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Studying biological ageing in animal models can circumvent some of the confounds exhibited by studies of human ageing. Ageing research in non-human primates has provided invaluable insights into human lifespan and healthspan. Yet data on patterns of ageing from wild primates remain relatively scarce, centred around a few populations of catarrhine species. Here, we introduce the white-faced capuchin, a long-lived platyrrhine primate, as a promising new model system for ageing research. Like humans, capuchins are highly social, omnivorous generalists, whose healthspan and lifespan relative to body size exceed that of other non-human primate model species. We review recent insights from capuchin ageing biology and outline our expanding, integrative research programme that combines metrics of the social and physical environments with physical, physiological and molecular hallmarks of ageing across the natural life courses of multiple longitudinally tracked individuals. By increasing the taxonomic breadth of well-studied primate ageing models, we generate new insights, increase the comparative value of existing datasets to geroscience and work towards the collective goal of developing accurate, non-invasive and reliable biomarkers with high potential for standardization across field sites and species, enhancing the translatability of primate studies.This article is part of the discussion meeting issue 'Understanding age and society using natural populations'.

The consumption of ethanol has frequently been seen as largely restricted to humans. Here, we take a broad eco-evolutionary approach to understanding ethanol's potential impact on the natural world. There is growing evidence that ethanol is present in many wild fruits, saps, and nectars and that ethanol ingestion offers benefits that favour adaptations for its use in multiple taxa. Explanations for ethanol consumption span both the nutritional and non-nutritional, with potential medicinal value or cognitive effects (with social-behavioural benefits) explored. We conclude that ethanol is ecologically relevant and that it has shaped the evolution of many species and structured symbiotic relationships among organisms, including plants, yeast, bacteria, insects, and mammals., Competing Interests: Declaration of interests No interests are declared., (Copyright © 2024 The Author(s). Published by Elsevier Ltd.. All rights reserved.)

Sensory systems mediate our social interactions, food intake, livelihoods, and other essential daily functions. Age-related decline and disease in sensory systems pose a significant challenge to healthy aging. Research on sensory decline in humans is informative but can often be difficult, subject to sampling bias, and influenced by environmental variation. Study of animal models, including mice, rats, rabbits, pigs, cats, dogs, and non-human primates, plays a complementary role in biomedical research, offering advantages such as controlled conditions and shorter lifespans for longitudinal study. Various species offer different advantages and limitations but have provided key insights in geroscience research. Here we review research on age-related decline and disease in vision, hearing, olfaction, taste, and touch. For each sense, we provide an epidemiological overview of impairment in humans, describing the physiological processes and diseases for each sense. We then discuss contributions made by research on animal models and ideas for future research. We additionally highlight the need for integrative, multimodal research across the senses as well as across disciplines. Long-term studies spanning multiple generations, including on species with longer life spans, are also highly valuable. Overall, integrative studies of appropriate animal models have high translational potential for clinical applications, the development of novel diagnostics, therapies, and medical interventions and future research will continue to close gaps in these areas. Research on animal models to improve understanding of the biology of the aging senses and improve the healthspan and additional research on sensory systems hold special promise for new breakthroughs., (© 2024. The Author(s), under exclusive licence to American Aging Association.)

Characterizing DNA methylation patterns is important for addressing key questions in evolutionary biology, geroscience, and medical genomics. While costs are decreasing, whole-genome DNA methylation profiling remains prohibitively expensive for most population-scale studies, creating a need for cost-effective, reduced representation approaches (i.e., assays that rely on microarrays, enzyme digests, or sequence capture to target a subset of the genome). Most common whole genome and reduced representation techniques rely on bisulfite conversion, which can damage DNA resulting in DNA loss and sequencing biases. Enzymatic methyl sequencing (EM-seq) was recently proposed to overcome these issues, but thorough benchmarking of EM-seq combined with cost-effective, reduced representation strategies has not yet been performed. To do so, we optimized Targeted Methylation Sequencing protocol (TMS)-which profiles ∼4 million CpG sites-for miniaturization, flexibility, and multispecies use at a cost of ∼$80. First, we tested modifications to increase throughput and reduce cost, including increasing multiplexing, decreasing DNA input, and using enzymatic rather than mechanical fragmentation to prepare DNA. Second, we compared our optimized TMS protocol to commonly used techniques, specifically the Infinium MethylationEPIC BeadChip (n=55 paired samples) and whole genome bisulfite sequencing (n=6 paired samples). In both cases, we found strong agreement between technologies (R² = 0.97 and 0.99, respectively). Third, we tested the optimized TMS protocol in three non-human primate species (rhesus macaques, geladas, and capuchins). We captured a high percentage (mean=77.1%) of targeted CpG sites and produced methylation level estimates that agreed with those generated from reduced representation bisulfite sequencing (R² = 0.98). Finally, we applied our protocol to profile age-associated DNA methylation variation in two subsistence-level populations-the Tsimane of lowland Bolivia and the Orang Asli of Peninsular Malaysia-and found age-methylation patterns that were strikingly similar to those reported in high income cohorts, despite known differences in age-health relationships between lifestyle contexts. Altogether, our optimized TMS protocol will enable cost-effective, population-scale studies of genome-wide DNA methylation levels across human and non-human primate species.

Purpose: The lamina cribrosa (LC) is hypothesized to be the site of initial axonal damage in glaucoma with the circumpapillary retinal nerve fiber layer thickness (RNFL-T) widely used as a standard metric for quantifying the glaucomatous damage. The purpose of this study was to determine in vivo, 3-dimensional (3D) differences in the microstructure of the LC in eyes of nonhuman primates (NHPs) with naturally occurring glaucoma., Methods: Spectral-domain optical coherence tomography (OCT) scans (Leica, Chicago, IL, USA) of the optic nerve head were acquired from a colony of 50 adult rhesus monkeys suspected of having high prevalence of glaucoma. The RNFL-T was analyzed globally and in quadrants using a semi-automated segmentation software. From a set of 100 eyes, 18 eyes with the thinnest global RNFL-T were selected as the study group and 18 eyes with RNFL-T values around the 50th percentile were used as controls. A previously described automated segmentation algorithm was used for LC microstructure analysis. Parameters included beam thickness, pore diameter and their ratio (beam-to-pore ratio [BPR]), pore area and shape parameters, beam and pore volume, and connective tissue volume fraction (CTVF; beam volume/total volume). The LC microstructure was analyzed globally and in the following volumetric sectors: quadrants, central and peripheral lamina, and three depth slabs (anterior, middle, and posterior)., Results: Although no significant difference was detected between groups for age, weight, or disc size, the study group had significantly thinner RNFL than the control group (P < 0.01). The study group had significantly smaller global and sectoral pore diameter and larger BPR compared with the control group. Across eyes, the global RNFL-T was associated positively with pore diameter globally. BPR and CTVF were significantly and negatively associated with the corresponding RNFL-T in the superior quadrant., Conclusions: Global and sectoral microstructural differences were detected when comparing thin and normal RNFL-T eyes. Whether these LC differences are the cause of RNFL damage or the result of remodeling of the LC requires further investigation., Translational Relevance: Our findings indicate structural alterations in the LC of NHP exhibiting natural thinning of the RNFL, a common characteristic of glaucomatous damage.

