Characterization of a novel simian immunodeficiency virus from guereza colobus monkeys (Colobus guereza) in Cameroon: a new lineage in the nonhuman primate lentivirus family

Exploration of the diversity among primate lentiviruses is necessary to elucidate the origins and evolution of immunodeficiency viruses. During a serological survey in Cameroon, we screened 25 wild-born guereza colobus monkeys (Colobus guereza) and identified 7 with HIV/SIV cross-reactive antibodies. In this study, we describe a novel lentivirus, named SIVcol, prevalent in guereza colobus monkeys. Genetic analysis revealed that SIVcol was very distinct from all other known SIV/HIV isolates, with average amino acid identities of 40% for Gag, 50% for Pol, 28% for Env, and around 25% for proteins encoded by five other genes. Phylogenetic analyses confirmed that SIVcol is genetically distinct from other previously characterized primate lentiviruses and clusters independently, forming a novel lineage, the sixth in the current classification. Cercopithecidae monkeys (Old World monkeys) are subdivided into two subfamilies, the Colobinae and the Cercopithecinae, and, so far, all Cercopithecidae monkeys from which lentiviruses have been isolated belong to the Cercopithecinae subfamily. Therefore, SIVcol from guereza colobus monkeys (C. guereza) is the first primate lentivirus identified in the Colobinae subfamily and the divergence of SIVcol may reflect divergence of the host lineage.     

Wear striations on the incisors of ceropithecid monkeys as an index of diet and habitat preference

Wear striations on the incisors of Old World monkeys were examined in order to determine associations between the distributions of striations, diet, and habitat preference. Significant differences exist between the Cercopithe-cinae and the Colobinae in respect to the orientation of incisor wear striations. In the Colobinae striations are oriented in a predominantly mesiodistal direction. In the Cercopithecinae striations usually have a labiolingual orientation. Comparisons of terrestrial and arboreal genera indicate that significant differences exist between the two groups in respect to the density of striations on the oc-clusal wear facets of maxillary central incisors. Arboreal and terrestrial monkeys also differ in the frequency of individual incisor wear facets completely devoid of wear striations.     

Gut microbiota in wild and captive Guizhou snub‐nosed monkeys,Rhinopithecus brelichi

Many colobine species—including the endangered Guizhou snub‐nosed monkey (Rhinopithecus brelichi) are difficult to maintain in captivity and frequently exhibit gastrointestinal (GI) problems. GI problems are commonly linked to alterations in the gut microbiota, which lead us to examine the gut microbial communities of wild and captive R. brelichi. We used high‐throughput sequencing of the 16S rRNA gene to compare the gut microbiota of wild (N = 7) and captive (N = 8) R. brelichi. Wild monkeys exhibited increased gut microbial diversity based on the Chao1 but not Shannon diversity metric and greater relative abundances of bacteria in the Lachnospiraceae and Ruminococcaceae families. Microbes in these families digest complex plant materials and produce butyrate, a short chain fatty acid critical to colonocyte health. Captive monkeys had greater relative abundances of Prevotella and Bacteroides species, which degrade simple sugars and carbohydrates, like those present in fruits and cornmeal, two staples of the captive R. brelichi diet. Captive monkeys also had a greater abundance of Akkermansia species, a microbe that can thrive in the face of host malnutrition. Taken together, these findings suggest that poor health in captive R. brelichi may be linked to diet and an altered gut microbiota.     

Sequence of eruption of permanent teeth and epiphyseal union in three species of African monkeys.

Sequences of eruption of teeth and union of epiphyses determined for three species of African Cercopithecinae. These sequences are highly scalable and are highly comparable between among the species. Some sex differences in sequence were found within each species. The sequences of epiphyseal union in these species of Old World monkeys are very similar to published sequences in New World monkeys and other groups of higher primates. It appears that there is a single pattern common to the Anthropoidea as a whole.     

