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A central goal of biological anthropology is connecting environmental variation to differences in host physiology, biology, health, and evolution. The microbiome represents a valuable pathway for studying how variation in host environments impacts health outcomes. While there are many resources for learning about methods related to microbiome sample collection, laboratory analyses, and genetic sequencing, there are fewer dedicated to helping researchers navigate the dense portfolio of bioinformatics and statistical approaches for analyzing microbiome data. Those that do exist are rarely related to questions in biological anthropology and instead are often focused on human biomedicine. To address this gap, we expand on existing tutorials and provide a "road map" to aid biological anthropologists in understanding, selecting, and deploying the data analysis and visualization methods that are most appropriate for their specific research questions. Leveraging an existing dataset of fecal samples and survey data collected from wild geladas living in Simien Mountains National Park in Ethiopia (Baniel et al., 2021), this paper guides researchers toward answering three questions related to variation in the gut microbiome across host and environmental factors. By providing explanations, examples, and a reproducible workflow for different analytic methods, we move beyond the theoretical benefits of considering the microbiome within anthropological research and instead present researchers with a guide for applying microbiome science to their work. This paper makes microbiome science more accessible to biological anthropologists and paves the way for continued research into the microbiome's role in the ecology, evolution, and health of human and non‐human primates. [ABSTRACT FROM AUTHOR]

Animal gut microbiomes are critical to host physiology and fitness. The gut microbiomes of fishes—the most abundant and diverse vertebrate clade—have received little attention relative to other clades. Coral reef fishes, in particular, make up a wide range of evolutionary histories and feeding ecologies that are likely associated with gut microbiome diversity. The repeated evolution of herbivory in fishes and mammals also allows us to examine microbiome similarity in relationship to diet across the entire vertebrate tree of life. Here, we generate a large coral reef fish gut microbiome dataset (n = 499 samples, 19 species) and combine it with a diverse aggregation of public microbiome data (n = 447) to show that host diet drives significant convergence between coral reef fish and mammalian gut microbiomes. We demonstrate that this similarity is largely driven by carnivory and herbivory and that herbivorous and carnivorous hosts exhibit distinct microbial compositions across fish and mammals. We also show that fish and mammal gut microbiomes share prominent microbial taxa, including Ruminoccocus spp. and Akkermansia spp., and predicted metabolic pathways. Despite the major evolutionary and ecological differences between fishes and mammals, our results reveal that their gut microbiomes undergo similar dietary selective pressures. Thus, diet, in addition to phylosymbiosis must be considered even when comparing the gut microbiomes of distantly related hosts. [ABSTRACT FROM AUTHOR]

Primates exhibit diverse social systems that are intricately linked to their biology, behavior, and evolution, all of which influence the acquisition and maintenance of their gut microbiomes (GMs). However, most studies of wild primate populations focus on taxa with relatively large group sizes, and few consider pair‐living species. To address this gap, we investigate how a primate's social system interacts with key environmental, social, and genetic variables to shape the GM in pair‐living, red‐bellied lemurs (Eulemur rubriventer). Previous research on this species suggests that social interactions within groups influence interindividual microbiome similarity; however, the impacts of other nonsocial variables and their relative contributions to gut microbial variation remain unclear. We sequenced the 16S ribosomal RNA hypervariable V4–V5 region to characterize the GM from 26 genotyped individuals across 11 social groups residing in Ranomafana National Park, Madagascar. We estimated the degree to which sex, social group identity, genetic relatedness, dietary diversity, and home range proximity were associated with variation in the gut microbial communities residing in red‐bellied lemurs. All variables except sex played a significant role in predicting GM composition. Our model had high levels of variance inflation, inhibiting our ability to determine which variables were most predictive of gut microbial composition. This inflation is likely due to red‐bellied lemurs' pair‐living, pair‐bonded social system that leads to covariation among environmental, social, and genetic variables. Our findings highlight some of the factors that predict GM composition in a tightly bonded, pair‐living species and identify variables that require further study. We propose that future primate microbiome studies should simultaneously consider environmental, social, and genetic factors to improve our understanding of the relationships among sociality, the microbiome, and primate ecology and evolution. Research Highlights: We highlight diverse social, environmental, and genetic factors that shape the red‐bellied lemur gut microbiome (GM) and encourage additional comparative studies with other pair‐living primate species to further investigate GM variation within the context of a pair‐living social organization.Multicollinearity among predictor variables—likely due to red‐bellied lemurs' social system—hindered our ability to estimate the relative contributions of each variable in predicting GM variation.We caution future microbiome studies to assess their variables for multicollinearity before analyses. [ABSTRACT FROM AUTHOR]