The sense of smell is an important mediator of health and sociality at all stages of life, yet it has received limited attention in our lineage. Olfaction starts in utero and participates in the establishment of social bonds in children, and of romantic and sexual relationships after puberty. Smell further plays a key role in food assessment and danger avoidance; in modern societies, it also guides our consumer behavior. Sensory abilities typically decrease with age and can be impacted by diseases, with repercussions on health and well-being. Here, we critically review our current understanding of human olfactory communication to refute outdated notions that our sense of smell is of low importance. We provide a summary of the biology of olfaction, give a prospective overview of the importance of the sense of smell throughout the life course, and conclude with an outline of the limitations and future directions in this field., (© 2024 The Authors. Evolutionary Anthropology published by Wiley Periodicals LLC.)

Bitter taste perception is important in preventing animals from ingesting potentially toxic compounds. Whole-genome assembly (WGA) data have revealed that bitter taste receptor genes (TAS2Rs) comprise a multigene family with dozens of intact and disrupted genes in primates. However, publicly available WGA data are often incomplete, especially for multigene families. In this study, we employed a targeted capture (TC) approach specifically probing TAS2Rs for ten species of cercopithecid primates with diverse diets, including eight omnivorous cercopithecine species and two folivorous colobine species. We designed RNA probes for all TAS2Rs that we modeled to be intact in the common ancestor of cercopithecids ("ancestral-cercopithecid TAS2R gene set"). The TC was followed by short-read and high-depth massive-parallel sequencing. TC retrieved more intact TAS2R genes than found in WGA databases. We confirmed a large number of gene "births" at the common ancestor of cercopithecids and found that the colobine common ancestor and the cercopithecine common ancestor had contrasting trajectories: four gene "deaths" and three gene births, respectively. The number of intact TAS2R genes was markedly reduced in colobines (25-28 detected via TC and 20-26 detected via WGA analysis) as compared with cercopithecines (27-36 via TC and 19-30 via WGA). Birth or death events occurred at almost every phylogenetic-tree branch, making the composition of intact genes variable among species. These results show that evolutionary change in intact TAS2R genes is a complex process, refute a simple general prediction that herbivory favors more TAS2R genes, and have implications for understanding dietary adaptations and the evolution of detoxification abilities., (© 2024. The Author(s).)

The copromicroscopic identification of gastrointestinal parasites is a common, cost-effective method vital to understanding host-parasite interactions. However, its efficacy depends on effective preservation of the samples. In this study, we compare the preservation of ethanol and formalin preserved gastrointestinal parasites collected from a wild population of Costa Rican capuchin monkeys (Cebus imitator). Fecal samples were collected, halved, and stored in either 10% formalin or 96% ethanol at ambient temperature, then microscopically screened for the presence of parasites. Parasites were morphologically identified and rated based on their preservation using a newly developed rubric. We identified more parasitic morphotypes in formalin-preserved samples but found no difference in the number of parasites per fecal gram (PFG) between mediums. There was no difference in the PFG of two most prevalent parasite morphotypes, Filariopsis barretoi larvae and Strongyle-type eggs, and while Filariopsis larvae were better preserved in formalin, strongyle eggs showed no preservation difference between mediums. Our results support the suitability of both ethanol and formalin for morphological parasite identification in samples stored over 1 year, describe the morphological changes and challenges associated with parasite degradation, and highlight the potential for future studies to use both morphological and molecular methods in non-invasively collected samples., (© 2024. The Author(s).)

Noncoding DNA is central to our understanding of human gene regulation and complex diseases 1,2 , and measuring the evolutionary sequence constraint can establish the functional relevance of putative regulatory elements in the human genome 3-9 . Identifying the genomic elements that have become constrained specifically in primates has been hampered by the faster evolution of noncoding DNA compared to protein-coding DNA 10 , the relatively short timescales separating primate species 11 , and the previously limited availability of whole-genome sequences 12 . Here we construct a whole-genome alignment of 239 species, representing nearly half of all extant species in the primate order. Using this resource, we identified human regulatory elements that are under selective constraint across primates and other mammals at a 5% false discovery rate. We detected 111,318 DNase I hypersensitivity sites and 267,410 transcription factor binding sites that are constrained specifically in primates but not across other placental mammals and validate their cis-regulatory effects on gene expression. These regulatory elements are enriched for human genetic variants that affect gene expression and complex traits and diseases. Our results highlight the important role of recent evolution in regulatory sequence elements differentiating primates, including humans, from other placental mammals., (© 2023. The Author(s).)

Background: Energy demands associated with pregnancy and lactation are significant forces in mammalian evolution. To mitigate increased energy costs associated with reproduction, female mammals have evolved behavioural and physiological responses. Some species alter activity to conserve energy during pregnancy and lactation, while others experience changes in metabolism and fat deposition. Restructuring of gut microbiota with shifting reproductive states may also help females increase the energy gained from foods, especially during pregnancy. The goal of this study was to examine the relationships among behaviour, gut microbiota composition, and reproductive state in a wild, non-human primate to better understand reproductive ecology. We combined life history data with > 13,000 behavioural scans and 298 fecal samples collected longitudinally across multiple years from 33 white-faced capuchin monkey (Cebus imitator) females. We sequenced the V4 region of the 16S rRNA gene and used the DADA2 pipeline to analyze microbial diversity. We used PICRUSt2 to assess putative functions., Results: Reproductive state explained some variation in activity, but overall resting behaviours were relatively stable across pregnancy and lactation. Foraging was less frequent among females in the early stage of nursing compared to the cycling stage, though otherwise remained at comparable levels. Maximum temperature was a strong, significantly positive predictor of resting, while social dominance had a small but significantly negative effect on resting. Ecological variables such as available fruit biomass and rainfall had a small but significantly positive effects on measures of foraging time. Gut microbial community structure, including richness, alpha diversity, and beta diversity remained stable across the reproductive cycle. In pairwise comparisons, pregnant females exhibited increased relative abundances of multiple microbial ASVs, suggesting small changes in relation to reproductive state. Reproductive state was not linked to differential abundance of putative metabolic pathways., Conclusions: Previous data suggest that activity budget and the gut microbiome shifts considerably during reproduction. The present study finds that both activity and gut microbial communities are less associated with reproduction compared to other predictors, including ecological contexts. This suggests that behavioural flexibility and gut microbial community plasticity is contrained by ecological factors in this population. These data contribute to a broader understanding of plasticity and stability in response to physiological shifts associated with mammalian reproduction., (© 2023. The Author(s).)