Pattern in craniofacial biology: Evidence from the old world monkeys (Cercopithecidae)

An understanding of craniofacial growth, both evolutionarily and clinically, requires an investigation of pattern —geometric relations that remain relatively constant among growing structures or components of the skull. Several craniofacial biologists have suggested that specific morphological relations remain invariant during growth and in interspecific comparisons of adults of varying size. We tested the hypothesized invariance of a series of craniofacial angles in a sample of adult Old World monkeys. Fifteen angles were determined from lateral cranial radiographs. Criteria for examining angular invariance included tests for significant correlations and regression slopes with palatal length (overall skull size), tests for significant mean differences (ANOVAs) in angular values between the two subfamilies of Cercopithecidae — Cercopithecinae and Colobinae — and the computation and ranking of standard deviations (SDs) and coefficients of variation (CVs). Results indicate that most of the cranial angles purported to be invariant do not in fact meet the criteria for acceptance. One of the few cranial angles that evinces a somewhat constant value is that between the posterior maxillary plane and the neutral axis of the orbits, providing very limited support for Enlow’s (1982) claim that this region represents a fundamental anatomical interface (at least within Old World monkeys). Our analysis suggests that while there may be several relatively invariant structural relations within the skull, most of those previously discussed as representing evidence of pattern in primate-wide or mammal-wide comparisons are incorrect.     

Pattern in craniofacial biology: Evidence from the old world monkeys (Cercopithecidae)

An understanding of craniofacial growth, both evolutionarily and clinically, requires an investigation of pattern —geometric relations that remain relatively constant among growing structures or components of the skull. Several craniofacial biologists have suggested that specific morphological relations remain invariant during growth and in interspecific comparisons of adults of varying size. We tested the hypothesized invariance of a series of craniofacial angles in a sample of adult Old World monkeys. Fifteen angles were determined from lateral cranial radiographs. Criteria for examining angular invariance included tests for significant correlations and regression slopes with palatal length (overall skull size), tests for significant mean differences (ANOVAs) in angular values between the two subfamilies of Cercopithecidae — Cercopithecinae and Colobinae — and the computation and ranking of standard deviations (SDs) and coefficients of variation (CVs). Results indicate that most of the cranial angles purported to be invariant do not in fact meet the criteria for acceptance. One of the few cranial angles that evinces a somewhat constant value is that between the posterior maxillary plane and the neutral axis of the orbits, providing very limited support for Enlow’s (1982) claim that this region represents a fundamental anatomical interface (at least within Old World monkeys). Our analysis suggests that while there may be several relatively invariant structural relations within the skull, most of those previously discussed as representing evidence of pattern in primate-wide or mammal-wide comparisons are incorrect.     

Y-chromosome Data and Tribal Affiliations of Allenopithecus and Miopithecus

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.     

Social structure,infant handling,and mothering styles in group-living old world monkeys

I argue that in Old World monkeys, infant handling by individuals other than the mother is a heterogeneous phenomenon in structural and functional terms; species differences in maternal tolerance of infant handling are related to differences in the relative proportion of abusive to affiliative responses made to infants by adult females other than the mother; and infant handling by adult females is related to the species-typical social structure, with particular reference to social relationships among females and patterns of food competition. I apply the proposed relationship among social structure, infant handling, and mothering style to explain the observed variation in mothering styles between and within the subfamilies Colobinae and Cercopithecinae.     

Fecal Bacterial Composition of Sichuan Snub-Nosed Monkeys (<Emphasis Type="Italic">Rhinopithecus roxellana</Emphasis>)

