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The study of the mammalian microbiome serves as a critical tool for understanding host-microbial diversity and coevolution and the impact of bacterial communities on host health. While studies of specific microbial systems (e.g., in the human gut) have rapidly increased, large knowledge gaps remain, hindering our understanding of the determinants and levels of variation in microbiomes across multiple body sites and host species. Here, we compare microbiome community compositions from eight distinct body sites among 17 phylogenetically diverse species of nonhuman primates (NHPs), representing the largest comparative study of microbial diversity across primate host species and body sites. Analysis of 898 samples predominantly acquired in the wild demonstrated that oral microbiomes were unique in their clustering, with distinctive divergence from all other body site microbiomes. In contrast, all other body site microbiomes clustered principally by host species and differentiated by body site within host species. These results highlight two key findings: (i) the oral microbiome is unique compared to all other body site microbiomes and conserved among diverse nonhuman primates, despite their considerable dietary and phylogenetic differences, and (ii) assessments of the determinants of host-microbial diversity are relative to the level of the comparison (i.e., intra-/inter-body site, -host species, and -individual), emphasizing the need for broader comparative microbial analyses across diverse hosts to further elucidate host-microbial dynamics, evolutionary and biological patterns of variation, and implications for human-microbial coevolution. IMPORTANCE The microbiome is critical to host health and disease, but much remains unknown about the determinants, levels, and evolution of host-microbial diversity. The relationship between hosts and their associated microbes is complex. Most studies to date have focused on the gut microbiome; however, large gaps remain in our understanding of host-microbial diversity, coevolution, and levels of variation in microbiomes across multiple body sites and host species. To better understand the patterns of variation and evolutionary context of host-microbial communities, we conducted one of the largest comparative studies to date, which indicated that the oral microbiome was distinct from the microbiomes of all other body sites and convergent across host species, suggesting conserved niche specialization within the Primates order. We also show the importance of host species differences in shaping the microbiome within specific body sites. This large, comparative study contributes valuable information on key patterns of variation among hosts and body sites, with implications for understanding host-microbial dynamics and human-microbial coevolution.

Compared with urban-industrial populations, small-scale human communities worldwide share a significant number of gut microbiome traits with nonhuman primates. This overlap is thought to be driven by analogous dietary triggers; however, the ecological and functional bases of this similarity are not fully understood. To start addressing this issue, fecal metagenomes of BaAka hunter-gatherers and traditional Bantu agriculturalists from the Central African Republic were profiled and compared with those of a sympatric western lowland gorilla group ( Gorilla gorilla gorilla ) across two seasons of variable dietary intake. Results show that gorilla gut microbiomes shared similar functional traits with each human group, depending on seasonal dietary behavior. Specifically, parallel microbiome traits were observed between hunter-gatherers and gorillas when the latter consumed more structural polysaccharides during dry seasons, while small-scale agriculturalist and gorilla microbiomes showed significant functional overlap when gorillas consumed more seasonal ripe fruit during wet seasons. Notably, dominance of microbial transporters, transduction systems, and gut xenobiotic metabolism was observed in association with traditional agriculture and energy-dense diets in gorillas at the expense of a functional microbiome repertoire capable of metabolizing more complex polysaccharides. Differential abundance of bacterial taxa that typically distinguish traditional from industrialized human populations (e.g., Prevotella spp.) was also recapitulated in the human and gorilla groups studied, possibly reflecting the degree of polysaccharide complexity included in each group's dietary niche. These results show conserved functional gut microbiome adaptations to analogous diets in small-scale human populations and nonhuman primates, highlighting the role of plant dietary polysaccharides and diverse environmental exposures in this convergence. IMPORTANCE The results of this study highlight parallel gut microbiome traits in human and nonhuman primates, depending on subsistence strategy. Although these similarities have been reported before, the functional and ecological bases of this convergence are not fully understood. Here, we show that this parallelism is, in part, likely modulated by the complexity of plant carbohydrates consumed and by exposures to diverse xenobiotics of natural and artificial origin. Furthermore, we discuss how divergence from these parallel microbiome traits is typically associated with adverse health outcomes in human populations living under culturally westernized subsistence patterns. This is important information as we trace the specific dietary and environmental triggers associated with the loss and gain of microbial functions as humans adapt to various dietary niches., (Copyright © 2020 Sharma et al.)

Background: Comparative data from non-human primates provide insight into the processes that shaped the evolution of the human gut microbiome and highlight microbiome traits that differentiate humans from other primates. Here, in an effort to improve our understanding of the human microbiome, we compare gut microbiome composition and functional potential in 14 populations of humans from ten nations and 18 species of wild, non-human primates., Results: Contrary to expectations from host phylogenetics, we find that human gut microbiome composition and functional potential are more similar to those of cercopithecines, a subfamily of Old World monkey, particularly baboons, than to those of African apes. Additionally, our data reveal more inter-individual variation in gut microbiome functional potential within the human species than across other primate species, suggesting that the human gut microbiome may exhibit more plasticity in response to environmental variation compared to that of other primates., Conclusions: Given similarities of ancestral human habitats and dietary strategies to those of baboons, these findings suggest that convergent ecologies shaped the gut microbiomes of both humans and cercopithecines, perhaps through environmental exposure to microbes, diet, and/or associated physiological adaptations. Increased inter-individual variation in the human microbiome may be associated with human dietary diversity or the ability of humans to inhabit novel environments. Overall, these findings show that diet, ecology, and physiological adaptations are more important than host-microbe co-diversification in shaping the human microbiome, providing a key foundation for comparative analyses of the role of the microbiome in human biology and health.

Microbiomes are vast communities of microorganisms and viruses that populate all natural ecosystems. Viruses have been considered to be the most variable component of microbiomes, as supported by virome surveys and examples of high genomic mosaicism. However, recent evidence suggests that the human gut virome is remarkably stable compared with that of other environments. Here, we investigate the origin, evolution and epidemiology of crAssphage, a widespread human gut virus. Through a global collaboration, we obtained DNA sequences of crAssphage from more than one-third of the world's countries and showed that the phylogeography of crAssphage is locally clustered within countries, cities and individuals. We also found fully colinear crAssphage-like genomes in both Old-World and New-World primates, suggesting that the association of crAssphage with primates may be millions of years old. Finally, by exploiting a large cohort of more than 1,000 individuals, we tested whether crAssphage is associated with bacterial taxonomic groups of the gut microbiome, diverse human health parameters and a wide range of dietary factors. We identified strong correlations with different clades of bacteria that are related to Bacteroidetes and weak associations with several diet categories, but no significant association with health or disease. We conclude that crAssphage is a benign cosmopolitan virus that may have coevolved with the human lineage and is an integral part of the normal human gut virome.