Introduction: Safe handling of biological samples sourced from wild ecosystems is a pressing concern for scientists in disparate fields, including ecology and evolution, OneHealth initiatives, bioresources, geography, veterinary medicine, conservation, and many others. This is especially relevant given the growing global research community and collaborative networks that often span international borders. Treatments to inactivate potential pathogens of concern during transportation and analysis of biospecimens while preserving molecular structures of interest are necessary., Objective: We provide a detailed resource on the effectiveness and limitations of TRIzol™ Reagent, a product commonly used in molecular biology to inactivate bacterial and viral pathogens found in wild animals., Methods: By literature review, we evaluate the mode of action of TRIzol Reagent and its main components on bacterial and viral structures. We also synthesize peer-reviewed literature on the effectiveness of TRIzol in inactivating a broad range of infectious bacteria and viruses., Key Findings: TRIzol Reagent inactivation is based on phenol, chaotropic salts, and sodium acetate. We find evidence of widespread efficacy in deactivating bacteria and a broad range of enveloped viruses. The efficacy against a subset of potential pathogens, including some nonenveloped viruses, remains uncertain., Conclusion: Available evidence suggests that TRIzol Reagent is effective in inactivating a broad spectrum of bacteria and viruses from cells, tissues, and liquids in biological samples when the matrices are exposed to at least 10 min at room temperature to the reagent. We highlight areas that require additional research and discuss implications for laboratory protocols., Competing Interests: No competing financial interests exist., (Copyright 2023, ABSA International 2023.)

Groups of animals inhabit vastly different sensory worlds, or umwelten, which shape fundamental aspects of their behaviour. Yet the sensory ecology of species is rarely incorporated into the emerging field of collective behaviour, which studies the movements, population-level behaviours, and emergent properties of animal groups. Here, we review the contributions of sensory ecology and collective behaviour to understanding how animals move and interact within the context of their social and physical environments. Our goal is to advance and bridge these two areas of inquiry and highlight the potential for their creative integration. To achieve this goal, we organise our review around the following themes: (1) identifying the promise of integrating collective behaviour and sensory ecology; (2) defining and exploring the concept of a 'sensory collective'; (3) considering the potential for sensory collectives to shape the evolution of sensory systems; (4) exploring examples from diverse taxa to illustrate neural circuits involved in sensing and collective behaviour; and (5) suggesting the need for creative conceptual and methodological advances to quantify 'sensescapes'. In the final section, (6) applications to biological conservation, we argue that these topics are timely, given the ongoing anthropogenic changes to sensory stimuli (e.g. via light, sound, and chemical pollution) which are anticipated to impact animal collectives and group-level behaviour and, in turn, ecosystem composition and function. Our synthesis seeks to provide a forward-looking perspective on how sensory ecologists and collective behaviourists can both learn from and inspire one another to advance our understanding of animal behaviour, ecology, adaptation, and evolution., Competing Interests: HW, VS, EH, GG, NB, GF, IC, CG, ND, HR, MH, JH, AS, AM No competing interests declared, (© 2023, Williams, Sridhar, Hurme et al.)

Color signals play an important role in intraspecific communication and are well studied in catarrhine primates, which exhibit uniform trichromatic vision that is well suited to detecting such signals. Platyrrhine primates exhibit polymorphic color vision with different individuals possessing different color vision types in most species. Intriguingly, some platyrrhine species exhibit bare faces, which are convergent with those of catarrhines. However, putative functions of bare-faced color signals in platyrrhines remain largely unexplored. We measured facial skin color of five captive golden lion tamarins (Leontopithecus rosalia) using color-calibrated digital photography and modeled these colors to the visual systems of the species. Our results show that facial coloration is different between infant and older adults and varies across reproductive condition, but not between breeding and nonbreeding adults. While preliminary, our study suggests that facial coloration may be involved in sociosexual signaling in golden lion tamarins, and provides intriguing evidence that we hope might stimulate more studies of bare-faced signaling in platyrrhines., (© 2023 The Authors. American Journal of Primatology published by Wiley Periodicals LLC.)

Understanding diet selectivity is a longstanding goal in primate ecology. Deciphering when and why primates consume different resources can provide insights into their nutritional ecology as well as adaptations to food scarcity. Plant pith, the spongy interior of plant stems, is occasionally eaten by primates, but the context is poorly understood. We examine the ecological, mechanical, chemical, and nutritional basis of plant pith selection by a wild, frugivorous-omnivorous primate (Cebus imitator). We test the hypothesis that pith is a fallback food, that is, consumed when fruit is less abundant, and test for differences between plant species from which pith is eaten versus avoided. We collected 3.5 years of capuchin pith consumption data to document dietary species and analyzed "pith patch visits" in relation to fruit availability, visits to fruit patches, and climatic seasonality. We analyzed dietary and non-dietary species for relative pith quantity, mechanical hardness, odor composition, and macronutrient concentrations. Capuchins ate pith from 11 of  ~300 plant species common in the dry forest, most commonly Bursera simaruba. We find that pith consumption is not directly related to fruit availability or fruit foraging but occurs most frequently (84% of patch visits) during the months of seasonal transition. Relative to common non-dietary species, dietary pith species have relatively higher pith quantity, have softer outer branches and pith, and contain more terpenoids, a class of bioactive compounds notable for their widespread medicinal properties. Our results suggest that greater pith quantity, lower hardness, and a more complex, terpenoid-rich odor profile contribute to species selectivity; further, as pith is likely to be consistently available throughout the year, the seasonality of pith foraging may point to zoopharmacognosy, as seasonal transitions typically introduce new parasites or pathogens. Our study furthers our understanding of how climatic seasonality impacts primate behavior and sheds new light on food choice by an omnivorous primate., (© 2023 The Authors. American Journal of Primatology published by Wiley Periodicals LLC.)

Studying fruit traits and their interactions with seed dispersers can improve how we interpret patterns of biodiversity, ecosystem function and evolution. Mounting evidence suggests that fruit ethanol is common and variable, and may exert selective pressures on seed dispersers. To test this, we comprehensively assess fruit ethanol content in a wild ecosystem and explore sources of variation. We hypothesize that both phylogeny and seed dispersal syndrome explain variation in ethanol levels, and we predict that fruits with mammalian dispersal traits will contain higher levels of ethanol than those with bird dispersal traits. We measured ripe fruit ethanol content in species with mammal- ( n = 16), bird- ( n = 14) or mixed-dispersal ( n = 7) syndromes in a Costa Rican tropical dry forest. Seventy-eight per cent of fruit species yielded measurable ethanol concentrations. We detected a phylogenetic signal in maximum ethanol levels (Pagel's λ = 0.82). Controlling for phylogeny, we observed greater ethanol concentrations in mammal-dispersed fruits, indicating that dispersal syndrome helps explain variation in ethanol content, and that mammals may be more exposed to ethanol in their diets than birds. Our findings further our understanding of wild fruit ethanol and its potential role as a selective pressure on frugivore sensory systems and metabolism.