Plant secondary metabolites (PSMs) are produced by plants to overcome environmental challenges, both biotic and abiotic. We were interested in characterizing how autumn seasonality in temperate and subtropical climates affects overall PSM production in comparison to herbivory. Herbivory is commonly measured between spring to summer when plants have high resource availability and prioritize growth and reproduction. However, autumn seasonality also challenges plants as they cope with limited resources and prepare survival for winter. This suggests a potential gap in our understanding of how herbivory affects PSM production in autumn compared to spring/summer. Using meta‐analysis, we recorded overall production of 22 different PSM subgroups from 58 published papers to calculate effect sizes from herbivory studies (absence to presence) and temperate to subtropical seasonal studies (summer to autumn), while considering other variables (e.g., plant type, increase in time since herbivory, temperature, and precipitation). We also compared production of five phenolic PSM subgroups – hydroxybenzoic acids, flavan‐3‐ols, flavonols, hydrolysable tannins, and condensed tannins. We wanted to detect a shared response across all PSMs and found that herbivory increased overall PSM production in herbaceous plants. Herbivory was also found to have a positive effect on individual PSM subgroups, such as flavonol production, while autumn seasonality was found to have a positive effect on flavan‐3‐ol and condensed tannin production. We discuss how these responses might stem from plants producing some PSMs constitutively, whereas others are induced only after herbivory, and how plants produce metabolites with higher costs only during seasons when other resources for growth and reproduction are less available, while other phenolic PSM subgroups serve more than one function for plants and such functions can be season dependent. The outcome of our meta‐analysis is that autumn seasonality changes some PSM production differently from herbivory, and we see value in further investigating seasonality–herbivory interactions with plant chemical defense. [ABSTRACT FROM AUTHOR]

Objectives: The gut microbiome (GM) connects physical and social environments to infant health. Since the infant GM affects immune system development, there is interest in understanding how infants acquire microbes from mothers and other household members. Materials and Methods: As a part of the Cebu Longitudinal Health and Nutrition Survey (CLHNS), we paired fecal samples (proxy for the GM) collected from infants living in Metro Cebu, Philippines at 2 weeks (N = 39) and 6 months (N = 36) with maternal interviews about prenatal household composition. We hypothesized that relationships between prenatal household size and composition and infant GM bacterial diversity (as measured in fecal samples) would vary by infant age, as well as by household member age and sex. We also hypothesized that infant GM bacterial abundances would differ by prenatal household size and composition. Results: Data from 16 S rRNA bacterial gene sequencing show that prenatal household size was the most precise estimator of infant GM bacterial diversity, and that the direction of the association between this variable and infant GM bacterial diversity changed between the two time points. The abundances of bacterial families in the infant GM varied by prenatal household variables. Conclusions: Results highlight the contributions of various household sources to the bacterial diversity of the infant GM, and suggest that prenatal household size is a useful measure for estimating infant GM bacterial diversity in this cohort. Future research should measure the effect of specific sources of household bacterial exposures, including social interactions with caregivers, on the infant GM. [ABSTRACT FROM AUTHOR]

