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Biology subjects

Jack, K. M.

Publications and source records attributed to Jack, K. M..

5 recordsLinked to original sources

Genetic and behavioural repertoires support olfactory communication in wild capuchin monkeys

Olfaction is a key sense for many mammals, but its role in the social lives of anthropoid primates (monkeys, apes, humans) is poorly understood. Studies of chemosensory receptor genes and olfactory behaviours can provide insight into the evolution and function of olfaction across social contexts. Vomeronasal receptor (VR) genes are especially relevant to social behaviour as they are specialized for the detection of pheromones and other cues involved in social signaling, reproductive behaviour, and individual recognition in mammals. Here, we examined the population genetics and gene repertoires of VR genes in wild white-faced capuchin monkeys (Cebus imitator) from Costa Rica and Panama using DNA sourced through both host tissues and through noninvasive fluorescence-activated cell sorting of fecal samples (fecalFACS). We compared VR diversity relative to putatively neutral reference loci (NRs) to investigate evidence of selection and potential effects of demography. To complement the genetic analysis, we also conducted a detailed observational study of capuchin olfactory behaviours. Combined, we find evidence of intact VRs subject to evolutionary constraint in capuchins, providing novel evidence that members of this gene family are maintained by evolutionary constraint in wild monkeys. We further document a rich and varied ethogram of olfactory behaviours that have clear potential for communication. Overall, our study provides compelling evidence for a role of olfaction in the complex social lives of capuchin monkeys, motivating future research on the contributions of olfaction to social communication and evolution in primates and other mammals.

animal behavior and cognition↗

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↗

MHC heterozygosity may increase subordinate but not alpha male siring success in white-faced capuchin monkeys (Cebus imitator)

The genes of the major histocompatibility complex (MHC) are vital to vertebrate immunity and may influence mate choice in several species. The extent to which the MHC influences female mate choice in primates remains poorly understood, and studies of MHC-based mate choice in platyrrhines are especially rare. White-faced capuchin monkeys (Cebus imitator) reside in multimale-multifemale groups where alpha males sire most of the offspring. In this study, we investigated the roles of social dominance, relatedness, and MHC genotypes in determining which mating pairs produced offspring in wild white-faced capuchins in the Sector Santa Rosa (SSR), Area de Conservacion Guanacaste, Costa Rica. We find that males in this population do not differ significantly in MHC metrics based on their social status or siring success. Using mixed conditional logit models and generalized linear models, we find that alpha males that are distantly related to reproducing females are significantly more likely to sire offspring while MHC metrics do not predict the probability of siring offspring, or becoming an alpha male. However, we do find some evidence that subordinate males heterozygous at MHC loci sire significantly more offspring than homozygous subordinates. Further, one-sided binomial simulations reveal that offspring are more frequently heterozygous at MHC loci than expected given the gene pool. We conclude that in this population with limited genomic variation, females may preferentially mate with MHC-diverse subordinate males when related to the alpha, leading to increased probabilities of MHC-diverse offspring.

evolutionary biology↗