allenopithecus and Miopithecus in the tribe Cercopithecini. A number of unexpected Y-chromosome relationships are also discussed, including a pattern suggesting resurrection of the genus Chlorocebus for the guenons currently identified as Erythrocebus patas, Cercopithecus aethiops, and Cercopithecus lhoesti. Relative rate tests reveal significant difference in the TSPY substitution rate across numerous lineages in the tribe Cercopithecini. Because the rate differences follow no obvious phylogenetic pattern, "local" molecular clocks were not employed and divergence dates were not estimated for this tribe. In contrast, similar analysis of the Papionini reveals rate heterogeneity between a single pair of taxonomic groups: Macaca vs. the "African papionins." Divergence dates were therefore calculated for the tribe by calibrating TSPY clocks specific to each of these two clades.

Animals↗

Myocardial bridging of the left anterior descending coronary artery in monkey hearts.

The presence of myocardial bridges over the left anterior descending coronary artery (LAD) has been studied in 55 monkey (Cercopithecus aethiops) hearts. The resemblance between the Cercopithecus LAD and the one in humans has been revealed. Cercopithecus LAD was the most frequently (70.9%) overbridged artery. The bridges were usually single. Only in 2 hearts (3.6%) LAD was overbridged by 2 MB. Their length varies from 0.5 mm to 31.6 mm (average 11.7 mm). No statistically significant sexual differences in the incidence and length of MB have been reported. Atherosclerotic lesions have been reported in overbridged parts of the vessel as well as in the subepicardial ones. Intimate correlation between the presence of myocardial bridges and atherosclerosis could not be suggested.

Animals↗

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.

Animals↗

Diurnal primate densities and biomass in the Kakamega Forest: an evaluation of census methods and a comparison with other forests.

Line-transect surveys were conducted at the Isecheno study site in the Kakamega Forest, western Kenya to estimate diurnal primate densities. The estimates from several different methods of analysis of census data were compared to "true" density values based on home range size and overlap for two species. The Whitesides method [Whitesides et al., 1988], which incorporates species-specific mean group spread into its formula for estimating transect width, provided the most accurate density estimates. The importance of including as many groups as possible when calculating density from home range size and overlap is demonstrated with long-term data from Colobus guereza and Cercopithecus mitis. Colobus guereza group density at Isecheno was much lower than that published from a recent brief study [von Hippel, 1996]. Cercopithecus mitis group density has fallen while overall population biomass appears to have remained stable over 20 years of study. Isecheno has the second highest diurnal primate biomass of the ten Guineo-Congolian rainforest sites for which biomass data are available, despite having the lowest primate species richness. Within the Guineo-Congolian rainforest system, primate biomass appears to vary to some extent between ecogeographic regions: two of three mid-elevation East African sites have high biomasses, two of two lowland West African sites have intermediate biomasses, and four of five lowland Central African sites have low biomasses. There is a strong positive correlation between total colobine biomass and total primate biomass at the ten Guineo-Congolian rainforest sites.

Animals↗

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.

Animals↗

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.

Adaptation, Biological↗

Positional behavior in five sympatric Old World monkeys.

Observations of positional behavior and habitat use were recorded on focal individuals of five species of Old World monkeys at Kibale Forest, Uganda, through the dry season of 1990 and 1991. Cercopithecus ascanius, Cercopithecus mitis, Cercocebus albigena, Colobus badius, and Colobus guereza commonly utilize five similar types of positional behavior (i.e., quadrupedalism, leaping, climbing, sitting, and standing), but in varying frequencies and situations. As a group, colobines use oblique supports and leap more often, and cover greater linear distances during leaps than do cercopithecines. Colobines also prefer to sit (about 90% of all postures), while cercopithecines stand more frequently. Body size differences between the sexes of a species are not reflected in positional behavior. The two small-bodied species climb more and leap less often than the three larger species, which is the reverse of what we would expect. Leaping is the most common method of crossing open spaces within the canopy; but most spatial gaps and leaps are over short distances, usually one meter or less. All five species, regardless of body size or the availability of forest supports, prefer medium-sized supports. Incorporating our work from Uganda with previous investigations of positional behavior reveals few consistent trends with respect to body size or habitat use across primates.