The study of the primate microbiome is critical in understanding the role of the microbial community in the host organism. To be able to isolate the main factors responsible for the differences observed in microbiomes within and between individuals, confounding factors due to technical variations need to be removed. To determine whether alterations due to preservatives outweigh differences due to factors such as host population, host species, body site, and habitat, we tested three methods (no preservative, 96% ethanol, and RNAlater) for preserving wild chimpanzee (fecal), wild lemur (fecal), wild vervet monkey (rectal, oral, nasal, otic, vaginal, and penile), and captive vervet monkey (rectal) samples. All samples were stored below - 20°C (short term) at the end of the field day and then at - 80°C until DNA extraction. Using 16S rRNA gene sequencing, we show a significant preservative effect on microbiota composition and diversity. Samples stored in ethanol and RNAlater appear to be less different compared with samples not stored in any preservative (none). Our differential analysis revealed significantly higher amounts of Enterococcaceae and Family XI in no preservative samples, Prevotellaceae and Spirochaetaceae in ethanol and RNAlater preserved samples, Oligosphaeraceae in ethanol-preserved samples, and Defluviitaleaceae in RNAlater preserved samples. While these preservative effects on the microbiome are not large enough to remove or outweigh the differences arising from biological factors (e.g., host species, body site, and habitat differences) they may promote misleading interpretations if they have large enough effect sizes compared to the biological factors (e.g., host population)., (© 2019 Wiley Periodicals, Inc.)

The gut microbiome of primates, including humans, is reported to closely follow host evolutionary history, with gut microbiome composition being specific to the genetic background of its primate host. However, the comparative models used to date have mainly included a limited set of closely related primates. To further understand the forces that shape the primate gut microbiome, with reference to human populations, we expanded the comparative analysis of variation among gut microbiome compositions and their primate hosts, including 9 different primate species and 4 human groups characterized by a diverse set of subsistence patterns ( n  = 448 samples). The results show that the taxonomic composition of the human gut microbiome, at the genus level, exhibits increased compositional plasticity. Specifically, we show unexpected similarities between African Old World monkeys that rely on eclectic foraging and human populations engaging in nonindustrial subsistence patterns; these similarities transcend host phylogenetic constraints. Thus, instead of following evolutionary trends that would make their microbiomes more similar to that of conspecifics or more phylogenetically similar apes, gut microbiome composition in humans from nonindustrial populations resembles that of generalist cercopithecine monkeys. We also document that wild cercopithecine monkeys with eclectic diets and humans following nonindustrial subsistence patterns harbor high gut microbiome diversity that is not only higher than that seen in humans engaging in industrialized lifestyles but also higher compared to wild primates that typically consume fiber-rich diets. IMPORTANCE The results of this study indicate a discordance between gut microbiome composition and evolutionary history in primates, calling into question previous notions about host genetic control of the primate gut microbiome. Microbiome similarities between humans consuming nonindustrialized diets and monkeys characterized by subsisting on eclectic, omnivorous diets also raise questions about the ecological and nutritional drivers shaping the human gut microbiome. Moreover, a more detailed understanding of the factors associated with gut microbiome plasticity in primates offers a framework to understand why humans following industrialized lifestyles have deviated from states thought to reflect human evolutionary history. The results also provide perspectives for developing therapeutic dietary manipulations that can reset configurations of the gut microbiome to potentially improve human health., (Copyright © 2019 Gomez et al.)

Background: Limited accessibility to intestinal epithelial tissue in wild animals and humans makes it challenging to study patterns of intestinal gene regulation, and hence to monitor physiological status and health in field conditions. To explore solutions to this limitation, we have used a noninvasive approach via fecal RNA-seq, for the quantification of gene expression markers in gastrointestinal cells of free-range primates and a forager human population. Thus, a combination of poly(A) mRNA enrichment and rRNA depletion methods was used in tandem with RNA-seq to quantify and compare gastrointestinal gene expression patterns in fecal samples of wild Gorilla gorilla gorilla (n = 9) and BaAka hunter-gatherers (n = 10) from The Dzanga Sangha Protected Areas, Central African Republic., Results: Although only a small fraction (< 4.9%) of intestinal mRNA signals was recovered, the data was sufficient to detect significant functional differences between gorillas and humans, at the gene and pathway levels. These intestinal gene expression differences were specifically associated with metabolic and immune functions. Additionally, non-host RNA-seq reads were used to gain preliminary insights on the subjects' dietary habits, intestinal microbiomes, and infection prevalence, via identification of fungi, nematode, arthropod and plant RNA., Conclusions: Overall, the results suggest that fecal RNA-seq, targeting gastrointestinal epithelial cells can be used to evaluate primate intestinal physiology and gut gene regulation, in samples obtained in challenging conditions in situ. The approach used herein may be useful to obtain information on primate intestinal health, while revealing preliminary insights into foraging ecology, microbiome, and diet.

Relationships between gastrointestinal parasites (GIPs) and the gastrointestinal microbiome (GIM) are widely discussed topics across mammalian species due to their possible impact on the host's health. GIPs may change the environment determining alterations in GIM composition. We evaluated the associations between GIP infections and fecal microbiome composition in two habituated and two unhabituated groups of wild western lowland gorillas ( Gorilla g. gorilla ) from Dzanga Sangha Protected Areas, Central African Republic. We examined 43 fecal samples for GIPs and quantified strongylid nematodes. We characterized fecal microbiome composition through 454 pyrosequencing of the V1-V3 region of the bacterial 16S rRNA gene. Entamoeba spp. infections were associated with significant differences in abundances of bacterial taxa that likely play important roles in nutrition and metabolism for the host, besides being characteristic members of the gorilla gut microbiome. We did not observe any relationships between relative abundances of several bacterial taxa and strongylid egg counts. Based on our findings, we suggest that there is a significant relationship between fecal microbiome and Entamoeba infection in wild gorillas. This study contributes to the overall knowledge about factors involved in modulating GIM communities in great apes.