Background and Aim: Filarial infections affect over 150 million people in the tropics. One of the major forms of filarial pathologies is lymphedema; a condition where the immune response is significantly altered, resulting in changes in the normal flora. Staphylococcus hominis, a human skin commensal, can also be pathogenic in immunocompromised individuals. Therefore, there is the possibility that S. hominis could assume a different behavior in filarial lymphedema patients. To this end, we investigated the levels of antibiotic resistance and extent of mecA gene carriage in S. hominis among individuals presenting with filarial lymphedema in rural Ghana. Method: We recruited 160 individuals with stages I–VII lymphedema, in a cross‐sectional study in the Ahanta West District of the Western Region of Ghana. Swabs from lymphedematous limb ulcers, pus, and cutaneous surfaces were cultured using standard culture‐based techniques. The culture isolates were subjected to Matrix‐Assisted Laser Desorption/Ionization Time of Flight (MALDI‐TOF) mass spectrometry for bacterial identification. Antimicrobial susceptibility testing (AST) was performed using the Kirby–Bauer method. mecA genes were targeted by polymerase chain reaction for strains that were cefoxitin resistant. Results: In all, 112 S. hominis were isolated. The AST results showed resistance to chloramphenicol (87.5%), tetracycline (83.3%), penicillin (79.2%), and trimethoprim/sulphamethoxazole (45.8%). Of the 112 strains of S. hominis, 51 (45.5%) were resistant to cefoxitin, and 37 (72.5%) of the cefoxitin‐resistant S. hominis haboured the mecA gene. Conclusion: This study indicates a heightened level of methicillin‐resistant S. hominis isolated among filarial lymphedema patients. As a result, opportunistic infections of S. hominis among the already burdened filarial lymphedema patients in rural Ghana may have reduced treatment success with antibiotics. [ABSTRACT FROM AUTHOR]

Mammals rely on the metabolic functions of their gut microbiota to meet their energetic needs and digest potentially toxic components in their diet. The gut microbiome plastically responds to shifts in host diet and may buffer variation in energy and nutrient availability. However, it is unclear how seasonal differences in the gut microbiome influence microbial metabolism and nutrients available to hosts. In this study, we examine seasonal variation in the gut metabolome of black howler monkeys (Alouatta pigra) to determine whether those variations are associated with differences in gut microbiome composition and nutrient intake, and if plasticity in the gut microbiome buffers shortfalls in energy or nutrient intake. We integrated data on the metabolome of 81 faecal samples from 16 individuals collected across three distinct seasons with gut microbiome, nutrient intake and plant metabolite consumption data from the same period. Faecal metabolite profiles differed significantly between seasons and were strongly associated with changes in plant metabolite consumption. However, microbial community composition and faecal metabolite composition were not strongly associated. Additionally, the connectivity and stability of faecal metabolome networks varied seasonally, with network connectivity being highest during the dry, fruit‐dominated season when black howler monkey diets were calorically and nutritionally constrained. Network stability was highest during the dry, leaf‐dominated season when most nutrients were being consumed at intermediate rates. Our results suggest that the gut microbiome buffers seasonal variation in dietary intake, and that the buffering effect is most limited when host diet becomes calorically or nutritionally restricted. [ABSTRACT FROM AUTHOR]

Objectives: The skin, as well as its microbial communities, serves as the primary interface between the human body and the surrounding environment. In order to implement the skin microbiome into human biology research, there is a need to explore the effects of different sample collection and storage methodologies, including the feasibility of conducting skin microbiome studies in field settings. Methods: We collected 99 skin microbiome samples from nine infants living in Veracruz, Mexico using a dual‐tipped "dry" swab on the right armpit, palm, and forehead and a "wet" swab (0.15 M NaCl and 0.1% Tween 20) on the same body parts on the left side of the body. One swab from each collection method was stored in 95% ethanol while the other was frozen at −20°C. 16S rRNA amplicon sequencing generated data on bacterial diversity and community composition, which were analyzed using PERMANOVA, linear mixed effects models, and an algorithm‐based classifier. Results: Treatment (wet_ethanol, wet_freezer, dry_ethanol, and dry_freezer) had an effect (~10% explanatory power) on the bacterial community diversity and composition of skin samples, although body site exhibited a stronger effect (~20% explanatory power). Within treatments, the collection method (wet vs. dry) affected measures of bacterial diversity to a greater degree than did the storage method (ethanol vs. freezer). Conclusions: Our study provides novel information on skin microbiome sample collection and storage methods, suggesting that ethanol storage is suitable for research in resource‐limited settings. Our results highlight the need for future study design to account for interbody site microbial variation. [ABSTRACT FROM AUTHOR]

