Paternity data reveal high MHC diversity among sires in a polygynandrous, egalitarian primate.

Evidence from human and nonhuman primates suggests that females avoid breeding with close kin and may choose mates based on MHC diversity, which can improve offspring survival. In despotic societies, female mate choice may be hindered by male sexual coercion, but in egalitarian societies, females may be less constrained. Among northern muriquis-an egalitarian, polygynandrous primate with male philopatry-analyses of new data on paternity and variation at microsatellite and MHC loci, combined with behavioural and life-history data, revealed that sires showed higher MHC diversity than expected by chance and were never close kin of dams, consistent with predictions of female mate choice and close inbreeding avoidance. However, females did not differentially reproduce with males who were more distantly related to them or more dissimilar at the MHC than expected by chance, nor with those who had more MHC alleles distinct from their own. The lack of male dominance may permit females to identify and reproduce preferentially with non-offspring males and with males who are more diverse at the MHC. Nonetheless, the absence of disassortative mating at the MHC and neutral loci suggests that female mate choice may be limited by other factors impacting male fertilization success.

Dispersal patterns in black howler monkeys (Alouatta pigra): Integrating multiyear demographic and molecular data.

Dispersal is a fundamental process in the functioning of animal societies as it regulates the degree to which closely related individuals are spatially concentrated. A species' dispersal pattern can be complex as it emerges from individuals' decisions shaped by the cost-benefit tradeoffs associated with either remaining in the natal group or dispersing. Given the potential complexity, combining long-term demographic information with molecular data can provide important insights into dispersal patterns of a species. Based on a 15-year study that integrates multiyear demographic data on six groups with longitudinal and cross-sectional genetic sampling of 20 groups (N = 169 individuals, N = 21 polymorphic microsatellite loci), we describe the various dispersal strategies of male and female black howler monkeys (Alouatta pigra) inhabiting Palenque National Park, Mexico. Genetically confirmed dispersal events (N = 21 of 59 males; N = 6 of 65 females) together with spatial autocorrelation analyses revealed that the dispersal pattern of black howlers is bisexual with strong sex-biases in both dispersal rate (males disperse more often than females) and dispersal distance (females disperse farther than males). Observational and genetic data confirm that both males and females can successfully immigrate into established groups, as well as form new groups with other dispersing individuals. Additionally, both males and females may disperse singly, as well as in pairs, and both may also disperse secondarily. Overall, our findings suggest multiple dispersal trajectories for black howler males and females, and longer multiyear studies are needed to unravel which demographic, ecological and social factors underlie individuals' decisions about whether to disperse and which dispersal options to take.

La dispersión es un proceso fundamental en el funcionamiento de las sociedades animales, ya que regula el grado en que los individuos parentados se concentran espacialmente. El patrón de dispersión de una especie puede ser complejo ya que surge de las decisiones de los individuos conformadas por las compensaciones de costo-beneficio asociadas con permanecer en el grupo natal o dispersarse. Dada esta posible complejidad, la combinación de información demográfica a largo plazo con datos moleculares puede proporcionar información importante sobre los patrones de dispersión de una especie en particular. Basado en un estudio de 15 años que integra datos demográficos de seis grupos sociales con muestreo genético longitudinal y transversal de 20 grupos (N = 169 individuos, N = 21 loci de microsatélites polimórficos), describimos las diversas estrategias de dispersión de machos y hembras del mono aullador negro (Alouatta pigra) que habitan el Parque Nacional Palenque, México. Los eventos de dispersión confirmados genéticamente (N = 21 de 59 machos; N = 6 de 65 hembras), junto con los análisis de autocorrelación espacial revelaron que el patrón de dispersión de los monos aulladores negros es bisexual con fuertes sesgos sexuales en ambas tasas de dispersión (los machos se dispersan más a menudo que las hembras) y distancia de dispersión (las hembras se dispersan más lejos que los machos). Los datos de observación y genéticos confirman que tanto machos como hembras pueden inmigrar con éxito a grupos ya establecidos, así como formar nuevos grupos con otros individuos que se están dispersando. Además, tanto los machos como las hembras pueden dispersarse individualmente, así como en parejas, y ambos también pueden dispersarse secundariamente. En general, nuestros hallazgos sugieren múltiples trayectorias de dispersión para aulladores negros de los dos sexos, y se necesitan más estudios para desentrañar qué factores demográficos, ecológicos y sociales subyacen en las decisiones de los individuos sobre si dispersarse y qué opciones de dispersión tomar.

