Steven R. Leigh

Habitat degradation impacts black howler monkey ( Alouatta pigra ) gastrointestinal microbiomes

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.

Patterns of variation in the ontogeny of primate body size dimorphism

Abstract This study investigates variability in the ontogeny of sexual dimorphism in body weight in anthropoid primates. Specifically, the hypothesis that the ontogenetic bases of dimorphism vary in primates is tested with a large comparative sample. This sample allows both specification of the range of variability in patterns of dimorphic growth and careful examination of some correlates of ontogenetic variability. The analysis is based on body weight growth in 45 species of captive primates. Growth curves are estimated for each sex in each species using a non-parametric regression technique (locally weighted least squares regression). These regressions facilitate estimation of the degree of differences in age at body weight maturation, the proportion of total adult dimorphism arising from sex differences in rate of growth, and the proportion of total dimorphism attributable to sex differences in duration of growth. Primates show great diversity in how adult weight dimorphism develops. Although males tend to reach adult weight later than females, cases in which rate differences are exclusively responsible for body weight dimorphism are observed. More generally, sex differences in both rate and duration of growth occur together to produce dimorphism, but these differences may occur independently. Relationships between these processes and size appear complex, as do relations between these processes and dimorphism. These results suggest that primates have evolved a number of developmental pathways that lead to similar levels of adult dimorphism. It is expected that male patterns of growth respond primarily to sexual selection, but that female patterns of growth respond to natural selection.

Ontogenetic Variation in Small-Bodied New World Primates: Implications for Patterns of Reproduction and Infant Care

This paper explores relations of ontogeny, life history strategies and patterns of infant care in 11 species of small-bodied New World monkeys. Analysis of these data suggests that differences in the social systems of Aotus, Callicebus, Saimiri, Callimico, Saguinus, Leontopithecus, Cebuella and Callithrix are closely tied to both the costs of reproduction and to the ontogenetic requirements of maturing young. In Saimiri, both rapid prenatal body weight and perinatal brain growth result in relatively high metabolic costs to breeding females. These costs, coupled with minimal nonmaternal assistance in caregiving, appear to favor a reproductive strategy that limits offspring production to a single birth at 2-year intervals. In contrast, tamarins and marmosets are capable of producing twins twice in the same year. Prenatal investment in each offspring is relatively low, and the potentially high postnatal costs of nursing 2 infants are minimized by the evolution of a social system involving extensive extramaternal care-giving. Cooperative infant care in callitrichins (tamarins and marmosets) serves to distribute the metabolic costs of infant ontogeny among several group members. Callimico is also characterized by a high reproductive output, with females capable of producing a single infant twice during the year. Infants continue to grow rapidly after weaning. Patterns of infant development in Callimico are similar to those found in tamarins and marmosets and support a close phylogenetic relationship among these taxa. Aotus and Callicebus are characterized by an alternative strategy. In these taxa, a monogamous mating system is associated with paternal certainty, male parental care, and provisioning of the young. The transfer of male energetic resources to a single offspring allows night and titi monkeys to maintain a comparatively short interbirth interval (1 year). Ecological and social factors, such as predation and feeding competition, do not appear to adequately explain much of the observed variation in infant development and preadult growth rates in these platyrrhines. Instead, reproductive strategies are strongly linked to ontogenetic patterns and life histories.

Characterization of the Fecal Microbiome from Non-Human Wild Primates Reveals Species Specific Microbial Communities