The intestinal microbiota plays an important role in maintaining the health of its host, including human and nonhuman primates. Little is known about the intestinal bacterial composition of the Sichuan snub-nosed monkey (Rhinopithecus roxellana), which has been classified as Endangered on the International Union for Conservation of Nature Red List since 2003. We evaluated the fecal bacterial compositions of 11 Sichuan snub-nosed monkeys, including six young captive individuals (one sample from each), three adult captive individuals (four samples each), and two adult provisioned free-ranging individuals (four samples each). We also quantified fecal Bacteroides vulgatus, Bifidobacterium spp., and Lactobacillus spp., which are defined as probiotics in humans, using real-time polymerase chain reaction. We identified five major phyla in the collected samples, including Firmicutes (32.4 %), Bacteroidetes (14.7 %), Verrucomicrobia (8.8 %), Actinobacteria (4.4 %), and unclassified microbacteria (39.7 %). Fecal bacteria composition varied with age and different seasons. The fecal bacterial composition of the captive monkeys was less variable than that of provisioned free-ranging monkeys. B. vulgatus amounts were almost 100 times higher in the provisioned free-ranging monkeys (10¹²) than in the captive monkeys (10¹⁰). Our results provide an initial catalogue of gut microbiota in the Sichuan snub-nosed monkey, which helps to enrich our knowledge of gut microbiota in nonhuman primates.     

Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities

Background

Host-associated microbes comprise an integral part of animal digestive systems and these interactions have a long evolutionary history. It has been hypothesized that the gastrointestinal microbiome of humans and other non-human primates may have played significant roles in host evolution by facilitating a range of dietary adaptations. We have undertaken a comparative sequencing survey of the gastrointestinal microbiomes of several non-human primate species, with the goal of better understanding how these microbiomes relate to the evolution of non-human primate diversity. Here we present a comparative analysis of gastrointestinal microbial communities from three different species of Old World wild monkeys.

Methodology/Principal Findings

We analyzed fecal samples from three different wild non-human primate species (black-and-white colobus [Colubus guereza], red colobus [Piliocolobus tephrosceles], and red-tailed guenon [Cercopithecus ascanius]). Three samples from each species were subjected to small subunit rRNA tag pyrosequencing. Firmicutes comprised the vast majority of the phyla in each sample. Other phyla represented were Bacterioidetes, Proteobacteria, Spirochaetes, Actinobacteria, Verrucomicrobia, Lentisphaerae, Tenericutes, Planctomycetes, Fibrobacateres, and TM7. Bray-Curtis similarity analysis of these microbiomes indicated that microbial community composition within the same primate species are more similar to each other than to those of different primate species. Comparison of fecal microbiota from non-human primates with microbiota of human stool samples obtained in previous studies revealed that the gut microbiota of these primates are distinct and reflect host phylogeny.

Conclusion/Significance

Our analysis provides evidence that the fecal microbiomes of wild primates co-vary with their hosts, and that this is manifested in higher intraspecies similarity among wild primate species, perhaps reflecting species specificity of the microbiome in addition to dietary influences. These results contribute to the limited body of primate microbiome studies and provide a framework for comparative microbiome analysis between human and non-human primates as well as a comparative evolutionary understanding of the human microbiome.     

A comparative study of gut microbiomes in captive nocturnal strepsirrhines

Feeding strategy and diet are increasingly recognized for their roles in governing primate gut microbiome (GMB) composition. Whereas feeding strategy reflects evolutionary adaptations to a host's environment, diet is a more proximate measure of food intake. Host phylogeny, which is intertwined with feeding strategy, is an additional, and often confounding factor that shapes GMBs across host lineages. Nocturnal strepsirrhines are an intriguing and underutilized group in which to examine the links between these three factors and GMB composition. Here, we compare GMB composition in four species of captive, nocturnal strepsirrhines with varying feeding strategies and phylogenetic relationships, but nearly identical diets. We use 16S rRNA sequences to determine gut bacterial composition. Despite similar husbandry conditions, including diet, we find that GMB composition varies significantly across host species and is linked to host feeding strategy and phylogeny. The GMBs of the omnivorous and the frugivorous species were significantly more diverse than were those of the insectivorous and exudativorous species. Across all hosts, GMBs were enriched for bacterial taxa associated with the macronutrient resources linked to the host's respective feeding strategy. Ultimately, the reported variation in microbiome composition suggests that the impacts of captivity and concurrent diet do not overshadow patterns of feeding strategy and phylogeny. As our understanding of primate GMBs progresses, populations of captive primates can provide insight into the evolution of host‐microbe relationships, as well as inform future captive management protocols that enhance primate health and conservation.     