Gut bacteria may coexist with other groups of organisms, such as nematode parasites, that inhabit the gastrointestinal tract of primates; however, the possible effects of endoparasites on bacterial communities are frequently overlooked. Here we explored whether infection with Trypanoxyuris, an oxyurid gastrointestinal parasite, is associated with changes in the gut bacterial community of wild black howler monkeys (Alouatta pigra), by comparing gut bacterial communities of consistently infected individuals and individuals that never tested positive for Trypanoxyuris throughout different months across the year. We additionally controlled for other sources of variation reported to influence the primate microbiome including individual identity, social group, and seasonality. Trypanoxyuris infection was not related to differences in gut bacterial alpha diversity, but was weakly associated with differences in gut bacterial community structure. In contrast, among the covariates considered, both individual identity and social group were more strongly associated with variation in the howler gut bacterial community. Our results suggest that gastrointestinal parasites may be associated, to some extent, with shifts in the gut bacterial communities hosted by free‐ranging primates, although a causal link still needs to be established. Further studies of wild primate hosts infected with parasite species with different pathogenicity are needed to better elucidate health‐related consequences from the parasite‐microbiome interplay. Research highlights: 1.Pinworm (Trypanoxyuris) infection was associated with slight shifts in the gut bacterial community of black howler monkeys.2.The individual ID and social group played a stronger role shaping bacterial communities in this Alouatta pigra population.3.Bacterial taxa associated with colonic inflammation were increased in parasite‐infected individuals. [ABSTRACT FROM AUTHOR]

Objectives: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late‐stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. Materials and methods: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed‐effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. Results: Late‐stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%–3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late‐stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. Discussion: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods. [ABSTRACT FROM AUTHOR]

Habitat disturbance, a common consequence of anthropogenic land use practices, creates human–animal interfaces where humans, wildlife, and domestic species can interact. These altered habitats can influence host–microbe dynamics, leading to potential downstream effects on host physiology and health. Here, we explored the effect of ecological overlap with humans and domestic species and infection with the protozoan parasite Giardia duodenalis on the bacteria of black and gold howler monkeys (Alouatta caraya), a key sentinel species, in northeastern Argentina. Fecal samples were screened for Giardia duodenalis infection using a nested PCR reaction, and the gut bacterial community was characterized using 16S rRNA gene amplicon sequencing. Habitat type was correlated with variation in A. caraya gut bacterial community composition but did not affect gut bacterial diversity. Giardia presence did not have a universal effect on A. caraya gut bacteria across habitats, perhaps due to the high infection prevalence across all habitats. However, some bacterial taxa were found to vary with Giardia infection. While A. caraya's behavioral plasticity and dietary flexibility allow them to exploit a range of habitat conditions, habitats are generally becoming more anthropogenically disturbed and, thus, less hospitable. Alterations in gut bacterial community dynamics are one possible indicator of negative health outcomes for A. caraya in these environments, since changes in host–microbe relationships due to stressors from habitat disturbance may lead to negative repercussions for host health. These dynamics are likely relevant for understanding organism responses to environmental change in other mammals. [ABSTRACT FROM AUTHOR]

Understanding the mechanisms by which organisms respond to environmental change is critical to conservation biology. Recent research indicates that the gut microbiome may mediate mammalian responses to the environment and can be used as a biomarker to understand host ecological strategies. Here, we explore the relationship between the gut microbiome, host dietary niche, and potential resilience to habitat alteration using two closely related, sympatric non‐human primate species: the tufted gray langur (Semnopithecus priam) and the purple‐faced langur (Semnopithecus vetulus). The gray langur is suspected to be a habitat generalist less perturbed by anthropogenic disturbance, while the purple‐faced langur is suspected to be a specialist more sensitive to disturbance. To test these characterizations, we assessed the gut microbiome using 16S rRNA gene amplicon sequencing of fecal samples collected from Kaludiyapokuna Forest Reserve, Sri Lanka (gray langur n = 50 samples, purple‐faced langur n = 7 samples). Our results demonstrate that despite strong gut microbial similarities, gray langurs had a more diverse gut microbiome that harbored Prevotella and Akkermansia, taxa involved in starch degradation, while the purple‐faced langur gut microbiome harbored Roseburia, Clostridium, and Ruminococcus, taxa involved in processing plant structural carbohydrates. Compared to related species in other locations, both Sri Lankan langurs harbored more pathogenic bacteria. These differences suggest that gray langurs have more generalist diets, making them more resilient to anthropogenic change, but also indicate that they are not impervious to human encroachment. Our findings suggest that microbiome analyses are an important tool for langur ecology and conservation, and should be integrated into ongoing studies. [ABSTRACT FROM AUTHOR]