Exposure to stressors can negatively impact the mammalian gastrointestinal microbiome (GIM). Here, we used 454 pyrosequencing of 16S rRNA bacterial gene amplicons to evaluate the impact of physiological stress, as evidenced by faecal glucocorticoid metabolites (FGCM; ng/g), on the GIM composition of free-ranging western lowland gorillas (Gorilla gorilla gorilla). Although we found no relationship between GIM alpha diversity (H) and FGCM levels, we observed a significant relationship between the relative abundances of particular bacterial taxa and FGCM levels. Specifically, members of the family Anaerolineaceae (ρ=0.4, FDR q=0.01), genus Clostridium cluster XIVb (ρ=0.35, FDR q=0.02) and genus Oscillibacter (ρ=0.35, FDR q=0.02) were positively correlated with FGCM levels. Thus, while exposure to stressors appears to be associated with minor changes in the gorilla GIM, the consequences of these changes are unknown. Our results may have implications for conservation biology as well as for our overall understanding of factors influencing the non-human primate GIM.

Studies of human and domestic animal models indicate that related individuals and those that spend the most time in physical contact typically have more similar gut microbial communities. However, few studies have examined these factors in wild mammals where complex social dynamics and a variety of interacting environmental factors may impact the patterns observed in controlled systems. Here, we explore the effect of host kinship and time spent in social contact on the gut microbiota of wild, black howler monkeys (Alouatta pigra). Our results indicate that closely related individuals had less similar gut microbial communities than non-related individuals. However, the effect was small. In contrast, as previously reported in baboons and chimpanzees, individuals that spent more time in contact (0 m) and close proximity (0-1 m) had more similar gut microbial communities. This pattern was driven by adult female-adult female dyads, which generally spend more time in social contact than adult male-adult male dyads or adult male-adult female dyads. Relative abundances of individual microbial genera such as Bacteroides, Clostridium, and Streptococcus were also more similar in individuals that spent more time in contact or close proximity. Overall, our data suggest that even in arboreal primates that live in small social groups and spend a relatively low proportion of their time in physical contact, social interactions are associated with variation in gut microbiota composition. Additionally, these results demonstrate that within a given host species, subgroups of individuals may interact with the gut microbiota differently.

The mammalian gastrointestinal (GI) microbiome, which plays indispensable roles in host nutrition and health, is affected by numerous intrinsic and extrinsic factors. Among them, antibiotic (ATB) treatment is reported to have a significant effect on GI microbiome composition in humans and other animals. However, the impact of ATBs on the GI microbiome of free-ranging or even captive great apes remains poorly characterized. Here, we investigated the effect of cephalosporin treatment (delivered by intramuscular dart injection during a serious respiratory outbreak) on the GI microbiome of a wild habituated group of western lowland gorillas (Gorilla gorilla gorilla) in the Dzanga Sangha Protected Areas, Central African Republic. We examined 36 fecal samples from eight individuals, including samples before and after ATB treatment, and characterized the GI microbiome composition using Illumina-MiSeq sequencing of the bacterial 16S rRNA gene. The GI microbial profiles of samples from the same individuals before and after ATB administration indicate that the ATB treatment impacts GI microbiome stability and the relative abundance of particular bacterial taxa within the colonic ecosystem of wild gorillas. We observed a statistically significant increase in Firmicutes and a decrease in Bacteroidetes levels after ATB treatment. We found disruption of the fibrolytic community linked with a decrease of Ruminoccocus levels as a result of ATB treatment. Nevertheless, the nature of the changes observed after ATB treatment differs among gorillas and thus is dependent on the individual host. This study has important implications for ecology, management, and conservation of wild primates.

Several primates show sex-based differences in activity patterns and social interactions during infancy. These differences have been associated with adult social and reproductive functions of males and females and are related to male-male competition. Our goal was to describe behavioral patterns of wild Alouatta caraya male and female infants, a species with sexual dimorphism in body size and behavioral strategies during adulthood. We also examined the relationship between life history variables, infant sex and age, activity patterns, and social interactions in order to determine whether males and females follow different trajectories during early growth. Over a 27-month study, we observed 21 male infants and 14 female infants across two similar sites in northern Argentina. Data were analyzed using generalized linear mixed model (GLMM) tests. We found no differences in suckling time or weaning age between males and females (9.7 vs. 9.4 months), but male infants spent more time feeding on solid food and resting than female infants. Males also invested more time in contact with their mothers than did female infants, and mothers rejected and broke contact with males more frequently than with females. Other behavioral categories did not differ between the sexes. Our results suggest that higher nutritional demands of males compared with females may affect some behaviors. However, mothers of sons did not experience immediate trade-offs between current and future reproduction. Other behaviors, similarly expressed by the two sexes, suggest a similar developmental trajectory between male and female A. caraya infants, meaning that most differences emerge following the infant period.

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., (© 2016 Wiley Periodicals, Inc.)

To understand how the gut microbiome is impacted by human adaptation to varying environments, we explored gut bacterial communities in the BaAka rainforest hunter-gatherers and their agriculturalist Bantu neighbors in the Central African Republic. Although the microbiome of both groups is compositionally similar, hunter-gatherers harbor increased abundance of Prevotellaceae, Treponema, and Clostridiaceae, while the Bantu gut microbiome is dominated by Firmicutes. Comparisons with US Americans reveal microbiome differences between Africans and westerners but show western-like features in the Bantu, including an increased abundance of predictive carbohydrate and xenobiotic metabolic pathways. In contrast, the hunter-gatherer gut shows increased abundance of predicted virulence, amino acid, and vitamin metabolism functions, as well as dominance of lipid and amino-acid-derived metabolites, as determined through metabolomics. Our results demonstrate gradients of traditional subsistence patterns in two neighboring African groups and highlight the adaptability of the microbiome in response to host ecology., (Copyright © 2016 The Authors. Published by Elsevier Inc. All rights reserved.)

Recent studies suggest that variation in diet across time and space results in changes in the mammalian gut microbiota. This variation may ultimately impact host ecology by altering nutritional status and health. Wild animal populations provide an excellent opportunity for understanding these interactions. However, compared to clinical studies, microbial research targeting wild animals is currently limited, and many published studies focus only on a single population of a single host species. In this study we utilize fecal samples from two species of howler monkey (Alouatta pigra and A. palliata) collected at four sites to investigate factors influencing the gut microbiota at three scales: taxonomic (host species), ecosystemic (forest type), and local (habitat disturbance/season). The results demonstrate that the effect of host species on the gut microbiota is stronger than the effect of host forest type, which is stronger than the effect of habitat disturbance or seasonality. Nevertheless, within host species, gut microbiota composition differs in response to forest type, habitat disturbance, and season. Variations in the effect size of these factors are associated both with host species and environment. This information may be beneficial for understanding ecological and evolutionary questions associated with Mesoamerican howler monkeys, as well as determining conservation challenges facing each species. These mechanisms may also provide insight into the ecology of other species of howler monkeys, non-human primates, and mammals.