Analysis of the hydrogenotrophic microbiota of wild and captive black howler monkeys (Alouatta pigra) in palenque national park, Mexico

Intestinal methanogenesis is one of the major pathways for consumption of hydrogen produced by bacterial fermentation and is considered to affect the efficiency of host energy harvest; however, little information is available regarding the hydrogenotrophic pathways of nonhuman primates in the wild, in general, and of howler monkeys, in particular. Microbial fermentation of plant structural carbohydrates is an important feature in wild howlers owing to the high fiber and low available energy content of leaves, which make up the primary component of their diet. In contrast, captive howlers may consume greater quantities of fruits and vegetables that are higher in water, lower in fiber, and, along with commercial monkey chow commonly added to captive monkey diets, more readily digestible than the natural diet. In this study, we analyzed the composition of methanogens and sulfate-reducing bacteria (SRB) from fecal samples of black howler monkeys (Alouatta pigra) in the wild and in captivity. The hydrogenotrophic microbiota of three groups of monkeys was evaluated by PCR-denaturing gradient gel electrophoresis (DGGE) fingerprinting, small clone library construction, and quantitative real-time PCR. Abundance of methanogens was lower than SRB in all howler monkey groups studied. DGGE banding patterns were highly similar within each wild and captive group but distinct among groups. Desulfovibrionales-enriched DGGE showed reduced microbial diversity in the captive animals compared with their wild counterparts. Taken together, the data demonstrate that environmental or dietary changes of the host imposed by captivity likely influence the composition of intestinal hydrogenotrophs in black howler monkeys.     

Diet strongly influences the gut microbiota of surgeonfishes

Intestinal tracts are among the most densely populated microbial ecosystems. Gut microbiota and their influence on the host have been well characterized in terrestrial vertebrates but much less so in fish. This is especially true for coral reef fishes, which are among the most abundant groups of vertebrates on earth. Surgeonfishes (family: Acanthuridae) are part of a large and diverse family of reef fish that display a wide range of feeding behaviours, which in turn has a strong impact on the reef ecology. Here, we studied the composition of the gut microbiota of nine surgeonfish and three nonsurgeonfish species from the Red Sea. High‐throughput pyrosequencing results showed that members of the phylum Firmicutes, especially of the genus Epulopiscium, were dominant in the gut microbiota of seven surgeonfishes. Even so, there were large inter‐ and intraspecies differences in the diversity of surgeonfish microbiota. Replicates of the same host species shared only a small number of operational taxonomic units (OTUs), although these accounted for most of the sequences. There was a statistically significant correlation between the phylogeny of the host and their gut microbiota, but the two were not completely congruent. Notably, the gut microbiota of three nonsurgeonfish species clustered with some surgeonfish species. The microbiota of the macro‐ and microalgavores was distinct, while the microbiota of the others (carnivores, omnivores and detritivores) seemed to be transient and dynamic. Despite some anomalies, both host phylogeny and diet were important drivers for the intestinal microbial community structure of surgeonfishes from the Red Sea.     

Gut microbiota are associated with sex and age of host: Evidence from semi‐provisioned rhesus macaques in southwest Guangxi,China

Host characteristics, such as sex and age, are closely associated with the structure and function of gut microbiota; however, less is known about the effects of age and sex on the gut microbiota of nonhuman primates, and therefore, our knowledge of interindividual variability in host gut microbiota is limited. In this study, 153 fecal samples from rhesus macaques (Macaca mulatta) were analyzed using high‐throughput 16S rRNA sequencing in order to explore associations between age and sex of the host and their gut microbiota. The results indicated that female macaques had higher alpha diversity and a more unique gut microbiota than did males. The proportion of Proteobacteria, Tenericutes, Cyanobacteria, unclassified bacteria, and Verrucomicrobia was higher in females than that in males. We also found that adults of both sexes had a higher alpha diversity, a higher proportion of norank Ruminococcaceae, Oscillospira, norank Lachnospiraceae, norank Clostridiales, and Succinivibrio, and a lower proportion of Enterococcus than immatures. Functional analyses revealed that the richness of metabolic pathways was higher in females than males and in adults compared with immatures. These results could be attributed to differences in the nutritional requirements and hormone levels of macaques of different sex and age classes. We conclude that variation in the gut microbiota of different sex and age classes of rhesus macaques may be linked to age‐ and sex‐specific differences in nutrient requirements and hormone levels. These results highlight the importance of host age and sex on the structure and function of the gut microbiota and the need to consider physiological traits when conducting studies on the gut microbiota.     