Reproductive endocrinology of wild female woolly monkeys (Lagothrix lagotricha poeppigii) during puberty, ovarian cyclicity, and pregnancy.

Behavioral observations can provide clues about female reproductive status. However, the study of the endocrine dynamics that underlie processes such as puberty, ovulation, conception, and gestation, may help increase our understanding of female reproductive biology. We used noninvasive methods to study female reproductive endocrinology in wild woolly monkeys (genus Lagothrix). We extracted ovarian steroid hormones from fecal samples collected non-invasively to examine changes in the concentrations of progesterone and estrogen metabolites (pregnanediol-3-glucuronide and estrone-3-glucuronide, respectively) during periods of female puberty, ovarian cyclicity, and pregnancy. The two subadult females in our study showed significant increases in ovarian hormone concentrations before disappearing and presumably dispersing, suggesting that they might reach the onset of puberty before emigrating from their natal groups. Ovarian cycle length in adult females was, on average, ~22 days (N = 21). Of the 10 cycling females, five conceived and four gave birth to offspring, with an average gestation period of ~214 days, but the infant born to the female with the shortest estimated gestation period (182 days) disappeared within a month after parturition. The fact that less than half of all cycling females conceived, and that only three out of five of those females gave birth to offspring that survived past the first month, suggests that reproduction is energetically costly for female woolly monkeys. Ovarian cycle length and gestation period among woolly monkeys are similar to those in their closest relatives, spider monkeys and muriquis suggesting that reproductive physiology may be highly conserved among females within the Tribe Atelini.

Social groups constrain the spatiotemporal dynamics of wild sifaka gut microbiomes.

Primates acquire gut microbiota from conspecifics through direct social contact and shared environmental exposures. Host behaviour is a prominent force in structuring gut microbial communities, yet the extent to which group or individual-level forces shape the long-term dynamics of gut microbiota is poorly understood. We investigated the effects of three aspects of host sociality (social groupings, dyadic interactions, and individual dispersal between groups) on gut microbiome composition and plasticity in 58 wild Verreaux's sifaka (Propithecus verreauxi) from six social groups. Over the course of three dry seasons in a 5-year period, the six social groups maintained distinct gut microbial signatures, with the taxonomic composition of individual communities changing in tandem among coresiding group members. Samples collected from group members during each season were more similar than samples collected from single individuals across different years. In addition, new immigrants and individuals with less stable social ties exhibited elevated rates of microbiome turnover across seasons. Our results suggest that permanent social groupings shape the changing composition of commensal and mutualistic gut microbial communities and thus may be important drivers of health and resilience in wild primate populations.

Color vision and niche partitioning in a diverse neotropical primate community in lowland Amazonian Ecuador.