Although the critical role that our gastrointestinal microbes play in host physiology is now well established, we know little about the factors that influenced the evolution of primate gut microbiomes. To further understand current gut microbiome configurations and diet-microbe co-metabolic fingerprints in primates, from an evolutionary perspective, we characterized fecal bacterial communities and metabolomic profiles in 228 fecal samples of lowland and mountain gorillas (G. g. gorilla and G. b. beringei, respectively), our closest evolutionary relatives after chimpanzees. Our results demonstrate that the gut microbiomes and metabolomes of these two species exhibit significantly different patterns. This is supported by increased abundance of metabolites and bacterial taxa associated with fiber metabolism in mountain gorillas, and enrichment of markers associated with simple sugar, lipid and sterol turnover in the lowland species. However, longitudinal sampling shows that both species' microbiomes and metabolomes converge when hosts face similar dietary constraints, associated with low fruit availability in their habitats. By showing differences and convergence of diet-microbe co-metabolic fingerprints in two geographically isolated primate species, under specific dietary stimuli, we suggest that dietary constraints triggered during their adaptive radiation were potential factors behind the species-specific microbiome patterns observed in primates today.

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.

The metabolic activities of gut microbes significantly influence host physiology; thus, characterizing the forces that modulate this micro-ecosystem is key to understanding mammalian biology and fitness. To investigate the gut microbiome of wild primates and determine how these microbial communities respond to the host's external environment, we characterized faecal bacterial communities and, for the first time, gut metabolomes of four wild lowland gorilla groups in the Dzanga-Sangha Protected Areas, Central African Republic. Results show that geographical range may be an important modulator of the gut microbiomes and metabolomes of these gorilla groups. Distinctions seemed to relate to feeding behaviour, implying energy harvest through increased fruit consumption or fermentation of highly fibrous foods. These observations were supported by differential abundance of metabolites and bacterial taxa associated with the metabolism of cellulose, phenolics, organic acids, simple sugars, lipids and sterols between gorillas occupying different geographical ranges. Additionally, the gut microbiomes of a gorilla group under increased anthropogenic pressure could always be distinguished from that of all other groups. By characterizing the interplay between environment, behaviour, diet and symbiotic gut microbes, we present an alternative perspective on primate ecology and on the forces that shape the gut microbiomes of wild primates from an evolutionary context., (© 2015 John Wiley & Sons Ltd.)

For most mammals, including nonhuman primates, diet composition varies temporally in response to differences in food availability. Because diet influences gut microbiota composition, it is likely that the gut microbiota of wild mammals varies in response to seasonal changes in feeding patterns. Such variation may affect host digestive efficiency and, ultimately, host nutrition. In this study, we investigate the temporal variation in diet and gut microbiota composition and function in two groups (N = 13 individuals) of wild Mexican black howler monkeys (Alouatta pigra) over a 10-month period in Palenque National Park, Mexico. Temporal changes in the relative abundances of individual bacterial taxa were strongly correlated with changes in host diet. For example, the relative abundance of Ruminococcaceae was highest during periods when energy intake was lowest, and the relative abundance of Butyricicoccus was highest when young leaves and unripe fruit accounted for 68 % of the diet. Additionally, the howlers exhibited increased microbial production of energy during periods of reduced energy intake from food sources. Because we observed few changes in howler activity and ranging patterns during the course of our study, we propose that shifts in the composition and activity of the gut microbiota provided additional energy and nutrients to compensate for changes in diet. Energy and nutrient production by the gut microbiota appears to provide an effective buffer against seasonal fluctuations in energy and nutrient intake for these primates and is likely to have a similar function in other mammal species.

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.

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., (© 2014 Wiley Periodicals, Inc.)

Primate gastrointestinal microbial communities are becoming increasingly appreciated for their relevance to comparative medicine and conservation, but the factors that structure primate "microbiomes" remain controversial. This study examined a community of primates in Kibale National Park, Uganda, to assess the relative importance of host species and location in structuring gastrointestinal microbiomes. Fecal samples were collected from primates in intact forest and from primates in highly disturbed forest fragments. People and livestock living nearby were also included, as was a geographically distant population of related red colobus in Kenya. A culture-free microbial community fingerprinting technique was used to analyze fecal microbiomes from 124 individual red colobus (Procolobus rufomitratus), 100 individual black-and-white colobus (Colobus guereza), 111 individual red-tailed guenons (Cercopithecus ascanius), 578 human volunteers, and 364 domestic animals, including cattle (Bos indicus and B. indicus × B. taurus crosses), goats (Caprus hircus), sheep (Ovis aries), and pigs (Sus scrofa). Microbiomes sorted strongly by host species, and forest fragmentation did not alter this pattern. Microbiomes of Kenyan red colobus sorted distinctly from microbiomes of Ugandan red colobus, but microbiomes from these two red colobus populations clustered more closely with each other than with any other species. Microbiomes from red colobus and black-and-white colobus were more differentiated than would be predicted by the phylogenetic relatedness of these two species, perhaps reflecting heretofore underappreciated differences in digestive physiology between the species. Within Kibale, social group membership influenced intra-specific variation among microbiomes. However, intra-specific variation was higher among primates in forest fragments than among primates in intact forest, perhaps reflecting the physical separation of fragments. These results suggest that, in this system, species-specific processes such as gastrointestinal physiology strongly structure microbial communities, and that primate microbiomes are relatively resistant to perturbation, even across large geographic distances or in the face of habitat disturbance., (© 2013 Wiley Periodicals, Inc.)