Animals↗

Seroepidemiologic, molecular, and phylogenetic analyses of simian T-cell leukemia viruses (STLV-I) from various naturally infected monkey species from central and western Africa.

A study of simian T-cell lymphoma/leukemia virus infection, conducted on 747 nonhuman primates belonging to 14 different species in Central and Western Africa, indicated that 4 species (Cercopithecus aethiops, Erythrocebus patas, Papio doguera, and Cercopithecus mona pogonias) had a high prevalence of seropositivity to simian T-cell lymphoma/leukemia virus type I (STLV-I). The other nonhuman primate species, however, had negative or low levels of anti-HTLV-I antibodies. STLV-I pol and env DNA was detected in 12 of 12 different animals among the seropositive species. However, STLV-I pX DNA could be detected in only 10 of 12 animals. Comparative phylogenetic analyses based on 140 bp sequence of the pol gene indicate that these STLV-I isolates were 0-9% divergent from each other and were 3.5-7% divergent from the prototype related human retrovirus HTLV-I (ATK). The West African STLV-I isolates formed a unique phylogenetic cluster as did most of the Central African STLV-I isolates, save for STLV-I (Tan 90). The phylogenetic data indicate that cross species transmission of HTLV-I and STLV-I continued to occur long after their ancestral strain separated from the progenitor to HTLV-II. Comparative amino acid analyses indicated that there was marked conservation of the TAX protein regardless of host species, while the pol and REX proteins exhibited increasing levels of diversity.

Africa, Central↗

Leishmania major: the suitability of East African nonhuman primates as animal models for cutaneous leishmaniasis.

The susceptibility of four species of East African nonhuman primates to experimental infection with Leishmania major was investigated. Four Syke's monkeys (Cercopithecus mitis), two vervet monkeys (Cercopithecus aethiops), two baboons (Papio cynocephalus), and two brown bushbabies (Galago garnettii) were each inoculated intradermally on the left eyelid, left ear, and nose with 0.1 ml of medium containing 1 x 10(7) promastigotes of a characterized L. major strain. All the nonhuman primates except the bushbabies developed erythema and conspicuous nodules on the eyelids and ears by 3 weeks PI. The nodules increased rapidly in size and ulceration was evident on the eyelids and ears by 49 days PI in the vervets, Syke's, and baboons. The aspirates were positive in culture or smears at 35, 49, 63, and 77 days PI. No parasites were observed in cultures or smears at 92, 105, 128, 147, and 161 days PI. The lesions in these animals began resolving by 84 days PI and were completely healed by 112 days PI. The exception was one baboon in which lesion healing did not start until around 147 days and was completely healed by 182 days PI. Cultures from the liver failed to demonstrate visceralization of the parasite in any of the animals throughout the 68 weeks of the experiment. Challenge with the same strain of L. major 6 months PI, corresponding to about 3 months after self cure, failed to produce infection in any of these experimental hosts. All the nonhuman primates except the bushbaby when challenged with the same strain of L. major at 12 months PI developed lesions and were positive for parasites at 14 and 28 days PI. Positive cultures were obtained from the eyelid and ear of one vervet up to 42 days PI. However, the lesion sizes in all these animals were smaller than in the initial infection and did not ulcerate. The nodules disappeared within 6 to 8 weeks as compared to 16 weeks in the initial infection. The histopathological appearance of the lesions varied from diffuse infiltration of plasma cells and lymphocytes which increased progressively to granulomata with epitheloid cells. This study shows that the vervets, Syke's, and the baboons are equally susceptible to L. major infection, while bushbabies are refractory. The vervets, Syke's, and baboons demonstrate a self-healing phenomenon within about 3 months which is comparable to that observed in humans infected with L. major. These three species of nonhuman primates are therefore considered as suitable models for drug or vaccine trials against human zoonotic cutaneous leishmaniasis.

Animals↗

An enzyme-linked immunosorbent assay, ELISA, for SV40 antigen detection.