A recent focus in community ecology has been on how within-species variability shapes interspecific niche partitioning. Primate color vision offers a rich system in which to explore this issue. Most neotropical primates exhibit intraspecific variation in color vision due to allelic variation at the middle-to-long-wavelength opsin gene on the X chromosome. Studies of opsin polymorphisms have typically sampled primates from different sites, limiting the ability to relate this genetic diversity to niche partitioning. We surveyed genetic variation in color vision of five primate species, belonging to all three families of the primate infraorder Platyrrhini, found in the Yasuní Biosphere Reserve in Ecuador. The frugivorous spider monkeys and woolly monkeys (Ateles belzebuth and Lagothrix lagotricha poeppigii, family Atelidae) each had two opsin alleles, and more than 75% of individuals carried the longest-wavelength (553-556 nm) allele. Among the other species, Saimiri sciureus macrodon (family Cebidae) and Pithecia aequatorialis (family Pitheciidae) had three alleles, while Plecturocebus discolor (family Pitheciidae) had four alleles-the largest number yet identified in a wild population of titi monkeys. For all three non-atelid species, the middle-wavelength (545 nm) allele was the most common. Overall, we identified genetic evidence of fourteen different visual phenotypes-seven types of dichromats and seven trichromats-among the five sympatric taxa. The differences we found suggest that interspecific competition among primates may influence intraspecific frequencies of opsin alleles. The diversity we describe invites detailed study of foraging behavior of different vision phenotypes to learn how they may contribute to niche partitioning.

Behavioral and physiological responses to instability in group membership in wild male woolly monkeys (Lagothrix lagotricha poeppigii).

In group-living species, integrating into a new social group after dispersal is an important life history milestone associated with physical and social challenges. Generally, this process seems to be accompanied by heightened glucocorticoid (GC) concentrations; however, most studies of physiological responses to group transfer have been conducted on species with despotic social relationships, where integrating individuals are often targets of frequent aggression. Here we present data on fecal glucocorticoid (fGC) concentrations during periods of unstable group membership for male woolly monkeys (Lagothrix lagotricha poeppigii), a species with extremely low rates of male-male aggression and generally tolerant male-male associations. We collected data on males in four study groups at the Tiputini Biodiversity Station, Ecuador, and observed three attempted transfer events, involving a total of four adult males, in one study group. We observed only three instances of overt aggression (chases) between males across the entire study period, though male display behaviors were more frequent. We tested whether rates of displays were higher during periods of unstable group membership using a generalized linear mixed model (LMM). We also examined whether male status, group stability, and the occurrence of intergroup encounters affected fGC concentrations using LMMs. Contrary to our predictions, rates of display behaviors were not higher during periods of unstable group membership. However, both transient/integrating males and those who were already group members showed elevated fGC concentrations during these unstable periods. Our results suggest that even in species with tolerant male-male relationships, the integration of unfamiliar individuals can provoke an increase in GCs.

The genomics of ecological flexibility, large brains, and long lives in capuchin monkeys revealed with fecalFACS.

Ecological flexibility, extended lifespans, and large brains have long intrigued evolutionary biologists, and comparative genomics offers an efficient and effective tool for generating new insights into the evolution of such traits. Studies of capuchin monkeys are particularly well situated to shed light on the selective pressures and genetic underpinnings of local adaptation to diverse habitats, longevity, and brain development. Distributed widely across Central and South America, they are inventive and extractive foragers, known for their sensorimotor intelligence. Capuchins have among the largest relative brain size of any monkey and a lifespan that exceeds 50 y, despite their small (3 to 5 kg) body size. We assemble and annotate a de novo reference genome for Cebus imitator Through high-depth sequencing of DNA derived from blood, various tissues, and feces via fluorescence-activated cell sorting (fecalFACS) to isolate monkey epithelial cells, we compared genomes of capuchin populations from tropical dry forests and lowland rainforests and identified population divergence in genes involved in water balance, kidney function, and metabolism. Through a comparative genomics approach spanning a wide diversity of mammals, we identified genes under positive selection associated with longevity and brain development. Additionally, we provide a technological advancement in the use of noninvasive genomics for studies of free-ranging mammals. Our intra- and interspecific comparative study of capuchin genomics provides insights into processes underlying local adaptation to diverse and physiologically challenging environments, as well as the molecular basis of brain evolution and longevity.

Reproductive seasonality in two sympatric primates (Ateles belzebuth and Lagothrix lagotricha poeppigii) from Amazonian Ecuador.