The primate body hosts trillions of microbes. Interactions between primate hosts and these microbes profoundly affect primate physiology, reproduction, health, survival, and ultimately, evolution. It is increasingly clear that primate health cannot be understood fully without knowledge of host-microbial interactions. Our goals here are to review what is known about microbiomes of the female reproductive tract and to explore several factors that influence variation within individuals, as well as within and between primate species. Much of our knowledge of microbial variation derives from studies of humans, and from microbes located in nonreproductive regions (e.g., the gut). We review work suggesting that the vaginal microbiota affects female health, fecundity, and pregnancy outcomes, demonstrating the selective potential for these agents. We explore the factors that correlate with microbial variation within species. Initial colonization by microbes depends on the manner of birth; most microbial variation is structured by estrogen levels that change with age (i.e., at puberty and menopause) and through the menstrual cycle. Microbial communities vary by location within the vagina and can depend on the sampling methods used (e.g., swab, lavage, or pap smear). Interindividual differences also exist, and while this variation is not completely understood, evidence points more to differences in estrogen levels, rather than differences in external physical environment. When comparing across species, reproductive-age humans show distinct microbial communities, generally dominated by Lactobacillus, unlike other primates. We develop evolutionary hypotheses to explain the marked differences in microbial communities. While much remains to be done to test these hypotheses, we argue that the ample variation in primate mating and reproductive behavior offers excellent opportunities to evaluate host-microbe coevolution and adaptation., (Copyright © 2013 Wiley Periodicals, Inc.)

The gastrointestinal (GI) microbiome contributes significantly to host nutrition and health. However, relationships involving GI microbes, their hosts and host macrohabitats remain to be established. Here, we define clear patterns of variation in the GI microbiomes of six groups of Mexican black howler monkeys (Alouatta pigra) occupying a gradation of habitats including a continuous evergreen rainforest, an evergreen rainforest fragment, a continuous semi-deciduous forest and captivity. High throughput microbial 16S ribosomal RNA gene sequencing indicated that diversity, richness and composition of howler GI microbiomes varied with host habitat in relation to diet. Howlers occupying suboptimal habitats consumed less diverse diets and correspondingly had less diverse gut microbiomes. Quantitative real-time PCR also revealed a reduction in the number of genes related to butyrate production and hydrogen metabolism in the microbiomes of howlers occupying suboptimal habitats, which may impact host health.

Background: Bacterial vaginosis (BV) is the most common vaginal disorder of reproductive-age women. Yet the cause of BV has not been established. To uncover key determinants of BV, we employed a multi-omic, systems-biology approach, including both deep 16S rRNA gene-based sequencing and metabolomics of lavage samples from 36 women. These women varied demographically, behaviorally, and in terms of health status and symptoms., Principal Findings: 16S rRNA gene-based community composition profiles reflected Nugent scores, but not Amsel criteria. In contrast, metabolomic profiles were markedly more concordant with Amsel criteria. Metabolomic profiles revealed two distinct symptomatic BV types (SBVI and SBVII) with similar characteristics that indicated disruption of epithelial integrity, but each type was correlated to the presence of different microbial taxa and metabolites, as well as to different host behaviors. The characteristic odor associated with BV was linked to increases in putrescine and cadaverine, which were both linked to Dialister spp. Additional correlations were seen with the presence of discharge, 2-methyl-2-hydroxybutanoic acid, and Mobiluncus spp., and with pain, diethylene glycol and Gardnerella spp., Conclusions: The results not only provide useful diagnostic biomarkers, but also may ultimately provide much needed insight into the determinants of BV.

Second-generation sequencing technologies have granted us greater access to the diversity and genetics of microbial communities that naturally reside endo- and ecto-symbiotically with animal hosts. Substantial research has emerged describing the diversity and broader trends that exist within and between host species and their associated microbial ecosystems, yet the application of these data to our evolutionary understanding of microbiomes appears fragmented. For the most part biological perspectives are based on limited observations of oversimplified communities, while mathematical and/or computational modeling of these concepts often lack biological precedence. In recognition of this disconnect, both fields have attempted to incorporate ecological theories, although their applicability is currently a subject of debate because most ecological theories were developed based on observations of macro-organisms and their ecosystems. For the purposes of this review, we attempt to transcend the biological, ecological and computational realms, drawing on extensive literature, to forge a useful framework that can, at a minimum be built upon, but ideally will shape the hypotheses of each field as they move forward. In evaluating the top-down selection pressures that are exerted on a microbiome we find cause to warrant reconsideration of the much-maligned theory of multi-level selection and reason that complexity must be underscored by modularity.

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.

Background: Gardnerella vaginalis is described as a common vaginal bacterial species whose presence correlates strongly with bacterial vaginosis (BV). Here we report the genome sequencing and comparative analyses of three strains of G. vaginalis. Strains 317 (ATCC 14019) and 594 (ATCC 14018) were isolated from the vaginal tracts of women with symptomatic BV, while Strain 409-05 was isolated from a healthy, asymptomatic individual with a Nugent score of 9., Principal Findings: Substantial genomic rearrangement and heterogeneity were observed that appeared to have resulted from both mobile elements and substantial lateral gene transfer. These genomic differences translated to differences in metabolic potential. All strains are equipped with significant virulence potential, including genes encoding the previously described vaginolysin, pili for cytoadhesion, EPS biosynthetic genes for biofilm formation, and antimicrobial resistance systems, We also observed systems promoting multi-drug and lantibiotic extrusion. All G. vaginalis strains possess a large number of genes that may enhance their ability to compete with and exclude other vaginal colonists. These include up to six toxin-antitoxin systems and up to nine additional antitoxins lacking cognate toxins, several of which are clustered within each genome. All strains encode bacteriocidal toxins, including two lysozyme-like toxins produced uniquely by strain 409-05. Interestingly, the BV isolates encode numerous proteins not found in strain 409-05 that likely increase their pathogenic potential. These include enzymes enabling mucin degradation, a trait previously described to strongly correlate with BV, although commonly attributed to non-G. vaginalis species., Conclusions: Collectively, our results indicate that all three strains are able to thrive in vaginal environments, and therein the BV isolates are capable of occupying a niche that is unique from 409-05. Each strain has significant virulence potential, although genomic and metabolic differences, such as the ability to degrade mucin, indicate that the detection of G. vaginalis in the vaginal tract provides only partial information on the physiological potential of the organism.