The exclusion of SV40 contamination in poliovaccine produced in Cynomolgus monkey kidney cell cultures is routinely done by inoculation of the inactivated vaccine into Cercopithecus monkey kidney cell cultures where a cytopathic effect reveals the presence of the virus. An ELISA is described for the detection of SV40 antigen and the efficiency of antigen detection was compared with the development of cytopathic effect in Cercopithecus tissue cultures. The assay shortened considerably the time for production control and was in full agreement with the conventional test method.

Animals↗

Interspecies semantic communication in two forest primates.

West African Diana monkeys (Cercopithecus diana) and Campbell's monkeys (Cercopithecus campbelli) frequently form mixed-species associations. Males of both species produce acoustically distinct alarm calls to crowned eagles (Stephanoaetus coronalus) and leopards (Panthera pardus), two of their main predators. Field playback experiments were conducted to investigate whether Diana monkeys respond to Campbell's alarm calls and whether they understand the calls' semantic content. Diana monkeys responded to playback of Campbell's leopard or eagle alarm calls as though the original predator were present. In a second experiment, Diana monkeys were primed with either Campbell's eagle or leopard alarm calls and then subsequently probed with the vocalizations of a crowned eagle or a leopard. Results showed that monkeys used the semantic information conveyed by the Campbell's alarm calls to predict the presence of a predator. The data are consistent with the hypothesis that non-human primates are able to use acoustic signals of diverse origin as labels for underlying mental representations.

Animals↗

A novel simian immunodeficiency virus from black mangabey (Lophocebus aterrimus) in the Democratic Republic of Congo.

In order to understand primate lentivirus evolution, characterization of additional simian immunodeficiency virus (SIV) strains is essential. Here, an SIV from a black mangabey (Lophocebus aterrimus) originating from the Democratic Republic of Congo was analysed phylogenetically. The monkey had cross-reactive antibodies against human immunodeficiency virus type 1 (HIV-1) and HIV-2. The viral pol region sequence was amplified by nested PCR and sequence analysis confirmed that it was related to known SIV sequences. This is the first report to characterize genetically an SIV from the monkey genus Lophocebus. Phylogenetic analysis of the pol region revealed that this novel SIV, designated SIVbkm, fell into the SIVsyk and SIVgsn virus group, containing viruses isolated from the genus Cercopithecus, and suggests that cross-species transmission has occurred between species of the genera Lophocebus and Cercopithecus.

Animals↗

Relation between phylogeny of African green monkey CD4 genes and their respective simian immunodeficiency virus genes.

An apparent species-specific relatedness of SIVagm suggests a coevolution with their natural hosts. However, the exact species or subspecies classification of African green monkeys, AGM, is uncertain because current classification schemes rely on phenotype markers, while more definitive genetic data are lacking. In this study, the CD4 protein involved in tissue type recognition was genetically cloned and sequenced from PBMC RNA from all AGM species, including Barbados green monkeys (BGM). Phylogenetic trees were constructed that also included genomic CD4 nucleotide sequences from patas, sooty mangabeys, rhesus and pig-tail macaques, chimpanzees, and humans. Chimpanzees and humans consistently clustered together. Monkeys within the Cercopithecus genus formed a separate cluster which included pata monkeys, supporting its grouping as a member of Cercopithecus. Surprisingly, sooty mangabeys were genetically more closely related to Asian macaques than to other African species, which might explain why macaques are more susceptible to infection by the SIVsm group than to infection by SIVagm or HIV-1 and why patas, on the other hand, are highly susceptible to SIVagm infection. Based on CD4 genetic data, tantalus, vervets, grivets, and sabaeus formed separate subgroups with BGM grouping closely with vervets. The branching order of the AGM species was related to that of their respective SIVagm env sequences. The study suggests a strong correlation between CD4 phylogeny and the susceptibility of the host species to infection by a specific lentivirus and supports the assumption of a coevolution of SIVagm and AGM. CD4 sequencing is suggested as a relevant method for genetic determination of primate species.