With their large body size and "slow" life histories, atelin primates are thought to follow a risk-averse breeding strategy, similar to capital breeders, in which they accumulate energy reserves in anticipation of future reproductive events such as gestation and lactation. However, given the paucity of longitudinal data from wild populations, few studies to date have been able to compare the timing of reproductive events (e.g., copulations, conceptions, and births) in relation to shifting resource availability over multiple years. We examined the reproductive patterns of two atelin species-white-bellied spider monkeys (Ateles belzebuth) and lowland woolly monkeys (Lagothrix lagotricha poeppigii)-in relation to habitat-wide estimates of fruit availability at the Tiputini Biodiversity Station (TBS) in Amazonian Ecuador. Our sample included 4 years of data on births (N = 36) and copulations (N = 170) for Lagothrix, 10 years of data on births (N = 35) and copulations (N = 74) for Ateles, and 7 years of data on ripe fruit availability. Reproductive events were distinctly seasonal. For both species, births were concentrated between May and September, a time period in which ripe fruit was relatively scarce, while inferred conceptions occurred between September and January, when ripe fruit availability was increasing and maintained at high-levels throughout the forest. Interannual variation in births was relatively stable, except for in 2016 when twice as many infants were born following a strong El Niño event that may have led to unusually high levels of fruit productivity during the 2015 breeding season. Although copulations were observed year-round, an overwhelming majority (>90% for Lagothrix and >80% for Ateles) took place between August and February when females were most likely to conceive. Collectively, these data follow the reproductive patterns observed in other atelin primates, and, as proposed by others, suggest that atelins may follow a risk-averse breeding strategy.

Ranging behavior and the potential for territoriality in pair-living titi monkeys (Plecturocebus discolor).

Patterns of ranging behavior and space use are key for evaluating current ideas about the evolution and maintenance of pair-living and sexual monogamy as they provide insights into the dispersion of females, the potential for territoriality, and whether males are limited to defending an area that can support only one female and her offspring. We examined ranging behavior and space use to evaluate the potential for territoriality in five groups of red titi monkeys (Plecturocebus discolor) during a 10-year study in Ecuadorian Amazonia. Mean home range size, calculated using a time-sensitive local convex hull estimation procedure, was 4.0 ± 1.4 ha. Annual home ranges of neighboring groups overlapped, on average, 0%-7%. Mean daily path length was 670 ± 194 m, resulting in defendability indices of 2.2-3.6 across groups. Groups visited, on average, 4 of 12 sections of their home range border area per day, but that was not more often than would be expected by chance, and intergroup encounters were infrequent. We did not find evidence of active monitoring for intruders in border areas, in that groups did not travel either faster or slower when at the border than when in central areas of their range. The absence of overt monitoring might be compensated for by engaging in loud calls, which the study groups did throughout their home ranges; these calls may serve as an advertisement of occupancy and a deterrent to intruding conspecifics. Our finding that red titis have a high potential for territoriality is consistent with several of the main hypotheses proposed to explain pair-living in mammals.

Tree mode of death and mortality risk factors across Amazon forests.

The carbon sink capacity of tropical forests is substantially affected by tree mortality. However, the main drivers of tropical tree death remain largely unknown. Here we present a pan-Amazonian assessment of how and why trees die, analysing over 120,000 trees representing > 3800 species from 189 long-term RAINFOR forest plots. While tree mortality rates vary greatly Amazon-wide, on average trees are as likely to die standing as they are broken or uprooted-modes of death with different ecological consequences. Species-level growth rate is the single most important predictor of tree death in Amazonia, with faster-growing species being at higher risk. Within species, however, the slowest-growing trees are at greatest risk while the effect of tree size varies across the basin. In the driest Amazonian region species-level bioclimatic distributional patterns also predict the risk of death, suggesting that these forests are experiencing climatic conditions beyond their adaptative limits. These results provide not only a holistic pan-Amazonian picture of tree death but large-scale evidence for the overarching importance of the growth-survival trade-off in driving tropical tree mortality.