Dietary variation within and across species drives the eco-evolutionary responsiveness of genes necessary to metabolize nutrients and other components. Recent evidence from humans and other mammals suggests that sugar-rich diets of floral nectar and ripe fruit have favoured mutations in, and functional preservation of, the ADH7 gene, which encodes the ADH class 4 enzyme responsible for metabolizing ethanol. Here we interrogate a large, comparative dataset of ADH7 gene sequence variation, including that underlying the amino acid residue located at the key site (294) that regulates the affinity of ADH7 for ethanol. Our analyses span 171 mammal species, including 59 newly sequenced. We report extensive variation, especially among frugivorous and nectarivorous bats, with potential for functional impact. We also report widespread variation in the retention and probable pseudogenization of ADH7 . However, we find little statistical evidence of an overarching impact of dietary behaviour on putative ADH7 function or presence of derived alleles at site 294 across mammals, which suggests that the evolution of ADH7 is shaped by complex factors. Our study reports extensive new diversity in a gene of longstanding ecological interest, offers new sources of variation to be explored in functional assays in future study, and advances our understanding of the processes of molecular evolution., Competing Interests: We declare we have no competing interests., (© 2023 The Authors.)

Chemosensation (olfaction, taste) is essential for detecting and assessing foods, such that dietary shifts elicit evolutionary changes in vertebrate chemosensory genes. The transition from hunting and gathering to agriculture dramatically altered how humans acquire food. Recent genetic and linguistic studies suggest agriculture may have precipitated olfactory degeneration. Here, we explore the effects of subsistence behaviors on olfactory (OR) and taste (TASR) receptor genes among rainforest foragers and neighboring agriculturalists in Africa and Southeast Asia. We analyze 378 functional OR and 26 functional TASR genes in 133 individuals across populations in Uganda (Twa, Sua, BaKiga) and the Philippines (Agta, Mamanwa, Manobo) with differing subsistence histories. We find no evidence of relaxed selection on chemosensory genes in agricultural populations. However, we identify subsistence-related signatures of local adaptation on chemosensory genes within each geographic region. Our results highlight the importance of culture, subsistence economy, and drift in human chemosensory perception., (© 2023. The Author(s).)

The rich diversity of morphology and behavior displayed across primate species provides an informative context in which to study the impact of genomic diversity on fundamental biological processes. Analysis of that diversity provides insight into long-standing questions in evolutionary and conservation biology and is urgent given severe threats these species are facing. Here, we present high-coverage whole-genome data from 233 primate species representing 86% of genera and all 16 families. This dataset was used, together with fossil calibration, to create a nuclear DNA phylogeny and to reassess evolutionary divergence times among primate clades. We found within-species genetic diversity across families and geographic regions to be associated with climate and sociality, but not with extinction risk. Furthermore, mutation rates differ across species, potentially influenced by effective population sizes. Lastly, we identified extensive recurrence of missense mutations previously thought to be human specific. This study will open a wide range of research avenues for future primate genomic research.

Purpose: Rhesus macaques (Macaca mulatta) are the premier nonhuman primate model for studying human health and disease. We investigated if age was associated with clinically relevant ocular features in a large cohort of free-ranging rhesus macaques from Cayo Santiago, Puerto Rico., Methods: We evaluated 120 rhesus macaques (73 males, 47 females) from 0 to 29 years old (mean ± SD: 12.6 ± 6.4) from September to December 2021. The ophthalmic evaluation included intraocular pressure (IOP) assessment, corneal pachymetry, biomicroscopy, A-scan biometry, automated refraction, and fundus photography after pupil dilation. The associations of age with the outcomes were investigated through multilevel mixed-effects models adjusted for sex and weight., Results: On average, IOP, pachymetry, axial length, and automated refraction spherical equivalent were 18.37 ± 4.68 mmHg, 474.43 ± 32.21 µm, 19.49 ± 1.24 mm, and 0.30 ± 1.70 diopters (D), respectively. Age was significantly associated with pachymetry (β coefficient = -1.20; 95% confidence interval [CI], -2.27 to -0.14; P = 0.026), axial length (β coefficient = 0.03; 95% CI, 0.01 to 0.05; P = 0.002), and spherical equivalent (β coefficient = -0.12; 95% CI, -0.22 to -0.02; P = 0.015). No association was detected between age and IOP. The prevalence of cataracts in either eye was 10.83% (95% CI, 6.34-17.89) and was significantly associated with age (odds ratio [OR] = 1.20; 95% CI, 1.06-1.36; P = 0.004). Retinal drusen in either eye was observed in 15.00% (95% CI, 9.60-22.68) of animals, which was also significantly associated with age (OR = 1.14; 95% CI, 1.02-1.27; P = 0.020)., Conclusions: Rhesus macaques exhibit age-related ocular associations similar to those observed in human aging, including decreased corneal thickness, increased axial length, myopic shift, and higher prevalence of cataract and retinal drusen.

Coevolution between signalers and receivers has played a significant role in the diversity of animal signals and sensory systems. Platyrrhines (monkeys in the Americas) exhibit a remarkable color vision polymorphism that may have been selected by both natural and sexual selection, but sociosexual color signaling among platyrrhines has received almost no attention. Here, we study the color of reproductive skin among different reproductive classes in free-ranging female saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins, modeling color spaces, and contrasts for the different visual systems. We find that the chromatic saturation and luminance of genital color vary between reproductive classes in saddleback tamarins. Chromatic contrast between the vulva and belly is lower in the parous females (PFs) relative to adult but not currently breeding females, while achromatic contrast is higher in PFs in saddleback tamarins relative to nonparous females. However, in emperor tamarins, genital color (saturation, hue, and luminance) does not vary between reproductive classes. Overall, genital skin color variation is present in tamarins and may play a role in sexual signaling. Nevertheless, the patterns are inconsistent between species, suggesting interspecific variation. Future studies should integrate the perceiver's behavioral responses and the physical and social signaling environments into comprehensive studies of communication as well as consider the role and interaction between multiple sensory modalities., (© 2022 Wiley Periodicals LLC.)

Twenty years ago, Dominy and colleagues published "The sensory ecology of primate food perception," an impactful review that brought new perspectives to understanding primate foraging adaptations. Their review synthesized information on primate senses and explored how senses informed feeding behavior. Research on primate sensory ecology has seen explosive growth in the last two decades. Here, we revisit this important topic, focusing on the numerous new discoveries and lines of innovative research. We begin by reviewing each of the five traditionally recognized senses involved in foraging: audition, olfaction, vision, touch, and taste. For each sense, we provide an overview of sensory function and comparative ecology, comment on the state of knowledge at the time of the original review, and highlight advancements and lingering gaps in knowledge. Next, we provide an outline for creative, multidisciplinary, and innovative future research programs that we anticipate will generate exciting new discoveries in the next two decades., (© 2022 Wiley Periodicals LLC.)