Changes in reproductive status influence energy and nutrient requirements in female primates. The gut microbiota may buffer changes in energy demands, with shifts in community composition increasing the energy production potential of the gut during pregnancy and lactation. In this study, we examine changes in the gut microbiome of wild, female white‐faced capuchins (Cebus capucinus) across different reproductive states. Fecal samples (n = 39) were collected from five adult females over the course of a year. Gut microbial community composition was assessed using 16S rRNA gene sequences, and PICRUSt was used to make metagenomic functional predictions. We found a significant relationship between reproductive state and both the structure and predicted function of the gut microbiome, neither of which were associated with host diet. For example, the relative abundance of Firmicutes was significantly lower in lactating females compared with cycling females; the relative abundance of Actinobacteria was significantly higher in pregnant females compared with lactating females, and there was a trend toward higher relative abundances of Proteobacteria in pregnant females compared with cycling females. The results of this study suggest that, in addition to behavioral and dietary adaptions, the gut microbiota may play a role in allowing female primates to meet their changing energetic needs during reproduction. Further studies of the “microbial reproductive ecology” of primates will help advance our understanding of gut microbial contributions to primate energetics. [ABSTRACT FROM AUTHOR]

Objectives: Invertebrate consumption is thought to be an integral part of early hominin diets, and many modern human populations regularly consume insects and other arthropods. This study examines the response of gut microbial community structure and function to changes in diet in wild white-faced capuchins (Cebus capucinus), a primate that incorporates a large proportion of invertebrates in its diet. The goal of the study is to better understand the role of both fruit and invertebrate prey consumption on shaping primate gut microbiomes. Materials and methods: Fecal samples (n=169) and dietary data were collected over 12 months. The V3-V5 region of microbial 16S rRNA genes was amplified and sequenced. The IM-TORNADO pipeline was used to analyze sequences. Results: White-faced capuchin gut bacterial communities were characterized primarily by Firmicutes (41.6%) and Proteobacteria (39.2%). There was a significant relationship between the invertebrate diet composition of individual capuchins and their gut microbiome composition. However, there was no relationship between the fruit diet composition of individual capuchins and their gut microbiome composition, even when examining multiple timescales. Discussion: The results of our study indicate that there is a stronger relationship between gut microbial community structure and invertebrate diet composition than between gut microbial community structure and fruit consumption. As invertebrates and other animal prey play an important role in the diet of many primates, these results give important insight into the role of faunivory in shaping the evolution of host-microbe interactions in primates. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

In addition to macronutrients, foods consist of a complex set of chemical compounds that can influence dietary selectivity and consumer physiology. Metabolomics allow us to describe this complexity by quantifying all small molecules, or metabolites, in a food item. In this study we use GC-MS based metabolomics to describe the metabolite profiles of foods consumed by one population of Mexican black howler monkeys ( Alouatta pigra) over a 10-month period. Our data indicate that each food exhibited a distinct metabolite profile, and the average weekly intake of metabolites such as neochlorogenic acid and serotonin (5-hydroxytryptamine) was correlated with the consumption of certain plant parts. We speculate that these patterns result in temporal changes in howler monkey physiology such as food retention time. In contrast, variation in the weekly intake of metabolites such as oxalic acid was 70% less than variation in the concentration of the same metabolites across food items, suggesting that howler monkeys regulated the intake of these metabolites, possibly to avoid physiological consequences such as kidney stone formation. Finally, seasonal variation in the consumption of individual nutrient and non-nutrient metabolites were correlated with changes in the relative abundances of associated gut microbial taxa, implying indirect effects of food item metabolites on howler monkey nutritional ecology that likely drive foraging decisions. While additional research is needed to validate these findings, the patterns we report serve as important baseline data for understanding the effects of plant metabolites on the food choice in primates. [ABSTRACT FROM AUTHOR]