The evolution of pair-living, sexual monogamy, and cooperative infant care: Insights from research on wild owl monkeys, titis, sakis, and tamarins.

"Monogamy" and pair bonding have long been of interest to anthropologists and primatologists. Their study contributes to our knowledge of human evolutionary biology and social evolution without the cultural trappings associated with studying human societies directly. Here, we first provide an overview of theoretical considerations, followed by an evaluation of recent comparative studies of the evolution of "social monogamy"; we are left with serious doubts about the conclusions of these studies that stem from the often poor quality of the data used and an overreliance on secondary sources without vetting the data therein. We then describe our field research program on four "monogamous" platyrrhines (owl monkeys, titis, sakis, and tamarins), evaluate how well our data support various hypotheses proposed to explain "monogamy," and compare our data to those reported on the same genera in comparative studies. Overall, we found a distressing lack of agreement between the data used in comparative studies and data from the literature for the taxa that we work with. In the final section, we propose areas of research that deserve more attention. We stress the need for more high-quality natural history data, and we urge researchers to be cautious about the uncritical use of variables of uncertain internal validity. Overall, it is imperative that biological anthropologists establish and follow clear criteria for comparing and combining results from published studies and that researchers, reviewers, and editors alike comply with these standards to improve the transparency, reproducibility, and interpretability of causal inferences made in comparative studies.

Correction to: Review of GPS collar deployments and performance on nonhuman primates.

In the original publication of the article, figure 1 was wrongly published as a duplication.

Review of GPS collar deployments and performance on nonhuman primates.

Over the past 20 years, GPS collars have emerged as powerful tools for the study of nonhuman primate (hereafter, "primate") movement ecology. As the size and cost of GPS collars have decreased and performance has improved, it is timely to review the use and success of GPS collar deployments on primates to date. Here we compile data on deployments and performance of GPS collars by brand and examine how these relate to characteristics of the primate species and field contexts in which they were deployed. The compiled results of 179 GPS collar deployments across 17 species by 16 research teams show these technologies can provide advantages, particularly in adding to the quality, quantity, and temporal span of data collection. However, aspects of this technology still require substantial improvement in order to make deployment on many primate species pragmatic economically. In particular, current limitations regarding battery lifespan relative to collar weight, the efficacy of remote drop-off mechanisms, and the ability to remotely retrieve data need to be addressed before the technology is likely to be widely adopted. Moreover, despite the increasing utility of GPS collars in the field, they remain substantially more expensive than VHF collars and tracking via handheld GPS units, and cost considerations of GPS collars may limit sample sizes and thereby the strength of inferences. Still, the overall high quality and quantity of data obtained, combined with the reduced need for on-the-ground tracking by field personnel, may help defray the high equipment cost. We argue that primatologists armed with the information in this review have much to gain from the recent, substantial improvements in GPS collar technology.

Biodiversity of protists and nematodes in the wild nonhuman primate gut.

Documenting the natural diversity of eukaryotic organisms in the nonhuman primate (NHP) gut is important for understanding the evolution of the mammalian gut microbiome, its role in digestion, health and disease, and the consequences of anthropogenic change on primate biology and conservation. Despite the ecological significance of gut-associated eukaryotes, little is known about the factors that influence their assembly and diversity in mammals. In this study, we used an 18S rRNA gene fragment metabarcoding approach to assess the eukaryotic assemblage of 62 individuals representing 16 NHP species. We find that cercopithecoids, and especially the cercopithecines, have substantially higher alpha diversity than other NHP groups. Gut-associated protists and nematodes are widespread among NHPs, consistent with their ancient association with NHP hosts. However, we do not find a consistent signal of phylosymbiosis or host-species specificity. Rather, gut eukaryotes are only weakly structured by primate phylogeny with minimal signal from diet, in contrast to previous reports of NHP gut bacteria. The results of this study indicate that gut-associated eukaryotes offer different information than gut-associated bacteria and add to our understanding of the structure of the gut microbiome.