Background Host-associated microbes comprise an integral part of animal digestive systems and these interactions have a long evolutionary history. It has been hypothesized that the gastrointestinal microbiome of humans and other non-human primates may have played significant roles in host evolution by facilitating a range of dietary adaptations. We have undertaken a comparative sequencing survey of the gastrointestinal microbiomes of several non-human primate species, with the goal of better understanding how these microbiomes relate to the evolution of non-human primate diversity. Here we present a comparative analysis of gastrointestinal microbial communities from three different species of Old World wild monkeys. Methodology/Principal Findings We analyzed fecal samples from three different wild non-human primate species (black-and-white colobus [Colubus guereza], red colobus [Piliocolobus tephrosceles], and red-tailed guenon [Cercopithecus ascanius]). Three samples from each species were subjected to small subunit rRNA tag pyrosequencing. Firmicutes comprised the vast majority of the phyla in each sample. Other phyla represented were Bacterioidetes, Proteobacteria, Spirochaetes, Actinobacteria, Verrucomicrobia, Lentisphaerae, Tenericutes, Planctomycetes, Fibrobacateres, and TM7. Bray-Curtis similarity analysis of these microbiomes indicated that microbial community composition within the same primate species are more similar to each other than to those of different primate species. Comparison of fecal microbiota from non-human primates with microbiota of human stool samples obtained in previous studies revealed that the gut microbiota of these primates are distinct and reflect host phylogeny. Conclusion/Significance Our analysis provides evidence that the fecal microbiomes of wild primates co-vary with their hosts, and that this is manifested in higher intraspecies similarity among wild primate species, perhaps reflecting species specificity of the microbiome in addition to dietary influences. These results contribute to the limited body of primate microbiome studies and provide a framework for comparative microbiome analysis between human and non-human primates as well as a comparative evolutionary understanding of the human microbiome.

Evolution of human growth spurts

This study investigates subadult growth spurts in a large sample of anthropoid primates, including humans. Analyses of body mass growth curves show that humans are not unique in the expression of female and male body mass growth spurts. Subadult growth spurts are observed in both New World and Old World anthropoid primates and are more common in males than in females. Allometric analyses of growth spurts indicate that many aspects of primate growth spurts are strongly correlated with species size. Small species tend not to exhibit growth spurts. Although male and female scaling patterns for velocity and size measures are comparable, scaling relations of variables that measure the timing of growth spurts differ by sex. These patterns can be related to sexual differences in life histories. Scaling analyses further show that humans do not depart substantially from patterns that describe other anthropoid primates. Thus, in relative terms, human growth spurts are not exceptional compared to this sample of primates. The long absolute delay in the initiation of the human growth spurt may be of substantial evolutionary importance and serves to distinguish humans from other primates. In essence, humans exhibit growth spurts that are comparable to other primates in many respects. However, human growth spurts are shifted to very late absolute ages.

Heterogeneity of Vaginal Microbial Communities within Individuals

ABSTRACT 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.

Comparative Genomics of Gardnerella vaginalis Strains Reveals Substantial Differences in Metabolic and Virulence Potential

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.

Comparative perspectives on bimaturism, ontogeny, and dimorphism in lemurid primates

We address questions regarding the general absence of dimorphism in lemurid primates (Hapalemur, Eulemur, and Varecia) through comparative analyses of ontogeny. We described and analyzed body mass growth data for 9 lemurid taxa and compared them to similar data for anthropoid primates. Lemurids tend to grow rapidly over a short period of time when compared to anthropoid primates of similar body sizes. Size variation among lemurid taxa arises primarily as a consequence of differences in rates of growth. Comparative analyses of body mass growth data suggest that natural selection has produced ontogenetic adaptations in lemurids that center on relatively short periods of growth. Reduced growth periods preclude the evolution of sexual dimorphism through bimaturism—a sex difference in the length of the growth period—despite high levels of intermale competition. Selective factors related to seasonal variability of lemurid habitats play important roles in limiting the potential for the evolution of bimaturism. Other selective factors that limit bimaturism are related to female reproductive synchrony. In combination, they favor relatively early male maturation, precluding sexual selection that would otherwise promote the evolution of dimorphism through bimaturism. Natural selection on growth rates may preclude somatic responses to sexual selection that involve elevated male growth rates. In general, existing ontogenetic or life history adaptations appear to restrict responses to sexual selection in male lemurids.

Gut Microbiome of Coexisting BaAka Pygmies and Bantu Reflects Gradients of Traditional Subsistence Patterns

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.

A multi-omic systems-based approach reveals metabolic markers of bacterial vaginosis and insight into the disease.

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.