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Abstract Life history theory predicts that organisms allocate resources across physiological processes to maximize fitness. Under this framework, early life adversity (ELA)—which often limits energetic capital—could shape investment in growth and reproduction, as well as trade-offs between them, ultimately contributing to variation in evolutionary fitness. Using long-term demographic, behavioral, and physiological data for 2,100 females from a non-human primate population, we tested whether naturally-occurring ELA influences investment in the competing physiological demands of growth and reproduction. By analyzing ELA, growth, and reproduction in the same individuals, we also assessed whether adversity intensifies trade-offs between life history domains. We found that ELA influenced life history patterns, and was associated with modified growth, delayed reproductive maturity, and small adult body size. Different types of ELA sometimes had distinct reproductive outcomes—e.g., large group size was linked to faster reproductive rates, while low maternal rank predicted slower ones. Adversity also amplified trade-offs between growth and reproduction: small body size was a stronger predictor of delayed and reduced reproductive output in females exposed to ELA, compared to those not exposed. Finally, we examined how traits modified by ELA related to lifetime reproductive success. Across the population, starting reproduction earlier and maintaining a moderate reproductive rate conferred the greatest number of offspring surviving to reproductive maturity. These findings suggest that ELA impacts key life history traits as well as relationships between them, and can constrain individuals from adopting the most optimal reproductive strategy. Significance StatementEarly life adversity (ELA) can have lasting effects on evolutionary fitness (e.g., the number of surviving offspring an animal produces); however, the paths connecting ELA to fitness—for example by influencing growth, reproductive timing or rate, or trade-offs between these processes—remain unclear. Leveraging long-term behavioral, physiological, and demographic data from 2,100 female rhesus macaques, we found that ELA-exposed females exhibited growth and reproductive schedules associated with less-optimal lifetime fitness outcomes. Further, ELA intensified trade-offs between growth and reproduction, suggesting that affected individuals face steeper energetic constraints. Our findings highlight the long-lasting impacts of ELA on traits of evolutionary and biomedical importance in a non-human primate model with relevance to humans. 

Age and early life adversity (ELA) are both key determinants of health, but whether they target similar physiological mechanisms across the body is unknown due to limited multi-tissue datasets from well-characterized cohorts. We generated DNA methylation (DNAm) profiles across 14 tissues in 237 semi-free ranging rhesus macaques, with records of naturally occurring ELA. We show that age-associated DNAm variation is predominantly tissue-dependent, yet tissue-specific epigenetic clocks reveal that the pace of epigenetic aging is relatively consistent within individuals. ELA effects on loci are adversity-dependent, but a given ELA has a coordinated impact across tissues. Finally, ELA targeted many of the same loci as age, but the direction of these effects varied, indicating that ELA does not uniformly contribute to accelerated age in the epigenome. ELA thus imprints a coordinated, tissue-spanning epigenetic signature that is both distinct from and intertwined with age-related change, advancing our understanding of how early environments sculpt the molecular foundations of aging and disease. 

Characterizing DNA methylation patterns is important for addressing key questions in evolutionary biology, development, 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 is currently lacking. To address this gap, we optimized the Targeted Methylation Sequencing protocol (TMS)—which profiles ~4 million CpG sites—for miniaturization, flexibility, and multispecies use. 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 confirmed that estimates of 1) epigenetic age and 2) tissue-specific DNA methylation patterns are strongly recapitulated using data generated from TMS versus other technologies. 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. 

Identifying biomarkers of age-related changes in immune system functioning that can be measured non-invasively is a significant step in progressing research on immunosenescence and inflammaging in free-ranging and wild animal populations. In the present study, we aimed to investigate the suitability of two urinary compounds, neopterin and suPAR, as biomarkers of age-related changes in immune activation and inflammation in a free-ranging rhesus macaque ( Macaca mulatta ) population. We also investigated age-associated variation in gene transcription from blood samples to understand the underlying proximate mechanisms that drive age-related changes in urinary neopterin or suPAR. Neopterin was significantly positively correlated with age, and had a moderate within-individual repeatability, indicating it is applicable as a biomarker of age-related changes. The age-related changes in urinary neopterin are not apparently driven by an age-related increase in the primary signaler of neopterin, IFN-y, but may be driven instead by an age-related increase in both CD14+ and CD14− monocytes. suPAR was not correlated with age, and had low repeatability within-individuals, indicating that it is likely better suited to measure acute inflammation rather than chronic age-related increases in inflammation (i.e., “inflammaging”). Neopterin and suPAR had a correlation of 25%, indicating that they likely often signal different processes, which if disentangled could provide a nuanced picture of immune-system function and inflammation when measured in tandem. 

Brain structure is predicted by social network size but not other key social attributes in free-ranging monkeys. 

Abstract ObjectiveReconstructing the social lives of extinct primates is possible only through an understanding of the interplay between morphology, sexual selection pressures, and social behavior in extant species. Somatic sexual dimorphism is an important variable in primate evolution, in part because of the clear relationship between the strength and mechanisms of sexual selection and the degree of dimorphism. Here, we examine body size dimorphism across ontogeny in male and female rhesus macaques to assess whether it is primarily achieved via bimaturism as predicted by a polygynandrous mating system, faster male growth indicating polygyny, or both. MethodsWe measured body mass in a cross‐sectional sample of 362 free‐ranging rhesus macaques from Cayo Santiago, Puerto Rico to investigate size dimorphism: (1) across the lifespan; and (2) as an outcome of sex‐specific growth strategies, including: (a) age of maturation; (b) growth rate; and (c) total growth duration, using regression models fit to sex‐specific developmental curves. ResultsSignificant body size dimorphism was observed by prime reproductive age with males 1.51 times the size of females. Larger male size resulted from a later age of maturation (males: 6.8–7.8 years vs. females: 5.5–6.5 years; logistic model) and elevated growth velocity through the pre‐prime period (LOESS model). Though males grew to larger sizes overall, females maintained adult size for longer before senescence (quadratic model). DiscussionThe ontogeny of size dimorphism in rhesus macaques is achieved by bimaturism and a faster male growth rate. Our results provide new data for understanding the development and complexities of primate dimorphism.