Phylogeographic evidence for two species of muriqui (genus Brachyteles).

The taxonomy of muriquis, the largest extant primates in the New World, is controversial. While some specialists argue for a monotypic genus (Brachyteles arachnoides), others favor a two-species classification, splitting northern muriquis (Brachyteles hypoxanthus) from southern muriquis (B. arachnoides). This uncertainty affects how we study the differences between these highly endangered and charismatic primates, as well as the design of more effective conservation programs. To address this issue, between 2003 and 2017 we collected over 230 muriqui fecal samples across the genus' distribution in the Brazilian Atlantic Forest, extracted DNA from these samples, and sequenced 423 base pairs of the mitochondrial DNA (mtDNA) control region. Phylogenetic and species delimitation analyses of our sequence dataset robustly support two reciprocally monophyletic groups corresponding to northern and southern muriquis separated by an average 12.7% genetic distance. The phylogeographic break between these lineages seems to be associated with the Paraíba do Sul River and coincides with the transition between the north and south Atlantic Forest biogeographic zones. Published divergence estimates from whole mitochondrial genomes and nuclear loci date the split between northern and southern muriquis to the Early Pleistocene (ca. 2.0 mya), and our new mtDNA dataset places the coalescence time for each of these two clades near the last interglacial (ca. 120-80 kya). Our results, together with both phenotypic and ecological differences, support recognizing northern and southern muriquis as sister species that should be managed as distinct evolutionarily significant units. Given that only a few thousand muriquis remain in nature, it is imperative that conservation strategies are tailored to protect both species from extinction.

Evolutionary diversity is associated with wood productivity in Amazonian forests.

Higher levels of taxonomic and evolutionary diversity are expected to maximize ecosystem function, yet their relative importance in driving variation in ecosystem function at large scales in diverse forests is unknown. Using 90 inventory plots across intact, lowland, terra firme, Amazonian forests and a new phylogeny including 526 angiosperm genera, we investigated the association between taxonomic and evolutionary metrics of diversity and two key measures of ecosystem function: aboveground wood productivity and biomass storage. While taxonomic and phylogenetic diversity were not important predictors of variation in biomass, both emerged as independent predictors of wood productivity. Amazon forests that contain greater evolutionary diversity and a higher proportion of rare species have higher productivity. While climatic and edaphic variables are together the strongest predictors of productivity, our results show that the evolutionary diversity of tree species in diverse forest stands also influences productivity. As our models accounted for wood density and tree size, they also suggest that additional, unstudied, evolutionarily correlated traits have significant effects on ecosystem function in tropical forests. Overall, our pan-Amazonian analysis shows that greater phylogenetic diversity translates into higher levels of ecosystem function: tropical forest communities with more distantly related taxa have greater wood productivity.

Metagenomic analyses reveal previously unrecognized variation in the diets of sympatric Old World monkey species.

Insectivory, or the consumption of insects and other arthropods, is a significant yet cryptic component of omnivorous primate diets. Here, we used high-throughput DNA sequencing to identify arthropods from fecal DNA and assess variation in insectivory by closely-related sympatric primates. We identified arthropod prey taxa and tested the hypothesis that variation in insectivory facilitates niche differentiation and coexistence among closely-related species with high dietary overlap. We collected 233 fecal samples from redtail (Cercopithecus ascanius; n = 118) and blue monkeys (C. mitis; n = 115) and used a CO1 metabarcoding approach to identify arthropod DNA in each fecal sample. Arthropod DNA was detected in 99% of samples (N = 223 samples), and a total of 68 families (15 orders) were identified. Redtails consumed arthropods from 54 families, of which 12 (21.8%) were absent from blue monkey samples. Blue monkeys consumed arthropods from 56 families, of which 14 (24.6%) were absent from redtail samples. For both species, >97% of taxa present belonged to four orders (Araneae, Diptera, Hymenoptera, Lepidoptera). Redtail samples contained more Lepidoptera taxa (p<0.05), while blue monkey samples contained more Araneae (p<0.05). Blue monkeys consumed a greater diversity of arthropod taxa than redtail monkeys (p<0.05); however, the average number of arthropod families present per fecal sample was greater in the redtail monkey samples (p<0.05). These results indicate that while overlap exists in the arthropod portion of their diets, 20-25% of taxa consumed are unique to each group. Our findings suggest that variation in arthropod intake may help decrease dietary niche overlap and hence facilitate coexistence of closely-related primate species.