Previous studies of resistance gene ecology have focused primarily on populations such as hospital patients and farm animals that are regularly exposed to antibiotics. Also, these studies have tended to focus on numerically minor populations such as enterics or enterococci. We report here a cultivation-independent approach that allowed us to assess the presence of antibiotic resistance genes in the numerically predominant populations of the vaginal microbiota of two populations of primates that are seldom or never exposed to antibiotics: baboons and mangabeys. Most of these animals were part of a captive colony in Texas that is used for scientific studies of female physiology and physical anthropology topics. Samples from some wild baboons were also tested. Vaginal swab samples, obtained in connection with a study designed to define the normal microbiota of the female vaginal canal, were tested for the presence of two types of antibiotic resistance genes: tetracycline resistance (tet) genes and erythromycin resistance (erm) genes. These genes are frequently found in human isolates of the two types of bacteria that were a substantial part of the normal microbiota of primates (Firmicutes and Bacteroidetes). Since cultivation was not feasible, polymerase chain reaction and DNA sequencing were used to detect and characterize these resistance genes. The tet(M) and tet(W) genes were found most commonly, and the tet(Q) gene was found in over a third of the samples from baboons. The ermB and ermF genes were found only in a minority of the samples. The ermG gene was not found in any of the specimens tested. Polymerase chain reaction analysis showed that at least some tet(M) and tet(Q) genes were genetically linked to DNA from known conjugative transposons (CTns), Tn916 and CTnDOT. Our results raise questions about the extent to which extensive exposure to antibiotics is the only pressure necessary to maintain resistance genes in natural settings.

Background: Methanogenesis by methanogenic Archaea and sulfate reduction by sulfate reducing bacteria (SRB) are the major hydrogenotrophic pathways in the human colon. Methanogenic status of mammals is suggested to be under evolutionary rather than dietary control. However, information is lacking regarding the dynamics of hydrogenotrophic microbial communities among different primate species., Methods: Rectal swabs were collected from 10 sooty mangabeys (Cercocebus atys) and 10 baboons (Papio hamadryas). The diversity and abundance of methanogens and SRB were examined using PCR-denaturing gradient gel electrophoresis (DGGE) and real-time quantitative PCR (qPCR)., Results: The DGGE results revealed that intestinal Archaea and SRB communities differ between mangabeys and baboons. Phylogenetic analyses of Archaea DGGE bands revealed two distinct clusters with one representing a putative novel order of methanogenic Archaea. The qPCR detected a similar abundance of methanogens and SRB., Conclusions: Intestinal Archaea and SRB coexist in these primates, and the community patterns are host species-specific.

Recent culture-independent studies have revealed that a healthy vaginal ecosystem harbors a surprisingly complex assemblage of microorganisms. However, the spatial distribution and composition of vaginal microbial populations have not been investigated using molecular methods. Here, we evaluated site-specific microbial composition within the vaginal ecosystem and examined the influence of sampling technique in detection of the vaginal microbiota. 16S rRNA gene clone libraries were prepared from samples obtained from different locations (cervix, fornix, outer vaginal canal) and by different methods (swabbing, scraping, lavaging) from the vaginal tracts of eight clinically healthy, asymptomatic women. The data reveal that the vaginal microbiota is not homogenous throughout the vaginal tract but differs significantly within an individual with regard to anatomical site and sampling method used. Thus, this study illuminates the complex structure of the vaginal ecosystem and calls for the consideration of microenvironments when sampling vaginal microbiota as a clinical predictor of vaginal health.

Sexual selection theory explains the evolution of exaggerated male morphologies and weaponry, but the fitness consequences of developmental and age-related changes in these features remain poorly understood. This long-term study of mandrill monkeys (Mandrillus sphinx) demonstrates how age-related changes in canine tooth weaponry and adult canine size correlate closely with male lifetime reproductive success. Combining long-term demographic and morphometric data reveals that male fitness covaries simply and directly with canine ontogeny, adult maximum size, and wear. However, fitness is largely independent of other somatometrics. Male mandrills sire offspring almost exclusively when their canines exceed approximately 30 mm, or two-thirds of average adult value (45 mm). Moreover, sires have larger canines than nonsires. The tooth diminishes through wear as animals age, corresponding with, and perhaps influencing, reproductive senescence. These factors combine to constrain male reproductive opportunities to a brief timespan, defined by the period of maximum canine length. Sexually-selected weaponry, especially when it is nonrenewable like the primate canine tooth, is intimately tied to the male life course. Our analyses of this extremely dimorphic species indicate that sexual selection is closely intertwined with growth, development, and aging, pointing to new directions for sexual selection theory. Moreover, the primate canine tooth has potential as a simple mammalian system for testing genetically-based models of aging. Finally, the tooth may record details of life histories in fossil primates, especially when sexual selection has played a role in the evolution of dimorphism.

This study investigates the relationship between serum hormone levels and morphometrics during ontogeny in olive baboons (Papio hamadryas anubis) and sooty mangabeys (Cercocebus atys), to test hypotheses about the endocrine regulation of species size differences. First, we expect that levels of hormones and binding proteins predict size change during ontogeny in both species. Second, a high level of integration among the hormones and binding proteins analyzed is expected, with the implication that they act in combination to influence the development of body size and shape. Utilizing a mixed longitudinal sample, we compare change in 18 different measurements, which reflect overall size growth as well as growth in length and circumference, with levels of six growth-related hormones and binding proteins. We examine the relationship between hormone and binding protein levels and morphometrics, using multivariate analyses and "arithmetically-estimated" velocity curves of hormones, binding proteins, to characterize how the endocrine factors analyzed relate to growth. Results suggest that levels of these endocrine factors can be used to predict local and overall growth during ontogeny and that integration between multiple hormone axes is indicated. While important for growth in both species, ontogenetic changes in hormone and binding protein levels are more tightly correlated with changes in morphometric measurements in baboons than mangabeys. These results have important implications for understanding why some smaller-bodied species have higher absolute growth-related hormone levels than larger-bodied species., (Copyright 2008 Wiley-Liss, Inc.)

Recent advances in developmental biology reveal that patterns of morphological development, even during early phases, may be highly susceptible to evolutionary change. Consequently, developmental data may be uninformative with regard to distinguishing homology and homoplasy. The present analysis evaluates postnatal ontogeny in papionin primates to test hypotheses about homology and homoplasy during later periods of development. Specifically, the analysis studies the allometric bases of craniometric resemblances among four papionin genera to test the hypothesis that homoplasy in adult cranial form, particularly of baboons (Papio) and mandrills (Mandrillus), is underwritten by divergent patterns of development. Bivariate and multivariate allometric analyses demonstrate that the developmental patterns in Papio baboons diverge markedly from ontogenetic allometric trajectories in other papionin species. The resemblances between Papio and Mandrillus (assuming that patterns of development in smaller papionins are ancestral) are largely consequences of perinatal increases in relative brain size in juvenile Papio. Postnatal growth to large size and strong negative allometry of neurocranial form results in shape similarities because developmental pathways for large papionin genera intersect. Analyses show that allometric data may not be particularly informative in revealing homoplasy. However, placed into proper phylogenetic context, such data illustrate derived patterns of development that may reflect critically important life-history or ontogenetic adaptations.

