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Biology subjects

Campos, F. A.

Publications and source records attributed to Campos, F. A..

8 recordsLinked to original sources

Sources of Variation in Fecal Haptoglobin in a Population of Wild Capuchin Monkeys (Cebus imitator)

Non-human primates support ecosystem function by enhancing forest regeneration through seed dispersal and other key ecological roles. Unfortunately, primate populations are declining, placing renewed emphasis on monitoring the health of wild populations. Non-invasive monitoring of reliable biomarkers of inflammation and immune activation allows researchers to assess individual health status without capturing or interfering with wild animals, but studies are limited by the availability of such biomarkers that are measurable from fecal and urine samples. In the present study, we aimed to validate the measurement of fecal haptoglobin, a biomarker of inflammation, in wild white-faced capuchin monkeys (Cebus imitator), and to evaluate the relationship between fecal haptoglobin concentrations and age, sex, dominance rank, circadian effects and environmental factors including temperature and rainfall. After analytically validating the measurement of fecal haptoglobin, our results did not demonstrate a relationship between haptoglobin concentrations and age, sex, dominance rank or circadian effects. However, we found significant influences of environmental conditions on fecal haptoglobin levels, with an increase and more variation observed during drier conditions, when the animals are typically under greater environmental stress. We conclude that haptoglobin measurement is feasible in wild white-faced capuchin monkeys, and its concentrations vary in our study population, reflecting seasonal patterns of inflammation that are consistent with changes to environmental stressors associated with lower access to food and water.

physiology↗

Fecal proteomics of wild capuchins reveals impacts of season, diet, age, and, sex on gut physiology

Understanding how the physiology of free-ranging mammals is impacted by environmental stressors is a major focus of ecological research. However, the constraints of non-invasive sampling pose serious challenges to the acquisition of physiological data from most species of primates. As a result, little is known about how the gut responds to ecological stimuli at the cellular level in wild populations. Recent research has demonstrated that proteomics could fill this knowledge gap by sequencing and quantifying proteins directly from primate feces. In order to ascertain how the gut of free-ranging white-faced capuchin monkeys (C. imitator) is influenced by environmental heterogeneity, diet, age, and sex, we sequenced 45 fecal proteomes from 24 individuals from the Sector Santa Rosa population in Costa Rica, using liquid chromatography-tandem mass spectrometry with label-free quantification. Fecal proteins assigned to C. imitator were strongly localized to gut tissues and functionally enriched for digestive and immune functions. We identified 41 capuchin candidate proteins linked to seasonality, age, sex, and diet. We also quantified abundances of dietary fruit, dietary insects, helminth gut parasites, and gut microbes. Our results demonstrate the viability of using quantitative fecal proteomics in free-ranging populations of mammals to integrate host physiology, diet, and microbial ecology through non-invasive means.

ecology↗

Non-invasive measures of DNA methylation capture molecular aging in wild capuchin monkeys

Elucidating the socio-ecological factors that shape patterns of epigenetic modification in long-lived vertebrates is of broad interest to evolutionary biologists, geroscientists, and ecologists. However, aging research in wild populations is limited due to inability to measure cellular hallmarks of aging noninvasively. Here, we demonstrate that cellular DNA methylation (DNAm) profiles from fecal samples provide an accurate and reliable molecular clock in wild capuchin monkeys. Analysis of blood, feces, and urine samples from a closely related species shows that DNAm differentiates between species and different types of biological samples. We further find age-associated differences in DNAm relevant to cellular damage, inflammation, and senescence, consistent with hallmarks conserved across humans and other mammalian species, speaking to the comparative potential. By demonstrating that DNAm can be studied non-invasively in wild animals, our research opens new avenues in the study of modifiers of the pace of aging, and increases potential for cross-population and species comparisons.

genomics↗

Causes for and consequences of winning intergroup encounters in colobus monkeys (Colobus vellerosus)

The outcome of an intergroup encounter depends on the relative competitive abilities of the participating groups and the value of the resource for which they compete. However, few studies have been able to assess the consequences of winning intergroup encounters. We used behavioral and demographic data from 94 adult and subadult individuals in 8 groups of Colobus vellerosus at Boabeng-Fiema, Ghana to investigate the factors that predict winning intergroup encounters, and whether intergroup encounter success determines access to food and female reproductive output. In support of the hypothesis that groups with high-quality males would be more likely to win encounters, winning the encounter was best predicted by rates of displays by the alpha male. Food trees that were contested during intergroup encounters were more likely to have young leaves or other higher quality food items and to be important food species. Feeding was more likely to occur during and after the intergroup encounter if the focal animals group had won the encounter. The percentage of encounters won was correlated with the groups dominance rank but not with home range size or the immature-to-female ratio. In populations such as the Boabeng-Fiema colobus in which male quality seems to be associated with winning intergroup encounters and gaining immediate access to food, one of the drivers for female transfer between groups may be differences in alpha male quality between groups and across time.

