Female Rhesus Macaques (Macaca mulatta) Sexual Skin Color Variability

Many primate species use colorful signals to communicate sexual receptivity, rank, pregnancy, health, and developmental maturity. Reproductive coloration may not be limited to signaling sexual receptivity or pregnancy, but may also communicate aspects of female quality. Our preliminary study examined the relationships between female sexual skin coloration, mating status, and female traits, including age and dominance rank. The study took place at the Cayo Santiago (CS) facility in Puerto Rico; data were collected May through August of 2006. We examined two questions: 1) Is sexual skin coloration related to mating status?; and 2) Are inter-and intra-individual color differences related to female traits? Facial coloration was not significantly related to mating status; genital saturation was significantly higher among mating females and among high-ranking females. Age was negatively correlated with both genital hue and genital saturation range; older females had more restricted coloration and younger females had more variable color. These preliminary results suggest that female coloration may reliably indicate aspects of female quality or condition to conspecifics, including potential mates

Comparative growth and static allometry in the genus Chlorocebus

Characterizing variation in growth across populations is critical to understanding multiple aspects of development in primates, including within-taxon developmental plasticity and the evolution of life history patterns. Growth in wild primates has often been reported and directly compared across larger taxonomic groups and within social groups, but comparisons are rarely investigated across widely dispersed populations of a single taxon. With the Vervet Phenome-Genome Project and the International Vervet Research Consortium, we trapped 936 vervet monkeys of all ages representing three populations (Kenyan pygerythrus, South African pygerythrus, and sabaeus from St. Kitts & Nevis). We gathered 10 different body measurements from each including mass, body breadth and length, segmental limb lengths, and chest circumference. To gain a better understanding of how ontogenetic patterns vary in these populations, we calculated bivariate allometry coefficients, derived using PCA on log-transformed and z-standardized trait values, and compared them to isometric vector coefficients. Within all population samples, around weaning age most traits showed a negative allometric relationship to body length. As each population ages, however, distinct patterns emerge, showing population differences in onset and intensity of growth among traits. In concordance with other analyses on growth in these populations, our results suggest that there exist relative differences in patterns of growth between Chlorocebus populations, further suggesting selection for unique developmental pathways in each

The static allometry of sexual and non-sexual traits in vervet monkeys

Sexual traits vary tremendously in static allometry. This variation may be explained in part by body size-related differences in the strength of selection. We tested this hypothesis in two populations of vervet monkeys, using estimates of the level of condition dependence for different morphological traits as a proxy for body size-related variation in the strength of selection. In support of the hypothesis, we found that the steepness of allometric slopes increased with the level of condition dependence. One trait of particular interest, the penis, had shallow allometric slopes and low levels of condition dependence, in agreement with one of the most consistent patterns yet detected in the study of allometry, namely that of genitalia exhibiting shallow allometries.This research was supported by NIH grant R01RR0163009

Morphological variation in the genus Chlorocebus: Ecogeographic and anthropogenically mediated variation in body mass, postcranial morphology, and growth

Objectives Direct comparative work in morphology and growth on widely dispersed wild primate taxa is rarely accomplished, yet critical to understanding ecogeographic variation, plastic local variation in response to human impacts, and variation in patterns of growth and sexual dimorphism. We investigated population variation in morphology and growth in response to geographic variables (i.e., latitude, altitude), climatic variables (i.e., temperature and rainfall), and human impacts in the vervet monkey (Chlorocebus spp.). Methods We trapped over 1,600 wild vervets from across Sub‐Saharan Africa and the Caribbean, and compared measurements of body mass, body length, and relative thigh, leg, and foot length in four well‐represented geographic samples: Ethiopia, Kenya, South Africa, and St. Kitts & Nevis. Results We found significant variation in body mass and length consistent with Bergmann\u27s Rule in adult females, and in adult males when excluding the St. Kitts & Nevis population, which was more sexually dimorphic. Contrary to Rensch\u27s Rule, although the South African population had the largest average body size, it was the least dimorphic. There was significant, although very small, variation in all limb segments in support for Allen\u27s Rule. Females in high human impact areas were heavier than those with moderate exposures, while those in low human impact areas were lighter; human impacts had no effect on males. Conclusions Vervet monkeys appear to have adapted to local climate as predicted by Bergmann\u27s and, less consistently, Allen\u27s Rule, while also responding in predicted ways to human impacts. To better understand deviations from predicted patterns will require further comparative work in vervets