Amino Acid Sequence↗

Reciprocal painting between humans, De Brazza's and patas monkeys reveals a major bifurcation in the Cercopithecini phylogenetic tree.

We report on reciprocal painting between humans and two Cercopithecini species, Erythrocebus patas (patas monkey) and Cercopithecus neglectus (De Brazza's monkey). Both human and monkeys chromosome-specific probes were made by degenerate oligonucleotide primed PCR (DOP-PCR) from flow sorted chromosomes. Metaphases of both monkey species were first hybridized with human chromosome-specific probes and then human metaphases were hybridized with chromosome paints from each monkey species. The human paint probes detected 34 homologous segments on the C. neglectus karyotype, while the C. neglectus probes, including the Y, revealed 41 homologous segments on the human karyotype. The probes specific for human chromosomes detected 29 homologous segments in the E. patas karyotype, while the patas monkey probes painted 34 segments on the human karyotype. We tested various hypotheses of Cercopithecini phylogeny and taxonomy developed by morphologists, molecular biologists and cytogeneticists. Our hybridization data confirm that fissions (both Robertsonian and non-Robertsonian) are the main mechanism driving the evolutionary trend in Cercopithecini toward higher diploid numbers and strongly suggest an early phylogenetic bifurcation in Cercopithecini. One branch leads to Cercopithecus neglectus/Cercopithecus wolfi while the other line leads to Erythrocebus patas/Chlorocebus aethiops. Allenopithecus nigroviridis may have diverged prior to this major phylogenetic node.

Animals↗

Red colobus as prey: the leaping habits of five sympatric Old World monkeys.

This study explored the leaping habits of five sympatric Old World monkeys (Colobus badius, Colobus guereza, Cercopithecus ascanius, Cercopithecus mitis and Cercocebus albigena) in an attempt to determine why chimpanzees prefer to hunt red colobus. We videotaped the leaps of the monkeys for 3 months in Uganda's Kibale National Park. Data were collected on leap preparation time as well as several other variables of the leaps. The leap preparation time of red colobus was found to be about double that of the other species studied. This difference is a likely reason why red colobus represent the preferred prey of chimpanzees. The hypothesis that red colobus spend more time in isolated trees than do other species was not supported.

Aging↗

Differential habitat utilizati of four Cercopithecidae in a Kenyan forest.

The presence of Papio cynocephalus, Cercopithecus mitis, Cercopithecus aethiops and Colobus angolensis in a small coastal forest is attributed to their differential habitat utilization. Data on diet, space-use patterns and polyspecific associations are given. Habitat partitioning is found to be resource-related and is accomplished through differential reliance on resources as well as different means of exploiting overlapping resources. The implications of the data for understanding the relationship between ecology and social structure are discussed.

Animals↗

Catarrhine photopigments are optimized for detecting targets against a foliage background.

The colour vision of many primates is trichromatic, whereas that of all other mammals is thought to be dichromatic or monochromatic. Moreover, the triplets of cone pigments in different catarrhines (Old World apes and monkeys) are strikingly similar in their spectral positions. We ask whether the selective advantage of trichromacy lies in an enhanced ability to find edible leaves or fruit. Further, we ask whether any factor in these two search tasks has constrained the particular set of cone spectral sensitivities observed in all catarrhines. We measured the spectral properties of the natural environments of six primate species in Uganda: Pan troglodytes, Cercopithecus mitis, Cercopithecus ascanius, Lophocebus albigena, Colobus guereza and Colobus badius. We concentrated on the fruit and leaves in their diets and the leaves of the trees that make up the background against which these diet items must be found. We plotted these measured stimuli in colour spaces appropriate for each primate species, and found that both frugivory and folivory are facilitated by the extra dimension of colour vision found in catarrhines but lacking in most other mammals. Furthermore, by treating the task of searching for food as a signal-detection task, we show that, of all possible combinations of cone sensitivities, the spectral positions of the actual primate pigments are optimal for finding fruit or young leaves against the background of mature leaves. This is because the variance of the chromaticities of the mature leaves is minimised in one channel of the primate's colour vision, so allowing anything that is not a mature leaf to stand out.

Algorithms↗