animal behavior and cognition↗

Early life adversity and adult social relationships have independent effects on survival in a wild animal model of aging

Does social isolation in adulthood predict survival because socially isolated individuals are already unhealthy due to adversity earlier in life (health selection)? Or do adult social environments directly cause poor health and increased mortality risk ("social causation")? These alternative hypotheses are difficult to disentangle in humans because prospective data on survival and the environment for both early life and adulthood are rarely available. Using data from the baboon population of Amboseli, Kenya, a model for human behavior and aging, we show that early adversity and adult social isolation contribute independently to reduced adult survival, in support of both health selection and social causation. Further, strong social bonds and high social status can buffer some negative effects of early adversity on survival. These results support a growing change in perspective, away from "either-or" hypotheses and towards a multi-causal perspective that points to multiple opportunities to mitigate the effects of social adversity. TeaserEarly life environments and adult social bonds have strong, but largely independent effects on survival in wild baboons.

animal behavior and cognition↗

Distinct gene regulatory signatures of dominance rank and social bond strength in wild baboons

The social environment is a major determinant of morbidity, mortality, and Darwinian fitness in social animals. Recent studies have begun to uncover the molecular processes associated with these relationships, but the degree to which they vary across different dimensions of the social environment remains unclear. Here, we draw on a long-term field study of wild baboons to compare the signatures of affiliative and competitive aspects of the social environment in white blood cell gene regulation, under both immune stimulated and non-stimulated conditions. We find that the effects of dominance rank on gene expression are directionally opposite in males versus females, such that high-ranking males resemble low-ranking females, and vice-versa. Among females, rank and social bond strength are both reflected in the activity of cellular metabolism and proliferation genes. However, pronounced rank-related differences in baseline immune gene activity are near-absent for social bond strength, while only bond strength predicts the fold-change response to immune (lipopolysaccharide) stimulation. Together, our results indicate that the directionality and magnitude of social effects on gene regulation depend on the aspect of the social environment under study. This heterogeneity may help explain why social environmental effects on health and longevity can also vary between measures.

genomics↗

Beyond orphaned infants: novel effects of maternal death in wild primates

Primate offspring often depend on their mothers well beyond the age of weaning, and offspring that experience maternal death in early life can suffer substantial reductions in fitness across the lifespan. Here we leverage data from eight wild primate populations (seven species) to examine two underappreciated pathways linking early maternal death and offspring fitness that are distinct from direct effects of orphaning on offspring survival. First, we show that, for five of the seven species, offspring face reduced survival during the years immediately preceding maternal death, while the mother is still alive. Second, we identify an intergenerational effect of early maternal loss in three species (muriquis, baboons, and blue monkeys), such that early maternal death experienced in one generation leads to reduced offspring survival in the next. Our results have important implications for the evolution of slow life histories in primates, as they suggest that maternal condition and survival are more important for offspring fitness than previously realized.

evolutionary biology↗

Comparing proportional and ordinal dominance ranks reveals multiple competitive landscapes in an animal society

Across group-living animals, linear dominance hierarchies lead to disparities in access to resources, health outcomes, and reproductive performance. Studies of how dominance rank affects these outcomes typically employ one of several dominance rank metrics without examining the assumptions each metric makes about its underlying competitive processes. Here we compare the ability of two dominance rank metrics--ordinal rank and proportional or standardized rank--to predict 20 distinct traits in a well-studied wild baboon population in Amboseli, Kenya. We propose that ordinal rank best predicts outcomes when competition is density-dependent, while proportional rank best predicts outcomes when competition is density-independent. We found that for 75% (15/20) of the traits, one of the two rank metrics performed better than the other. Strikingly, all male traits were better predicted by ordinal than by proportional rank, while female traits were evenly split between being better predicted by proportional or ordinal rank. Hence, male and female traits are shaped by different competitive regimes: males competitive environments are largely driven by density-dependent resource access (e.g., access to estrus females), while females competitive environments are shaped by both density-independent resource access (e.g. distributed food resources) and density-dependent resource access. However, traits related to competition for social and mating partners are an exception to this sex-biased pattern: these traits were better predicted by ordinal rank than by proportional rank for both sexes. We argue that this method of comparing how different rank metrics predict traits of interest can be used as a way to distinguish between different competitive processes operating in animal societies.

animal behavior and cognition↗