Diet drives convergent evolution of gut microbiomes in bamboo-eating species

Gut microbiota plays a critical role in host physiology and health. The coevolution between the host and its gut microbes facilitates animal adaptation to its specific ecological niche. Multiple factors such as host diet and phylogeny modulate the structure and function of gut microbiota. However, the relative contribution of each factor in shaping the structure of gut microbiota remains unclear. The giant(Ailuropoda melanoleuca) and red(Ailurus styani) pandas belong to different families of order Carnivora. They have evolved as obligate bamboo-feeders and can be used as a model system for studying the gut microbiome convergent evolution. Here, we compare the structure and function of gut microbiota of the two pandas with their carnivorous relatives using 16S rRNA and metagenome sequencing. We found that both panda species share more similarities in their gut microbiota structure with each other than each species shares with its carnivorous relatives. This indicates that the specialized herbivorous diet rather than host phylogeny is the dominant driver of gut microbiome convergence within Arctoidea.Metagenomic analysis revealed that the symbiotic gut microbiota of both pandas possesses a high level of starch and sucrose metabolism and vitamin B12 biosynthesis. These findings suggest a diet-driven convergence of gut microbiomes and provide new insight into host-microbiota coevolution of these endangered species.     

Gut microbiota composition of Japanese macaques associates with extent of human encroachment

In recent decades, human–wildlife interaction and associated anthropogenic food provisioning has been increasing and becoming more severe due to fast population growth and urban development. Noting the role of the gut microbiome in host physiology like nutrition and health, it is thus essential to understand how human–wildlife interactions and availability of anthropogenic food in habitats can affect an animal's gut microbiome. This study, therefore, set out to examine the gut microbiota of Japanese macaques (Macaca fuscata) with varying accessibility to anthropogenic food and the possibility of using gut microbiota as indicator for macaques’ reliance on anthropogenic food. Using 16S ribosomal RNA gene sequencing, we described the microbial composition of Japanese macaques experiencing different types of human disturbance and anthropogenic food availability—captive, provisioned, crop‐raiding, and wild. In terms of alpha diversity, our results showed that observed richness of gut microbiota did not differ significantly between disturbance types but among collection sites, whereas Shannon diversity index differed by both disturbance types and sites. In terms of beta diversity, captive populations harbored the most distinctive gut microbial composition, and had the greatest difference compared with wild populations. Whereas for provisioned and crop‐raiding groups, the macaques exhibited intermediate microbiota between wild and captive. We identified several potential bacterial taxa at different taxonomic ranks whose abundance potentially could help in assessing macaques’ accessibility to anthropogenic food. This study revealed the flexibility of the gut microbiome of Japanese macaques and provided possible indices based on the gut microbiome profile in assessing macaques’ accessibility to/reliance on anthropogenic foods.     

Simian homologues of human herpesvirus 8

Gamma-herpesviruses can be found in most primates including Old World an New World monkeys. The gamma-herpesvirinae are grouped into two classes: lymphocryptoviruses (gamma1) and rhadinoviruses (gamma2). The lymphocryptoviruses include Epstein-Barr virus, lymphocryptovirus of rhesus monkeys, and Herpesvirus papio of baboons. Rhadinoviruses that infect New World monkeys include Herpesvirus saimiri, whose natural host is the squirrel monkey, and Herpesvirus ateles, which infects spider monkeys. Rhadinoviruses that infect hominoids and Old World monkeys include Kaposi's sarcoma-associated herpesvirus, also known as HHV-8, and rhesus monkey rhadinovirus.     