Initiation of feeding by four sympatric Neotropical primates (Ateles belzebuth, Lagothrix lagotricha poeppigii, Plecturocebus (Callicebus) discolor, and Pithecia aequatorialis) in Amazonian Ecuador: Relationships to photic and ecological factors.

We examined photic and ecological factors related to initiation of feeding by four sympatric primates in the rain forest of Amazonian Ecuador. With rare exceptions, morning activities of all taxa began only after the onset of nautical twilight, which occurred 47-48 min before sunrise. The larger spider and woolly monkeys, Ateles belzebuth and Lagothrix lagotricha poeppigii, left their sleeping trees before sunrise about half the time, while the smaller sakis and titi monkeys, Pithecia aequatorialis and Plecturocebus (formerly Callicebus) discolor, did not emerge until sunrise or later. None of the four taxa routinely began feeding before sunrise. Pithecia began feeding a median 2.17 h after sunrise, at least 0.8 h later than the median feeding times of the other three taxa. The early movement of Ateles and Lagothrix, and late initiation of feeding by Pithecia are consistent with temporal niche partitioning. Among most New World primate species, all males and many females, have dichromatic color vision, with only two cone photopigments, while some females are trichromats with three cone photopigments. Current evidence indicates that the dichromats have a foraging advantage in dim light, which could facilitate utilization of twilight periods and contribute to temporal niche partitioning. However, in our study, dichromatic males did not differentially exploit the dim light of twilight, and times of first feeding bouts of female Ateles and Lagothrix were similar to those of males. First feeding bouts followed a seasonal pattern, occurring latest in May-August, when ripe fruit abundance and ambient temperature were both relatively low. The most frugivorous taxon, Ateles, exhibited the greatest seasonality, initiating feeding 1.4 h later in May-August than in January-April. This pattern may imply a strategy of conserving energy when ripe fruit is scarcer, but starting earlier to compete successfully when fruit is more abundant. Lower temperatures were associated with later feeding of Ateles (by 26 min / °C) and perhaps Pithecia, but not Lagothrix or Plecturocebus. The potential for modification of temporal activity patterns and temporal niche partitioning by relatively small changes in temperature should be considered when predicting the effects of climate change.

Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes.

Over the past decade several studies have reported that the gut microbiomes of mammals with similar dietary niches exhibit similar compositional and functional traits. However, these studies rely heavily on samples from captive individuals and often confound host phylogeny, gut morphology, and diet. To more explicitly test the influence of host dietary niche on the mammalian gut microbiome we use 16S rRNA gene amplicon sequencing and shotgun metagenomics to compare the gut microbiota of 18 species of wild non-human primates classified as either folivores or closely related non-folivores, evenly distributed throughout the primate order and representing a range of gut morphological specializations. While folivory results in some convergent microbial traits, collectively we show that the influence of host phylogeny on both gut microbial composition and function is much stronger than that of host dietary niche. This pattern does not result from differences in host geographic location or actual dietary intake at the time of sampling, but instead appears to result from differences in host physiology. These findings indicate that mammalian gut microbiome plasticity in response to dietary shifts over both the lifespan of an individual host and the evolutionary history of a given host species is constrained by host physiological evolution. Therefore, the gut microbiome cannot be considered separately from host physiology when describing host nutritional strategies and the emergence of host dietary niches.