Research examining the gut microbiota is currently exploding, and results are providing new perspectives on human biology. Factors such as host diet and physiology influence the composition and function of the gut microbiota, which in turn affects human nutrition, health, and behavior via interactions with metabolism, the immune system, and the brain. These findings represent an exciting new twist on familiar topics, and as a result, gut microbiome research is likely to provide insight into unresolved biological mechanisms driving human health. However, much remains to be learned about the broader ecological and evolutionary contexts within which gut microbes and humans are affecting each other. Here, I outline the procedures for generating data describing the gut microbiota with the goal of facilitating the wider integration of microbiome analyses into studies of human biology. I describe the steps involved in sample collection, DNA extraction, PCR amplification, high-throughput sequencing, and bioinformatics. While this review serves only as an introduction to these topics, it provides sufficient resources for researchers interested in launching new microbiome initiatives. As knowledge of these methods spreads, microbiome analysis should become a standard tool in the arsenal of human biology research. [ABSTRACT FROM AUTHOR]

The gut microbiota contributes to host health by maintaining homeostasis, increasing digestive efficiency, and facilitating the development of the immune system. The composition of the gut microbiota can change dramatically within and between individuals of a species as a result of diet, age, or habitat. Therefore, understanding the factors determining gut microbiota diversity and composition can contribute to our knowledge of host ecology as well as to conservation efforts. Here we use high-throughput sequencing to describe variation in the gut microbiota of the endangered ring-tailed lemur ( Lemur catta) at the Bezà Mahafaly Special Reserve (BMSR) in southwestern Madagascar. Specifically, we measured the diversity and composition of the gut microbiota in relation to social group, age, sex, tooth wear and loss, and habitat disturbance. While we found no significant variation in the diversity of the ring-tailed lemur gut microbiota in response to any variable tested, the taxonomic composition of the gut microbiota was influenced by social group, age, and habitat disturbance. However, effect sizes were small and appear to be driven by the presence or absence of relatively low abundance taxa. These results suggest that habitat disturbance may not impact the lemur gut microbiota as strongly as it impacts the gut microbiota of other primate species, highlighting the importance of distinct host ecological and physiological factors on host-gut microbe relationships. Am. J. Primatol. 78:883-892, 2016. © 2016 Wiley Periodicals, Inc. [ABSTRACT FROM AUTHOR]

ABSTRACT The mammalian gut is home to a diverse community of microbes. Advances in technology over the past two decades have allowed us to examine this community, the gut microbiota, in more detail, revealing a wide range of influences on host nutrition, health, and behavior. These host-gut microbe interactions appear to shape host plasticity and fitness in a variety of contexts, and therefore represent a key factor missing from existing models of human and non-human primate ecology and evolution. However, current studies of the gut microbiota tend to include limited contextual data or are clinical, making it difficult to directly test broad anthropological hypotheses. Here, I review what is known about the animal gut microbiota and provide examples of how gut microbiota research can be integrated into the study of human and non-human primate ecology and evolution with targeted data collection. Specifically, I examine how the gut microbiota may impact primate diet, energetics, disease resistance, and cognition. While gut microbiota research is proliferating rapidly, especially in the context of humans, there remain important gaps in our understanding of host-gut microbe interactions that will require an anthropological perspective to fill. Likewise, gut microbiota research will be an important tool for filling remaining gaps in anthropological research. Am J Phys Anthropol 159:S196-S215, 2016. © 2016 Wiley Periodicals, Inc. [ABSTRACT FROM AUTHOR]