Primate vaginal microbiomes exhibit species specificity without universal Lactobacillus dominance

Bacterial communities colonizing the reproductive tracts of primates (including humans) impact the health, survival and fitness of the host, and thereby the evolution of the host species. Despite their importance, we currently have a poor understanding of primate microbiomes. The composition and structure of microbial communities vary considerably depending on the host and environmental factors. We conducted comparative analyses of the primate vaginal microbiome using pyrosequencing of the 16S rRNA genes of a phylogenetically broad range of primates to test for factors affecting the diversity of primate vaginal ecosystems. The nine primate species included: humans (Homo sapiens), yellow baboons (Papio cynocephalus), olive baboons (Papio anubis), lemurs (Propithecus diadema), howler monkeys (Alouatta pigra), red colobus (Piliocolobus rufomitratus), vervets (Chlorocebus aethiops), mangabeys (Cercocebus atys) and chimpanzees (Pan troglodytes). Our results indicated that all primates exhibited host-specific vaginal microbiota and that humans were distinct from other primates in both microbiome composition and diversity. In contrast to the gut microbiome, the vaginal microbiome showed limited congruence with host phylogeny, and neither captivity nor diet elicited substantial effects on the vaginal microbiomes of primates. Permutational multivariate analysis of variance and Wilcoxon tests revealed correlations among vaginal microbiota and host species-specific socioecological factors, particularly related to sexuality, including: female promiscuity, baculum length, gestation time, mating group size and neonatal birth weight. The proportion of unclassified taxa observed in nonhuman primate samples increased with phylogenetic distance from humans, indicative of the existence of previously unrecognized microbial taxa. These findings contribute to our understanding of host–microbe variation and coevolution, microbial biogeography, and disease risk, and have important implications for the use of animal models in studies of human sexual and reproductive diseases.     

Primate defensins

Defensins are endogenous, cysteine-rich antimicrobial peptides that contribute to host defence against bacterial, fungal and viral infections. There are three subfamilies of defensins in primates: alpha-defensins are most common in neutrophils and Paneth cells of the small intestine; beta-defensins protect the skin and the mucous membranes of the respiratory, genitourinary and gastrointestinal tracts; and theta-defensins, which are expressed only in Old World monkeys, lesser apes and orangutans, are lectins with broad-spectrum antiviral efficacy. Here, their discovery and recent advances in understanding their properties and functions are described.     

Patterns of seasonality and group membership characterize the gut microbiota in a longitudinal study of wild Verreaux's sifakas (Propithecus verreauxi)

The intestinal microbiota plays a major role in host development, metabolism, and health. To date, few longitudinal studies have investigated the causes and consequences of microbiota variation in wildlife, although such studies provide a comparative context for interpreting the adaptive significance of findings from studies on humans or captive animals. Here, we investigate the impact of seasonality, diet, group membership, sex, age, and reproductive state on gut microbiota composition in a wild population of group‐living, frugi‐folivorous primates, Verreaux's sifakas (Propithecus verreauxi). We repeatedly sampled 32 individually recognizable animals from eight adjacent groups over the course of two different climatic seasons. We used high‐throughput sequencing of the 16S rRNA gene to determine the microbiota composition of 187 fecal samples. We demonstrate a clear pattern of seasonal variation in the intestinal microbiota, especially affecting the Firmicutes‐Bacteroidetes ratio, which may be driven by seasonal differences in diet. The relative abundances of certain polysaccharide‐fermenting taxa, for example, Lachnospiraceae, were correlated with fruit and fiber consumption. Additionally, group membership influenced microbiota composition independent of season, but further studies are needed to determine whether this pattern is driven by group divergences in diet, social contacts, or genetic factors. In accordance with findings in other wild mammals and primates with seasonally fluctuating food availability, we demonstrate seasonal variation in the microbiota of wild Verreaux's sifakas, which may be driven by food availability. This study adds to mounting evidence that variation in the intestinal microbiota may play an important role in the ability of primates to cope with seasonal variation in food availability.