Aging is accompanied by a host of social and biological changes that correlate with behavior, cognitive health and susceptibility to neurodegenerative disease. To understand trajectories of brain aging in a primate, we generated a multiregion bulk (N = 527 samples) and single-nucleus (N = 24 samples) brain transcriptional dataset encompassing 15 brain regions and both sexes in a unique population of free-ranging, behaviorally phenotyped rhesus macaques. We demonstrate that age-related changes in the level and variance of gene expression occur in genes associated with neural functions and neurological diseases, including Alzheimer's disease. Further, we show that higher social status in females is associated with younger relative transcriptional ages, providing a link between the social environment and aging in the brain. Our findings lend insight into biological mechanisms underlying brain aging in a nonhuman primate model of human behavior, cognition and health., (© 2022. The Author(s), under exclusive licence to Springer Nature America, Inc.)

Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use.

Senses form the interface between animals and environments, and provide a window into the ecology of past and present species. However, research on sensory behaviours by wild frugivores is sparse. Here, we examine fruit assessment by three sympatric primates ( Alouatta palliata , Ateles geoffroyi and Cebus imitator ) to test the hypothesis that dietary and sensory specialization shape foraging behaviours. Ateles and Cebus groups are comprised of dichromats and trichromats, while all Alouatta are trichomats. We use anatomical proxies to examine smell, taste and manual touch, and opsin genotyping to assess colour vision. We find that the frugivorous spider monkeys ( Ateles geoffroyi ) sniff fruits most often, omnivorous capuchins ( Cebus imitator ), the species with the highest manual dexterity, use manual touch most often, and that main olfactory bulb volume is a better predictor of sniffing behaviour than nasal turbinate surface area. We also identify an interaction between colour vision phenotype and use of other senses. Controlling for species, dichromats sniff and bite fruits more often than trichromats, and trichromats use manual touch to evaluate cryptic fruits more often than dichromats. Our findings reveal new relationships among dietary specialization, anatomical variation and foraging behaviour, and promote understanding of sensory system evolution.

A defining feature of catarrhine primates is uniform trichromacy-the ability to distinguish red (long; L), green (medium; M), and blue (short; S) wavelengths of light. Although the tuning of photoreceptors is conserved, the ratio of L:M cones in the retina is variable within and between species, with human cone ratios differing from other catarrhines. Yet, the sources and structure of variation in cone ratios are poorly understood, precluding a broader understanding of color vision variability. Here, we report a large-scale study of a pedigreed population of rhesus macaques (Macaca mulatta). We collected foveal RNA and analyzed opsin gene expression using cDNA and estimated additive genetic variance of cone ratios. The average L:M ratio and standard error was 1.03:1 ± 0.02. There was no age effect, and genetic contribution to variation was negligible. We found marginal sex effects with females having larger ratios than males. S cone ratios (0.143:1 ± 0.002) had significant genetic variance with a heritability estimate of 43% but did not differ between sexes or age groups. Our results contextualize the derived human condition of L-cone dominance and provide new information about the heritability of cone ratios and variation in primate color vision., (© 2022 The Authors. Evolution published by Wiley Periodicals LLC on behalf of The Society for the Study of Evolution.)

Mitochondrial DNA remains a cornerstone for molecular ecology, especially for study species from which high-quality tissue samples cannot be easily obtained. Methods using mitochondrial markers are usually reliant on reference databases, but these are often incomplete. Furthermore, available mitochondrial genomes often lack crucial metadata, such as sampling location, limiting their utility for many analyses. Here, we assembled 205 new mitochondrial genomes for platyrrhine primates, most from the Amazon and with known sampling locations. We present a dated mitogenomic phylogeny based on these samples along with additional published platyrrhine mitogenomes, and use this to assess support for the long-standing riverine barrier hypothesis (RBH), which proposes that river formation was a major driver of speciation in Amazonian primates. Along the Amazon, Negro, and Madeira rivers, we found mixed support for the RBH. While we identified divergences that coincide with a river barrier, only some occur synchronously and also overlap with the proposed dates of river formation. The most compelling evidence is for the Amazon river potentially driving speciation within bearded saki monkeys (Chiropotes spp.) and within the smallest extant platyrrhines, the marmosets and tamarins. However, we also found that even large rivers do not appear to be barriers for some primates, including howler monkeys (Alouatta spp.), uakaris (Cacajao spp.), sakis (Pithecia spp.), and robust capuchins (Sapajus spp.). Our results support a more nuanced, clade-specific effect of riverine barriers and suggest that other evolutionary mechanisms, besides the RBH and allopatric speciation, may have played an important role in the diversification of platyrrhines., (© 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)

Primates have adapted to numerous environments and lifestyles but very few species are native to high elevations. Here we investigated high-altitude adaptations in the gelada (Theropithecus gelada), a monkey endemic to the Ethiopian Plateau. We examined genome-wide variation in conjunction with measurements of haematological and morphological traits. Our new gelada reference genome is highly intact and assembled at chromosome-length levels. Unexpectedly, we identified a chromosomal polymorphism in geladas that could potentially contribute to reproductive barriers between populations. Compared with baboons at low altitude, we found that high-altitude geladas exhibit significantly expanded chest circumferences, potentially allowing for greater lung surface area for increased oxygen diffusion. We identified gelada-specific amino acid substitutions in the alpha-chain subunit of adult haemoglobin but found that gelada haemoglobin does not exhibit markedly altered oxygenation properties compared with lowland primates. We also found that geladas at high altitude do not exhibit elevated blood haemoglobin concentrations, in contrast to the normal acclimatization response to hypoxia in lowland primates. The absence of altitude-related polycythaemia suggests that geladas are able to sustain adequate tissue-oxygen delivery despite environmental hypoxia. Finally, we identified numerous genes and genomic regions exhibiting accelerated rates of evolution, as well as gene families exhibiting expansions in the gelada lineage, potentially reflecting altitude-related selection. Our findings lend insight into putative mechanisms of high-altitude adaptation while suggesting promising avenues for functional hypoxia research., (© 2022. The Author(s), under exclusive licence to Springer Nature Limited.)

Capuchins are platyrrhines (monkeys found in the Americas) within the Cebidae family. For most of their taxonomic history, the two main morphological types of capuchins, gracile (untufted) and robust (tufted), were assigned to a single genus, Cebus . Further, all tufted capuchins were assigned to a single species, Cebus apella , despite broad geographic ranges spanning Central and northern South America. In 2012, tufted capuchins were assigned to their genus, Sapajus , with eight currently recognized species and five Cebus species, although these numbers are still under debate. Alu retrotransposons are a class of mobile element insertion (MEI) widely used to study primate phylogenetics. However, Alu elements have rarely been used to study capuchins. Recent genome-level assemblies for capuchins ( Cebus imitator ; [Cebus&#95;imitator&#95;1.0] and Sapajus apella [GSC&#95;monkey&#95;1.0]) facilitated large scale ascertainment of young lineage-specific Alu insertions. Reported here are 1607 capuchin specific and 678 Sapajus specific Alu insertions along with candidate oligonucleotides for locus-specific PCR assays for many elements. PCR analyses identified 104 genus level and 51 species level Alu insertion polymorphisms. The Alu datasets reported in this study provide a valuable resource that will assist in the classification of archival samples lacking phenotypic data and for the study of capuchin phylogenetic relationships.