This study examines the evolution of size differences among papionin primates by measuring hormones that regulate size growth during ontogeny and influence ultimate adult size (insulin-like growth factor-I (IGF-I), insulin-like growth factor binding protein-3 (IGFBP-3), growth hormone binding protein (GHBP), dehydroepiandrosterone sulfate (DHEAS), testosterone, estradiol). The analyses assess longstanding ideas about circulating hormone levels and body size. Importantly, because the consensus papionin molecular phylogeny implies at least two episodes of size increase, this study offers opportunities to determine whether or not similar hormone profiles regulate this apparent evolutionary convergence (i.e., do larger-bodied papionins have higher levels of growth-related hormones than smaller-bodied papionins?). Five hundred and sixty serum samples (from 161 individuals) from 11 papionin species were analyzed using a two-level approach to address this issue. One used mixed longitudinal samples from two papionin species to test whether, during growth, large- and small-bodied species have higher and lower hormone levels, respectively. The second compared multiple papionin species to assess whether or not hormone levels covary with size in adult animals. Result show that size and hormone levels do not covary consistently across papionins, either during growth or in adulthood. Specifically, some smaller-bodied papionin species have higher absolute hormone levels than larger-bodied species. Differences in some hormone levels appear to track phylogeny more closely than body size. In contrast to studies based on single species, we demonstrate that, while the hormones analyzed affect growth, absolute circulating hormone levels either during growth or adulthood may be decoupled from interspecific differences in body size., (Copyright 2006 Wiley-Liss, Inc.)

Buried in the same South African cave deposits as Australopithecus, fossil papionins have been referred to Parapapio (Pp. whitei, Pp. broomi, Pp. jonesi, Pp. antiquus), Papio (P. izodi, P. angusticeps, P. h. robinsoni), Theropithecus (e.g., T. darti), Gorgopithecus, or Dinopithecus on the basis of postcanine tooth size and descriptive morphology of the muzzle. The morphological patterns of variation that these papionins demonstrate can help to place the Australopithecus fossils into a biochronological context and provide valuable information for reconstructing regional Plio-Pleistocene turnover. To document these patterns of variation across fossil-bearing sites, we explore morphometric affinities within Parapapio, and between Parapapio and other Plio-Pleistocene taxa (Dinopithecus ingens, Papio angusticeps, Papio izodi, and Theropithecus darti) by analyzing a sample of interlandmark distances derived from 3-D coordinate data of the most complete fossil papionin specimens available. Bivariate and multivariate analyses show that Pp. whitei exhibits as much variation between sites and between individuals as Pp. broomi and Pp. whitei combined. Diversity in Parapapio at Makapansgat and Sterkfontein may suggest substantial time depth to the caves. Theropithecus darti, Dinopithecus ingens, Papio angusticeps, Pp. whitei from Bolt's Farm (BF 43), and Pp. jonesi from Sterkfontein (STS 565) differ considerably from one another. Other Parapapio specimens across sites form a separate cluster with P. izodi from Taung, suggesting a Pliocene age for this site., (Copyright 2006 Wiley-Liss, Inc.)

Cranial form in subspecies of Papio baboons (Papio hamadryas) varies in relation to size, geography, and sex. However, knowledge about this variation is based mainly on adults, precluding direct assessments of the evolutionary factors that are ultimately responsible for adult shape variation. Consequently, this study tests hypotheses about the development of size and shape differences among subspecies of Papio baboons, anticipating limited evolutionary divergences in the ontogenetic pathways leading to adult endpoints. Geometric morphometric and bivariate allometric analyses are used to explore developmental size and shape variation. Allometric scaling in adult Papio baboons occurs because both sexes and all subspecies follow similar developmental pathways to a variety of adult forms. However, complex allometry contributes to form differences, producing potentially important shape differences that emerge during development. Modest shape differences that are statistically independent of size distinguish chacma baboons (P. h. ursinus) from other forms. A small-headed subspecies, the Kinda baboon (P. h. kindae), also presents a distinctive ontogeny, and may provide insights into the evolution of size change in this species. Variation among subspecies that is statistically independent of size involves the rostrum, zygomatic breadths, and cranial flexion. These features may be related to diet, but the precise biomechanical correlates of baboon form variation remain unclear., (Copyright 2005 Wiley-Liss, Inc.)

This study tests hypotheses regarding the ontogeny of canine tooth size dimorphism in five anthropoid primate species (Saguinus fuscicollis, Macaca mulatta, Cercocebus atys, Papio hamadryas, and Mandrillus sphinx). Canine measurements and chronological age data are analyzed to determine if bimaturism, a sex difference in the age at which eruption ceases, accounts for canine tooth sexual dimorphism. Canine height measurements are evaluated through a variety of regression techniques. Results show a lack of sexual dimorphism in Saguinus. While size dimorphism is absent in the deciduous teeth of all species analyzed, the adult teeth in cercopithecines become increasingly dimorphic through ontogeny. Female adult tooth eruption regularly precedes male tooth eruption, and regression-based eruption trajectories for both sexes intersect at about the age at which the female tooth reaches adult size. Males erupt the tooth later and more rapidly than females. Males also reach a larger adult size than females by erupting the tooth for much longer periods of time. Bimaturism is primary in the production of dimorphism, but rates of eruption show modest variation. These results point to the scheduling of sexual selection through intermale competition as a primary factor determining male eruption timing, rates of eruption, and adult size. Life history factors may play a role in determining the relations between the scheduling of intrasexual competition and canine eruption. Female contributions to sexual dimorphism are apparent in these species, suggesting that similar levels of dimorphism can be attained through diverse ontogenetic pathways., ((c) 2004 Wiley-Liss, Inc)

This study investigates brain size ontogeny in a sample of seven anthropoid primate species (including humans) in order to evaluate longstanding ideas about the relations between brain size, brain ontogeny, life history, and cognition. First, this analysis tests the hypothesis that primate brain growth patterns vary across species. Second, the relations between the duration of the brain growth period and the duration of the pre-adult period are evaluated. Brain growth data, derived from a number of sources, are analyzed through parametric and nonparametric regressions. The results indicate that primates are characterized by significant variation in patterns of brain growth. In addition, the degree to which brain growth is allocated to either the pre- or the postnatal period varies substantially. Analyses of phylogenetically adjusted data show no correlation between the lengths of the brain growth period and the juvenile period, but there are correlations with other life-history variables. These results are explained in terms of maternal metabolic adaptations. Specifically, primates appear to present at least two major metabolic adaptations. In the first, brain growth occurs mainly during the prenatal period, reflecting heavy maternal investment. In the second, brain growth occupies large portions of the postnatal period. These differing patterns have important implications for maturation age, necessitating late maternal maturation in the first case and enabling relatively early maternal maturation in the second. Overall, these adaptations represent components of distinctive life-history adaptations, with potentially important implications for the evolution of primate cognition., (Copyright 2004 Wiley-Liss, Inc.)