Variable responses of human and non-human primate gut microbiomes to a Western diet

BACKGROUND: The human gut microbiota interacts closely with human diet and physiology. To better understand the mechanisms behind this relationship, gut microbiome research relies on complementing human studies with manipulations of animal models, including non-human primates. However, due to unique aspects of human diet and physiology, it is likely that host-gut microbe interactions operate differently in humans and non-human primates. RESULTS: Here, we show that the human microbiome reacts differently to a high-protein, high-fat Western diet than that of a model primate, the African green monkey, or vervet (Chlorocebus aethiops sabaeus). Specifically, humans exhibit increased relative abundance of Firmicutes and reduced relative abundance of Prevotella on a Western diet while vervets show the opposite pattern. Predictive metagenomics demonstrate an increased relative abundance of genes associated with carbohydrate metabolism in the microbiome of only humans consuming a Western diet. CONCLUSIONS: These results suggest that the human gut microbiota has unique properties that are a result of changes in human diet and physiology across evolution or that may have contributed to the evolution of human physiology. Therefore, the role of animal models for understanding the relationship between the human gut microbiota and host metabolism must be re-focused.P40 OD010965 - NIH HHS; P40 RR019963 - NCRR NIH HHS; P51 OD011132 - NIH HHS; R01 RR016300 - NCRR NIH HHS; 5R01RR016300 - NCRR NIH HH

Shifts in microbial diversity, composition, and functionality in the gut and genital microbiome during a natural SIV infection in vervet monkeys

BACKGROUND: The microbiota plays an important role in HIV pathogenesis in humans. Microbiota can impact health through several pathways such as increasing inflammation in the gut, metabolites of bacterial origin, and microbial translocation from the gut to the periphery which contributes to systemic chronic inflammation and immune activation and the development of AIDS. Unlike HIV-infected humans, SIV-infected vervet monkeys do not experience gut dysfunction, microbial translocation, and chronic immune activation and do not progress to immunodeficiency. Here, we provide the first reported characterization of the microbial ecosystems of the gut and genital tract in a natural nonprogressing host of SIV, wild vervet monkeys from South Africa. RESULTS: We characterized fecal, rectal, vaginal, and penile microbiomes in vervets from populations heavily infected with SIV from diverse locations across South Africa. Geographic site, age, and sex affected the vervet microbiome across different body sites. Fecal and vaginal microbiome showed marked stratification with three enterotypes in fecal samples and two vagitypes, which were predicted functionally distinct within each body site. External bioclimatic factors, biome type, and environmental temperature influenced microbiomes locally associated with vaginal and rectal mucosa. Several fecal microbial taxa were linked to plasma levels of immune molecules, for example, MIG was positively correlated with Lactobacillus and Escherichia/Shigella and Helicobacter, and IL-10 was negatively associated with Erysipelotrichaceae, Anaerostipes, Prevotella, and Anaerovibrio, and positively correlated with Bacteroidetes and Succinivibrio. During the chronic phase of infection, we observed a significant increase in gut microbial diversity, alterations in community composition (including a decrease in Proteobacteria/Succinivibrio in the gut) and functionality (including a decrease in genes involved in bacterial invasion of epithelial cells in the gut), and partial reversibility of acute infection-related shifts in microbial abundance observed in the fecal microbiome. As part of our study, we also developed an accurate predictor of SIV infection using fecal samples. CONCLUSIONS: The vervets infected with SIV and humans infected with HIV differ in microbial responses to infection. These responses to SIV infection may aid in preventing microbial translocation and subsequent disease progression in vervets, and may represent host microbiome adaptations to the virus. Video Abstract.R01 RR016300 - NCRR NIH HHS; R01 DK113919 - NIDDK NIH HHS; R01 AI119346 - NIAID NIH HHS; R01 DK119936 - NIDDK NIH HHS; R01 OD010980 - NIH HHS; IK2 CX001717 - CSRD VA; R01 HL123096 - NHLBI NIH HHS; R01 HL117715 - NHLBI NIH HHSPublished versio

Mutational Analyses of the Influenza A Virus Polymerase Subunit PA Reveal Distinct Functions Related and Unrelated to RNA Polymerase Activity