Taste perception plays an essential role in food selection. Umami (savory) tastes are sensed by a taste receptor complex, T1R1/T1R3, that detects proteinogenic amino acids. 1 High sensitivity to l-glutamate (l-Glu) is a characteristic of human T1R1/T1R3, but the T1R1/T1R3 of other vertebrates does not consistently show this l-Glu response. 1 , 2 Here, we demonstrate that the l-Glu sensitivity of T1R1/T1R3 is a derived state that has evolved repeatedly in large primates that rely on leaves as protein sources, after their divergence from insectivorous ancestors. Receptor expression experiments show that common amino acid substitutions at ligand binding sites that render T1R1/T1R3 sensitive to l-Glu occur independently at least three times in primate evolution. Meanwhile T1R1/T1R3 senses 5'-ribonucleotides as opposed to l-Glu in several mammalian species, including insectivorous primates. Our chemical analysis reveal that l-Glu is one of the major free amino acids in primate diets and that insects, but not leaves, contain large amounts of free 5'-ribonucleotides. Altering the ligand-binding preference of T1R1/T1R3 from 5'-ribonucleotides to l-Glu might promote leaf consumption, overcoming bitter and aversive tastes. Altogether, our results provide insight into the foraging ecology of a diverse mammalian radiation and help reveal how evolution of sensory genes facilitates invasion of new ecological niches., Competing Interests: Declaration of Interests The authors declare no competing interest., (Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.)

For female mammals, communicating the timing of ovulation is essential for reproduction. Olfactory communication via volatile organic compounds (VOCs) can play a key role. We investigated urinary VOCs across the oestrous cycle using laboratory mice. We assessed the oestrous stage through daily vaginal cytology and analysed urinary VOCs using headspace gas chromatography-mass spectrometry (GC-MS), testing a portable GC-MS against a benchtop system. We detected 65 VOCs from 40 samples stored in VOC traps and analysed on a benchtop GC-MS, and 15 VOCs from 90 samples extracted by solid-phase microextraction (SPME) and analysed on a portable GC-MS. Only three compounds were found in common between the two techniques. Urine collected from the fertile stages of the oestrous cycle had increased quantities of a few notable VOCs compared with urine from non-fertile stages. These VOCs may be indicators of fertility. However, we did not find significant differences in chemical composition among oestrous stages. It is possible that changes in VOC abundance were too small to be detected by our analytical methods. Overall, the use of VOC traps combined with benchtop GC-MS was the more successful of the two methods, yet portable GC-MS systems may still have utility for some in situ applications., (© 2021 The Authors.)

The major histocompatibility complex (MHC) is an important gene complex contributing to adaptive immunity. Studies of platyrrhine MHC have focused on identifying experimental models of immune system function in the equivalent Human Leukocyte Antigen (HLA). These genes have thus been explored primarily in captive platyrrhine individuals from research colonies. However, investigations of standing MHC variation and evolution in wild populations are essential to understanding its role in immunity, sociality and ecology. Capuchins are a promising model group exhibiting the greatest habitat diversity, widest diet breadth and arguably the most social complexity among platyrrhines, together likely resulting in varied immunological challenges. We use high-throughput sequencing to characterize polymorphism in four Class II DR and DQ exons for the first time in seven capuchin species. We find evidence for at least three copies for DQ genes and at least five for DRB, with possible additional unrecovered diversity. Our data also reveal common genotypes that are inherited across our most widely sampled population, Cebus imitator in Sector Santa Rosa, Costa Rica. Notably, phylogenetic analyses reveal that platyrrhine DQA sequences form a monophyletic group to the exclusion of all Catarrhini sequences examined. This result is inconsistent with the trans-species hypothesis for MHC evolution across infraorders in Primates and provides further evidence for the independent origin of current MHC genetic diversity in Platyrrhini. Identical allele sharing across cebid species, and more rarely genera, however, does underscore the complexity of MHC gene evolution and the need for more comprehensive assessments of allelic diversity and genome structure., Competing Interests: The authors have declared that no competing interests exist.

Objectives: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits., Materials and Methods: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates., Results: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%-3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late-stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures., Discussion: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods., (© 2021 Wiley Periodicals LLC.)

The novel coronavirus SARS-CoV-2, which in humans leads to the disease COVID-19, has caused global disruption and more than 2 million fatalities since it first emerged in late 2019. As we write, infection rates are at their highest point globally and are rising extremely rapidly in some areas due to more infectious variants. The primary target of SARS-CoV-2 is the cellular receptor angiotensin-converting enzyme-2 (ACE2). Recent sequence analyses of the ACE2 gene predict that many nonhuman primates are also likely to be highly susceptible to infection. However, the anticipated risk is not equal across the Order. Furthermore, some taxonomic groups show high ACE2 amino acid conservation, while others exhibit high variability at this locus. As an example of the latter, analyses of strepsirrhine primate ACE2 sequences to date indicate large variation among lemurs and lorises compared to other primate clades despite low sampling effort. Here, we report ACE2 gene and protein sequences for 71 individual strepsirrhines, spanning 51 species and 19 genera. Our study reinforces previous results while finding additional variability in other strepsirrhine species, and suggests several clades of lemurs have high potential susceptibility to SARS-CoV-2 infection. Troublingly, some species, including the rare and endangered aye-aye (Daubentonia madagascariensis), as well as those in the genera Avahi and Propithecus, may be at high risk. Given that lemurs are endemic to Madagascar and among the primates at highest risk of extinction globally, further understanding of the potential threat of COVID-19 to their health should be a conservation priority. All feasible actions should be taken to limit their exposure to SARS-CoV-2., (© 2021 Wiley Periodicals LLC.)

Background: An individual's microbiome changes over the course of its lifetime, especially during infancy, and again in old age. Confounding factors such as diet and healthcare make it difficult to disentangle the interactions between age, health, and microbial changes in humans. Animal models present an excellent opportunity to study age- and sex-linked variation in the microbiome, but captivity is known to influence animal microbial abundance and composition, while studies of free-ranging animals are typically limited to studies of the fecal microbiome using samples collected non-invasively. Here, we analyze a large dataset of oral, rectal, and genital swabs collected from 105 free-ranging rhesus macaques (Macaca mulatta, aged 1 month-26 years), comprising one entire social group, from the island of Cayo Santiago, Puerto Rico. We sequenced 16S V4 rRNA amplicons for all samples., Results: Infant gut microbial communities had significantly higher relative abundances of Bifidobacterium and Bacteroides and lower abundances of Ruminococcus, Fibrobacter, and Treponema compared to older age groups, consistent with a diet high in milk rather than solid foods. The genital microbiome varied widely between males and females in beta-diversity, taxonomic composition, and predicted functional profiles. Interestingly, only penile, but not vaginal, microbiomes exhibited distinct age-related changes in microbial beta-diversity, taxonomic composition, and predicted functions. Oral microbiome composition was associated with age, and was most distinctive between infants and other age classes., Conclusions: Across all three body regions, with notable exceptions in the penile microbiome, while infants were distinctly different from other age groups, microbiomes of adults were relatively invariant, even in advanced age. While vaginal microbiomes were exceptionally stable, penile microbiomes were quite variable, especially at the onset of reproductive age. Relative invariance among adults, including elderly individuals, is contrary to findings in humans and mice. We discuss potential explanations for this observation, including that age-related microbiome variation seen in humans may be related to changes in diet and lifestyle. Video abstract.