This study investigates the developmental bases of size and shape variation in papionin primates (Macaca, Cercocebus, Mandrillus, Lophocebus, and Papio). The analysis tests hypotheses predicting that heterochronic changes in ontogeny, particularly in the degree of overall size growth, can account for cranial diversity and "allometric scaling" in this clade. Large developmental samples of extant papionin crania are examined to test heterochronic hypotheses using bivariate allometric methods. Analyses indicate that the crania of larger papionins (Mandrillus and Papio) are generally peramorphic, surpassing size and shape ranges of smaller, and probably less-derived, macaques and mangabeys. At least two heterochronic processes, including acceleration and hypermorphosis, can account for this pattern. Ontogenetic changes include decoupling of growth and development among cranial regions, along with simple shifts in size. Allometric scaling has complex developmental bases. Size change itself is not sufficient to explain all developmental differences among papionins, but these changes are extremely important in comparisons within cranial regions such as the face. Results imply that Papio exhibits strongly derived patterns of brain growth that impact postnatal patterns of size and shape transformation. Consideration of these results in the context of recent socioecological analyses suggests that derived patterns of cranial growth in Papio may be a response to selection during the early periods of ontogeny, resulting in a distinctive life history pattern.

We present the results of a 4-month field investigation of positional behavior, vertical ranging, and species differences in limb proportions and body mass in a mixed-species troop of Saguinus fuscicollis, Saguinus labiatus, and Callimico goeldii in northwestern Brazil. Despite certain similarities in overall positional repertoire, patterns of positional behavior varied significantly between species. Travel in Callimico occurred principally in the lowest levels of the canopy, and was characterized by an exaggerated form of hindlimb-dominated bounding (bounding-hop), and leaping to and from vertical trunks (55.1% of leaps). In contrast, saddle-back tamarins traveled in the lower and middle levels of the canopy, and engaged in a range of leaping behaviors, including stationary leaps (37.3%), acrobatic leaps (31.3%), and trunk-to-trunk leaps (20%). Red-bellied tamarins exploited the highest levels of the arboreal canopy. Travel in this species was dominated by quadrupedal bounding and acrobatic leaps (67% of leaps) that began and ended on thin, flexible supports. Species differences in positional behavior correlated with species differences in limb proportions and locomotor anatomy, and provide a framework for understanding niche partitioning in mixed-species troops of Saguinus and Callimico., (Copyright 2001 Wiley-Liss, Inc.)

Investigations of size variation in fossil and archaeological skeletal assemblages may be complicated by incomplete skeletons, biased representation of sexes, and the lack of morphological features that identify sex. In order to refine our ability to evaluate size variation, we test the accuracy of three methods that are currently used to estimate size differences in unsexed (pooled) samples: the means method, the median method, and a newly applied technique, the method of moments. Using body mass data from 42 primate species, we calculated actual levels of sexual dimorphism for each species and compared these values to estimates produced by each method. Multivariate regression was used to examine the effects of sample distribution characteristics, including sample size, kurtosis, skewness, sample variance, sex ratio, and intrasexual variance on the performance of the methods. None of the methods appears to be especially accurate. However, one of the simplest methods, the means method, performs relatively well. Factors that lead to inaccuracies in estimation are not readily evident based on multiple regression analysis. We urge caution in the utilization of these techniques, and advocate further analysis of simulated data. Am J Phys Anthropol 110: 95-104, 1999., (Copyright 1999 Wiley-Liss, Inc.)

This investigation evaluates hypotheses that seek to explain temporal retardation or prolongation of human ontogeny. Current hypotheses that address this issue are poorly defined and conflate several distinct theoretical positions. A model that predicts homogeneity in the extension of human growth periods is evaluated. This model is contrasted with two alternatives. The first alternative predicts heterogeneity in the extension of human growth periods. The second anticipates that human growth prolongation is the result of the uniquely derived "insertion" of a human childhood period into an ancestral ontogenetic trajectory. Allometric analyses of body mass growth data from 21 species of anthropoid primates suggest that human female and male ontogenies often depart from patterns established by other primates, but these departures are not uniformly exceptional. Comparisons imply that derived changes in human growth are heterogeneous. Relative to interspecific expectations, early growth periods are much prolonged, but later growth periods are actually reduced. Moreover, the attributes of early growth periods, including growth rates, timing of growth events, and size-for-age, are highly variable across primates. Low correlations among growth periods suggest independence among growth phases. These analyses highlight minimal distinctions between competing models (heterogeneous extension and insertion hypotheses) that attempt to explain human growth prolongation. More important, the present study facilitates refinements of causal models that have been proposed to explain human growth prolongation. Specifically, human growth prolongation may be related to derived changes in patterns of brain development. Alternatively, metabolic factors may have exerted influences on human ontogeny. However, models that predict long growth periods as a byproduct of metabolic factors do not adequately explain temporal retardation of human ontogeny.

Data were collected on neonatal body mass for 109 primate species. For 23 species with sample sizes of nine or more for each sex, dimorphism (male/female ratio) in neonatal body mass ranged from 0.94 in Galago senegalensis and Aotus trivirgatus to 1.19 in Pongo pygmaeus. Dimorphism in neonatal body mass was positively correlated both with adult body mass and with dimorphism in adult body mass, but the apparent relationship with adult mass was eliminated after controlling for the relationship with adult dimorphism. Comparative studies concerned with neonatal body mass in primates have almost always ignored sexual dimorphism. However, neonatal sexual dimorphism in primates does exist and appears to be of sufficient magnitude to be biologically significant in some species. It may be important to consider the consequences of neonatal dimorphism for a variety of research questions related to maternal investment, life history, postnatal growth, and the relationship between neonatal size and adult female pelvic dimensions, both in extant and in extinct primates.