ABSTRACT In all mammals, growth, development, pregnancy, and lactation increase nutritional demands. Although primate field studies tend to focus on shifts in activity and diet as mechanisms to compensate for these demands, differences in digestive efficiency also are likely to be important. Because the gut microbiota can impact host digestive efficiency, we examined differences in activity budget, diet, and the gut microbial community among adult male ( N = 4), adult female ( N = 4), and juvenile ( N = 5) wild black howler monkeys ( Alouatta pigra) across a ten-month period in Palenque National Park, Mexico to determine how adult females and juveniles compensate for increased nutritional demands. Results indicate that adult females and juveniles consumed more protein and energy than adult males. Adult males, adult females, and juveniles also possessed distinct gut microbial communities, unrelated to diet. Juveniles exhibited a gut microbiota characterized by bacteria from the phylum Firmicutes, such as Roseburia and Ruminococcus, and demonstrated high fecal volatile fatty acid content, suggesting increased microbial contributions to host energy balances. Adult females possessed a higher Firmicutes to Bacteroidetes ratio, also suggesting increased energy production, and their gut microbiota was characterized by Lactococcus, which has been associated with folate biosynthesis. On the basis of these patterns, it appears that the gut microbiota differentially contributes to howler monkey nutrition during reproduction and growth. Determining the nutritional and energetic importance of shifts in activity, diet, and the gut microbiota in other nonhuman primate taxa, as well as humans, will transform our understanding of these life history processes and the role of host-microbe relationships in primate evolution. Am J Phys Anthropol 155:652-664, 2014. © 2014 Wiley Periodicals, Inc. [ABSTRACT FROM AUTHOR]

Food resources consumed by primates vary markedly in nutritional content. As a result, foragers must develop a feeding strategy to select resources that balance energy and macronutrient intake and reduce the consumption of fiber and toxins. In this study, we collected data on dietary patterns, rates of food consumption, and weight of food items consumed and combined them with published values of the nutritional content of Neotropical foods to estimate energy and nutrient intake during a 10-month period in two groups ( N = 16 individuals) of black howler monkeys ( Alouatta pigra) inhabiting Palenque National Park, Mexico. Although howler monkeys are generally assumed to exploit a leaf-dominated diet and be energy-limited, our results indicated that black howlers met their estimated energy requirements, consuming an average of 0.58 MJ of overall energy per metabolic body mass per day. The howlers also surpassed protein requirements by consuming an average of 8.2 g of protein per metabolic body mass per day. The amount of time they spent resting was not correlated with the amount of leaves or fruit in the diet or with overall energy intake. Therefore, despite consuming a leaf-heavy diet during some months of the year, black howlers do not appear to be energy-limited. Additionally, the howlers maintained a relatively consistent level of average daily protein energy intake regardless of diet composition, while non-protein energy intake varied in response to the amount of ripe fruits consumed. Although our use of published nutritional data introduces error, these findings suggest that black howler feeding ecology is more similar to other fruit-eating atelines than previously suspected, and several common assumptions regarding howler behavior and feeding ecology need to be reexamined. Am. J. Primatol. 76:774-787, 2014. © 2014 Wiley Periodicals, Inc. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Despite careful attention to animal nutrition and wellbeing, gastrointestinal distress remains relatively common in captive non‐human primates (NHPs), particularly dietary specialists such as folivores. These patterns may be a result of marked dietary differences between captive and wild settings and associated impacts on the gut microbiome. However, given that most existing studies target NHP dietary specialists, it is unclear if captive environments have distinct impacts on the gut microbiome of NHPs with different dietary niches. To begin to examine this question, we used 16S ribosomal RNA gene amplicon sequences to compare the gut microbiomes of five NHP genera categorized either as folivores (Alouatta, Colobus) or non‐folivores (Cercopithecus, Gorilla, Pan) sampled both in captivity and in the wild. Though captivity affected the gut microbiomes of all NHPs in this study, the effects were largest in folivorous NHPs. Shifts in gut microbial diversity and in the relative abundances of fiber‐degrading microbial taxa suggest that these findings are driven by marked dietary shifts for folivorous NHPs in captive settings. We propose that zoos and other captive care institutions consider including more natural browse in folivorous NHP diets and regularly bank fecal samples to further explore the relationship between NHP diet, the gut microbiome, and health outcomes. Research Highlights: Captive environments differentially affect the gut microbiomes of non‐human primates from distinct dietary niches.Folivorous non‐human primates appear to be more microbially sensitive to captive environments than those with more generalist diets.Differences in microbial sensitivity to captive environments may be associated with the magnitude of dietary shifts experienced and may also contribute to differences in the prevalence of GI distress among non‐human primate species. [ABSTRACT FROM AUTHOR]