Chemosignals are mediators of social interactions in mammals, providing con- and hetero-specifics with information on fixed (e.g., species, sex, group, and individual identity) and variable (e.g., social, reproductive, and health status) features of the signaler. Yet, methodological difficulties of recording and quantifying odor signals, especially in field conditions, have hampered studies of natural systems. We present the first use of the Torion® portable gas chromatography-mass spectrometry (GC-MS) instrument for in situ chemical analysis of primate scents. We collected and analyzed swab samples from the scent glands and skin from 13 groups (57 individuals) of two sympatric species of wild emperor tamarins, Saguinus imperator, and Weddell's saddleback tamarins, Leontocebus weddelli (Callitrichidae). In total, 11 compounds of interest (i.e., probably derived from the animals) could be detected in the samples, with 31 of 215 samples containing at least one compound of interest. The composition of these 31 samples varied systematically with species, group, sex, and breeding status. Moreover, we tentatively identified seven of the compounds of interest as methyl hexanoate, benzaldehyde, ethyl hexanoate, acetophenone, a branched C15 alkane, 4-methoxybenzaldehyde, and hexadecan-1-ol. As the field of primate semiochemistry continues to grow, we believe that portable GC-MS instruments have the potential to help make progress in the study of primate chemosignaling in field conditions, despite limitations that we encountered. We further provide recommendations for future use of the Torion® portable GC-MS for in situ analyses., (© 2021 Wiley Periodicals LLC.)

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., Competing Interests: The authors declare no competing interest., (Copyright © 2021 the Author(s). Published by PNAS.)

The emergence of SARS-CoV-2 has caused over a million human deaths and massive global disruption. The viral infection may also represent a threat to our closest living relatives, nonhuman primates. The contact surface of the host cell receptor, ACE2, displays amino acid residues that are critical for virus recognition, and variations at these critical residues modulate infection susceptibility. Infection studies have shown that some primate species develop COVID-19-like symptoms; however, the susceptibility of most primates is unknown. Here, we show that all apes and African and Asian monkeys (catarrhines), exhibit the same set of twelve key amino acid residues as human ACE2. Monkeys in the Americas, and some tarsiers, lemurs and lorisoids, differ at critical contact residues, and protein modeling predicts that these differences should greatly reduce SARS-CoV-2 binding affinity. Other lemurs are predicted to be closer to catarrhines in their susceptibility. Our study suggests that apes and African and Asian monkeys, and some lemurs, are likely to be highly susceptible to SARS-CoV-2. Urgent actions have been undertaken to limit the exposure of great apes to humans, and similar efforts may be necessary for many other primate species.

Cannibalism has been observed in a variety of animal taxa; however, it is relatively uncommon in primates. Thus, we rely heavily on case reports of this behavior to advance our understanding of the contexts under which it occurs. Here, we report the first observation of cannibalism in a group of wild white-faced capuchin monkeys ( Cebus imitator ). The subject was a dead infant, estimated to be 10 days old, and the probable victim of infanticide. Consumption of the corpse was initiated by a 2-year-old male (second cousin of the infant), though it was eventually taken over and monopolized by the group's alpha female (grandaunt of the infant). Although most group members expressed interest in the corpse (sniffing, touching, and threatening it), no others made an attempt to consume it. Given that this is the only observation of cannibalism recorded in over 37 years of study on this population, we consider it to be a rare behavior in this species. This detailed record contributes new data, which, when combined with other reports within and across species and contexts, enables the evaluation of adaptive explanations of cannibalism., Competing Interests: None declared., (© 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.)

Humans have a long evolutionary relationship with ethanol, pre-dating anthropogenic sources, and possess unusually efficient ethanol metabolism, through a mutation that evolved in our last common ancestor with African great apes. Increased exposure to dietary ethanol through fermenting fruits and nectars is hypothesized to have selected for this in our lineage. Yet, other mammals have frugivorous and nectarivorous diets, raising the possibility of natural ethanol exposure and adaptation in other taxa. We conduct a comparative genetic analysis of alcohol dehydrogenase class IV (ADH IV) across mammals to provide insight into their evolutionary history with ethanol. We find genetic variation and multiple pseudogenization events in ADH IV, indicating the ability to metabolize ethanol is variable. We suggest that ADH enzymes are evolutionarily plastic and show promise for revealing dietary adaptation. We further highlight the derived condition of humans and draw attention to problems with modelling the physiological responses of other mammals on them, a practice that has led to potentially erroneous conclusions about the likelihood of natural intoxication in wild animals. It is a fallacy to assume that other animals share our metabolic adaptations, rather than taking into consideration each species' unique physiology.

Extreme climate events can have important consequences for the dynamics of natural populations, and severe droughts are predicted to become more common and intense due to climate change. We analysed infant mortality in relation to drought in two primate species (white-faced capuchins, Cebus capucinus imitator, and Geoffroy's spider monkeys, Ateles geoffroyi ) in a tropical dry forest in northwestern Costa Rica. Our survival analyses combine several rare and valuable long-term datasets, including long-term primate life-history, landscape-scale fruit abundance, food-tree mortality, and climate conditions. Infant capuchins showed a threshold mortality response to drought, with exceptionally high mortality during a period of intense drought, but not during periods of moderate water shortage. By contrast, spider monkey females stopped reproducing during severe drought, and the mortality of infant spider monkeys peaked later during a period of low fruit abundance and high food-tree mortality linked to the drought. These divergent patterns implicate differing physiology, behaviour or associated factors in shaping species-specific drought responses. Our findings link predictions about the Earth's changing climate to environmental influences on primate mortality risk and thereby improve our understanding of how the increasing severity and frequency of droughts will affect the dynamics and conservation of wild primates., Competing Interests: We declare we have no competing interests., (© 2020 The Authors.)