Influenza A viral polymerase is a heterotrimeric complex that consists of PA, PB1, and PB2 subunits. We previously reported that a di-codon substitution mutation (G507A-R508A), denoted J10, in the C-terminal half of PA had no apparent effect on viral RNA synthesis but prevented infectious virus production, indicating that PA may have a novel role independent of its polymerase activity. To further examine the roles of PA in the viral life cycle, we have now generated and characterized additional mutations in regions flanking the J10 site from residues 497 to 518. All tested di-codon mutations completely abolished or significantly reduced viral infectivity, but they did so through disparate mechanisms. Several showed effects resembling those of J10, in that the mutant polymerase supported normal levels of viral RNA synthesis but nonetheless failed to generate infectious viral particles. Others eliminated polymerase activity, in most cases by perturbing the normal nuclear localization of PA protein in cells. We also engineered single-codon mutations that were predicted to pack near the J10 site in the crystal structure of PA, and found that altering residues K378 or D478 each produced a J10-like phenotype. In further studies of J10 itself, we found that this mutation does not affect the formation and release of virion-like particles per se, but instead impairs the ability of those particles to incorporate each of the eight essential RNA segments (vRNAs) that make up the viral genome. Taken together, our analysis identifies mutations in the C-terminal region of PA that differentially affect at least three distinct activities: protein nuclear localization, viral RNA synthesis, and a trans-acting function that is required for efficient packaging of all eight vRNAs

Characterizing Emerging Canine H3 Influenza Viruses.

The continual emergence of novel influenza A strains from non-human hosts requires constant vigilance and the need for ongoing research to identify strains that may pose a human public health risk. Since 1999, canine H3 influenza A viruses (CIVs) have caused many thousands or millions of respiratory infections in dogs in the United States. While no human infections with CIVs have been reported to date, these viruses could pose a zoonotic risk. In these studies, the National Institutes of Allergy and Infectious Diseases (NIAID) Centers of Excellence for Influenza Research and Surveillance (CEIRS) network collaboratively demonstrated that CIVs replicated in some primary human cells and transmitted effectively in mammalian models. While people born after 1970 had little or no pre-existing humoral immunity against CIVs, the viruses were sensitive to existing antivirals and we identified a panel of H3 cross-reactive human monoclonal antibodies (hmAbs) that could have prophylactic and/or therapeutic value. Our data predict these CIVs posed a low risk to humans. Importantly, we showed that the CEIRS network could work together to provide basic research information important for characterizing emerging influenza viruses, although there were valuable lessons learned

Factors Affecting the Distribution of Copulatory Plugs in Rhesus Monkeys (Macaca mulatta) on Cayo Santiago

Although the proximate mechanisms behind the formation of copulatory plugs are well understood, their distribution and function among primates remain largely unstudied. During a study of female rhesus macaque (Macaca mulatta) mating behaviour on Cayo Santiago, we examined the pattern of the distribution of visible copulatory plugs among females and their potential relationship to female reproductive traits and sexual skin colouration. Our results indicate that non-pregnant females were observed more frequently with visible copulatory plugs than were pregnant females. Female parity status, age and rank were unrelated to copulatory plug observation. Genital colouration components were higher among females observed with copulatory plugs. We suggest that although copulatory plugs are generally thought of in terms of male physiology, plug observation may also be affected by female reproductive status

Evidence of selection in the uncoupling protein 1 gene region suggests local adaptation to solar irradiance in savannah monkeys (Chlorocebus spp.).

In the last 300 thousand years, the genus Chlorocebus expanded from equatorial Africa into the southernmost latitudes of the continent, where colder climate was a probable driver of natural selection. We investigated population-level genetic variation in the mitochondrial uncoupling protein 1 (UCP1) gene region-implicated in non-shivering thermogenesis (NST)-in 73 wild savannah monkeys from three taxa representing this southern expansion (Chlorocebus pygerythrus hilgerti, Chlorocebus cynosuros and Chlorocebus pygerythrus pygerythrus) ranging from Kenya to South Africa. We found 17 single nucleotide polymorphisms with extended haplotype homozygosity consistent with positive selective sweeps, 10 of which show no significant linkage disequilibrium with each other. Phylogenetic generalized least-squares modelling with ecological covariates suggest that most derived allele frequencies are significantly associated with solar irradiance and winter precipitation, rather than overall low temperatures. This selection and association with irradiance is demonstrated by a relatively isolated population in the southern coastal belt of South Africa. We suggest that sunbathing behaviours common to savannah monkeys, in combination with the strength of solar irradiance, may mediate adaptations to thermal stress via NST among savannah monkeys. The variants we discovered all lie in non-coding regions, some with previously documented regulatory functions, calling for further validation and research