Human evolution has been punctuated by climate anomalies, structuring environments, deadly infections, and altering landscapes. How well humans adapted to these new circumstances had direct effects on fitness and survival. Here, how the gut microbiome could have contributed to human evolutionary success through contributions to host nutritional buffering and infectious disease resistance is reviewed. How changes in human genetics, diet, disease exposure, and social environments almost certainly altered microbial community composition is also explored. Emerging research points to the microbiome as a key player in host responses to environmental change. Therefore, the reciprocal interactions between humans and their microbes are likely to have shaped human patterns of local adaptation throughout our shared evolutionary history. Recent alterations in human lifestyle, however, are altering human microbiomes in unprecedented ways. The consequences of interrupted host–microbe relationships for human adaptive potential in the future are unknown. [ABSTRACT FROM AUTHOR]

This essay, written by a biologist, a microbial ecologist, a biological anthropologist, and an anthropologist‐historian, examines tensions and translations in microbiome research on animals in the laboratory and field. The authors trace how research questions and findings in the laboratory are extrapolated into the field and vice versa, and the shifting evidentiary standards that these research settings require. Showing how complexities of microbiomes challenge traditional standards of causation, the authors contend that these challenges require new approaches to inferences used in ecology, anthropology, and history. As social scientists incorporate investigations of microbial life into their human studies, microbiome researchers venture into field settings to develop mechanistic understandings about the functions of complex microbial communities. These efforts generate new possibilities for cross‐fertilizations and inference frameworks to interpret microbiome findings. Microbiome research should integrate multiple scales, levels of variability, and other disciplinary approaches to tackle questions spanning conditions from the laboratory to the field. [ABSTRACT FROM AUTHOR]

Primate microbiome research is a quickly growing field with exciting potential for informing our understanding of primate biology, ecology, and evolution as well as host‐microbe interactions more broadly. This introductory essay to a special section of the American Journal of Primatology provides a cross‐sectional snapshot of current activity in these areas by briefly summarizing the diversity of contributed papers and their relationships to key themes in host‐associated microbiome research. It then uses this survey as a foundation for consolidating a set of key research questions to broadly guide future research. It also argues for the importance of methods standardization to facilitate comparative analyses and the identification of generalizable patterns and relationships. While primatology will benefit greatly from the integration of microbial datasets, it is uniquely positioned to address important questions regarding microbiology and macro‐ecology and evolution more generally. We are eager to see where the primate microbiome leads us. Research Highlights: Primate microbiome research is a quickly growing field with great potential.A broad set of key research questions should be used to guide future research.Efforts should be made to standardize methods across research groups.Primatology, microbiology, and macro‐ecology and evolution will all benefit from further research in this area. [ABSTRACT FROM AUTHOR]

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. Research Highlights: Wild R. brelichi microbiota is more diverse and abundant in plant degrading microbes.Starch, sugar, and mucin degrading microbes are increased in captive R. brelichi.Diet and altered microbiota may be key to the poor health of captive monkeys [ABSTRACT FROM AUTHOR]

Introduction: Social interactions shape the infant microbiome by providing opportunities for caregivers to spread bacteria through physical contact. With most research focused on the impact of maternal–infant contact on the infant gut microbiome, it is unclear how alloparents (i.e., caregivers other than the parents) influence the bacterial communities of infant body sites that are frequently contacted during bouts of caregiving, including the skin.Methods: To begin to understand how allocare may influence the diversity of the infant microbiome, detailed questionnaire data on infant–alloparent relationships and specific allocare behaviors were coupled with skin and fecal microbiome samples (four body sites) from 48 infants living in Chicago, United States.Results: Data from 16S rRNA gene amplicon sequencing indicated that infant skin and fecal bacterial diversity showed strong associations (positive and negative) to having female adult alloparents. Alloparental feeding and co‐sleeping displayed stronger associations to infant bacterial diversity compared to playing or holding. The associations with allocare behaviors differed in magnitude and direction across infant body sites. Bacterial relative abundances varied by infant–alloparent relationship and breastfeeding status.Conclusion: This study provides some of the first evidence of an association between allocare and infant skin and fecal bacterial diversity. The results suggest that infants' exposure to bacteria from the social environment may vary based on infant–alloparent relationships and allocare behaviors. Since the microbiome influences immune system development, variation in allocare that impacts the diversity of infant bacterial communities may be an underexplored dimension of the social determinants of health in early life. [ABSTRACT FROM AUTHOR]