A key goal in behavioral ecology is to investigate the factors influencing the access to food resources and energetic condition of females, which are strong predictors of their reproductive success. We aimed to investigate how ecological factors, social factors, and reproductive state are associated with energetic condition in a wild neotropical primate using non-invasive measures. We first assessed and compared urinary C-peptide levels (uCP), the presence of urinary ketones (uKet), and behaviorally assessed energy balance (bEB) in female white-faced capuchin monkeys (Cebus imitator) living in Santa Rosa, Costa Rica. Then, we assessed how these measures were associated with feeding competition, dominance rank, and reproductive state. As predicted, uCP and bEB were positively associated with each other, and bEB was negatively associated with uKet. However, we did not find a relationship between uCP and uKet. Females showed lower uCP and bEB values during periods of intense feeding competition, but this relationship was not dependent on dominance rank. Furthermore, rank was not directly associated with uCP and bEB. Urinary ketones, on the other hand, were only produced in the most adverse conditions: by low-ranking, lactating females during periods of intense feeding competition. Behavioral strategies are assumed to maximize reproductive success and not energetic condition per se, which might explain why rank was not generally associated with energetic condition in our study population. This highlights the importance of considering potential differences between reproductive success and proxies of reproductive success, such as energetic condition or food intake, when investigating predictions of socioecological models., Competing Interests: Declaration of competing interest None., (Copyright © 2019 Elsevier Inc. All rights reserved.)

Mouse kidney parvovirus (MKPV) is a member of the provisional genus Chapparvovirus that causes renal disease in immune-compromised mice, with a disease course reminiscent of polyomavirus-associated nephropathy in immune-suppressed kidney transplant patients. Here we map four major MKPV transcripts, created by alternative splicing, to a common initiator region, and use mass spectrometry to identify "p10" and "p15" as novel chapparvovirus accessory proteins produced in MKPV-infected kidneys. p15 and the splicing-dependent putative accessory protein NS2 are conserved in all near-complete amniote chapparvovirus genomes currently available (from mammals, birds and a reptile). In contrast, p10 may be encoded only by viruses with >60% amino acid identity to MKPV. We show that MKPV is kidney-tropic and that the bat chapparvovirus DrPV-1 and a non-human primate chapparvovirus, CKPV, are also found in the kidneys of their hosts. We propose, therefore, that many mammal chapparvoviruses are likely to be nephrotropic., Competing Interests: B.R. and W.W. are co-inventors on an international patent application (PCT/AU2018/050505) submitted by the Centenary Institute that is related to the detection and use of MKPV in research and commercial applications. M.J.C is an employee of IDEXX BioAnalytics, a division of IDEXX Laboratories, Inc., a veterinary diagnostics company with a commercial interest in MKPV. B.R. is presently an employee at Novartis Institutes for BioMedical Research. Novartis did not fund the study. IDEXX BioAnalytics and Novartis had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. All other authors declare no competing interests.

Objectives: Invertebrates are important foods for many primates and provide valuable nutrients often unavailable from plant sources. We examine the diet of white-faced capuchins (Cebus capucinus imitator) to determine: (a) timing and types of invertebrate food consumption; (b) whether invertebrate consumption varies with availability of plant foods; and (c) how invertebrates contribute to energy and protein intake of females during different reproductive states., Materials and Methods: We analyze 2 years of behavioral data from 25 adult female capuchins to determine which invertebrates are eaten. We describe annual and monthly invertebrate consumption patterns, and, employing circular statistics, analyze seasonal consumption of the four most important invertebrate groups eaten. We apply logistic regression analyses to tree density and fruit energy data to determine whether capuchin invertebrate foraging is related to fruit energy availability of their most commonly consumed fruits. We evaluate the nutritional contribution of invertebrates to energetic and protein requirements of females over time and across reproductive stages., Results: Capuchins consumed invertebrates from 21 identifiable groups, but their diet was dominated by four orders: Lepidoptera, Orthoptera, Hemiptera, and Hymenoptera. All four orders were consumed in a significantly seasonal pattern, and reduced fruit energy availability was a significant predictor of increased invertebrate foraging. Capuchin females often required invertebrate energy intake to meet their overall monthly energetic needs, particularly while they were lactating, even though they appear to exceed their protein requirements every month., Discussion: These results indicate that invertebrate consumption is critical for capuchin energetic needs, particularly during periods of reduced fruit availability and lactation., (© 2019 Wiley Periodicals, Inc.)

Like catarrhines, some platyrrhines show exposed and reddish skin, raising the possibility that reddish signals have evolved convergently. This variation in skin exposure and color combined with sex-linked polymorphic color vision in platyrrhines presents a unique, and yet underexplored, opportunity to investigate the relative importance of chromatic versus achromatic signals, the influence of color perception on signal evolution, and to understand primate communication broadly. By coding the facial skin exposure and color of 96 platyrrhines, 28 catarrhines, 7 strepsirrhines, 1 tarsiiform, and 13 nonprimates, and by simulating the ancestral character states for these traits, we provide the first analysis of the distribution and evolution of facial skin exposure and color in platyrrhini. We highlight ways in which studying the presence and use of color signals by platyrrhines and other primates will enhance our understanding of the evolution of color signals, and the forces shaping color vision., (© 2019 The Authors. Evolutionary Anthropology: Issues, News, and Reviews published by Wiley Periodicals, Inc.)

The senses play critical roles in helping animals evaluate foods, including fruits that can change both in colour and scent during ripening to attract frugivores. Although numerous studies have assessed the impact of colour on fruit selection, comparatively little is known about fruit scent and how olfactory and visual data are integrated during foraging. We combine 25 months of behavioural data on 75 wild, white-faced capuchins (Cebus imitator) with measurements of fruit colours and scents from 18 dietary plant species. We show that frequency of fruit-directed olfactory behaviour is positively correlated with increases in the volume of fruit odours produced during ripening. Monkeys with red-green colour blindness sniffed fruits more often, indicating that increased reliance on olfaction is a behavioural strategy that mitigates decreased capacity to detect red-green colour contrast. These results demonstrate a complex interaction among fruit traits, sensory capacities and foraging strategies, which help explain variation in primate behaviour.

Treeshrews are small, squirrel-like mammals in the order Scandentia, which is nested together with Primates and Dermoptera in the superordinal group Euarchonta. They are often described as living fossils, and researchers have long turned to treeshrews as a model or ecological analogue for ancestral primates. A comparative study of colour vision-encoding genes within Scandentia found a derived amino acid substitution in the long-wavelength sensitive opsin gene ( OPN1LW ) of the Bornean smooth-tailed treeshrew ( Dendrogale melanura ). The opsin, by inference, is red-shifted by ca 6 nm with an inferred peak sensitivity of 561 nm. It is tempting to view this trait as a novel visual adaptation; however, the genetic and functional diversity of visual pigments in treeshrews is unresolved outside of Borneo. Here, we report gene sequences from the northern smooth-tailed treeshrew ( Dendrogale murina ) and the Mindanao treeshrew ( Tupaia everetti , the senior synonym of Urogale everetti ). We found that the opsin genes are under purifying selection and that D. murina shares the same substitution as its congener, a result that distinguishes Dendrogale from other treeshrews, including T. everetti. We discuss the implications of opsin functional variation in light of limited knowledge about the visual ecology of smooth-tailed treeshrews., Competing Interests: We have no competing interests.