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Across mammals, fertility and offspring survival are often lowest at the beginning and end of females’ reproductive careers. However, extrinsic drivers of reproductive success—including infanticide by males—could stochastically obscure these expected age-related trends. Here, we modelled reproductive ageing trajectories in two cercopithecine primates that experience high rates of male infanticide: the chacma baboon (Papio ursinus) and the gelada (Theropithecus gelada). We found that middle-aged mothers generally achieved the shortest interbirth intervals in chacma baboons. By contrast, old gelada females often showed shorter interbirth intervals than their younger group-mates with one exception: the oldest females typically failed to produce additional offspring before their deaths. Infant survival peaked in middle-aged mothers in chacma baboons but in young mothers in geladas. While infant mortality linked with maternal death increased as mothers aged in both species, infanticide risk did not predictably shift with maternal age. Thus, infanticide patterns cannot explain the surprising young mother advantage observed in geladas. Instead, we argue that this could be a product of their graminivorous diets, which might remove some energetic constraints on early reproduction. In sum, our data suggest that reproductive ageing is widespread but may be differentially shaped by ecological pressures. 

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. 

Abstract Neopterin, a product of activated white blood cells, is a marker of nonspecific inflammation that can capture variation in immune investment or disease-related immune activity and can be collected noninvasively in urine. Mounting studies in wildlife point to lifetime patterns in neopterin related to immune development, aging, and certain diseases, but rarely are studies able to assess whether neopterin can capture multiple concurrent dimensions of health and disease in a single system. We assessed the relationship between urinary neopterin stored on filter paper and multiple metrics of health and disease in wild geladas (Theropithecus gelada), primates endemic to the Ethiopian highlands. We tested whether neopterin captures age-related variation in inflammation arising from developing immunity in infancy and chronic inflammation in old age, inflammation related to intramuscular tapeworm infection, helminth-induced anti-inflammatory immunomodulation, and perturbations in the gastrointestinal microbiome. We found that neopterin had a U-shaped relationship with age, no association with larval tapeworm infection, a negative relationship with metrics related to gastrointestinal helminth infection, and a negative relationship with microbial diversity. Together with growing research on neopterin and specific diseases, our results demonstrate that urinary neopterin can be a powerful tool for assessing multiple dimensions of health and disease in wildlife. 

Abstract Male reproductive competition can select for condition‐dependent, conspicuous traits that signal some aspect of fighting ability and facilitate assessment of potential rivals. However, the underlying mechanisms that link the signal to a male's current condition are difficult to investigate in wild populations, often requiring invasive experimental manipulation. Here, we use digital photographs and chest skin samples to investigate the mechanisms of a visual signal used in male competition in a wild primate, the red chest patch in geladas (Theropithecus gelada). We analysed photographs collected during natural (n = 144) and anaesthetized conditions (n = 38) to understand variability in male and female chest redness, and we used chest skin biopsies (n = 38) to explore sex differences in gene expression. Male and female geladas showed similar average redness, but males exhibited a wider within‐individual range in redness under natural conditions. These sex differences were also reflected at the molecular level, with 10.5% of genes exhibiting significant sex differences in expression. Subadult males exhibited intermediate gene expression patterns between adult males and females, pointing to mechanisms underlying the development of the red chest patch. We found that genes more highly expressed in males were associated with blood vessel development and maintenance but not with androgen or oestrogen activity. Together, our results suggest male gelada redness variability is driven by increased blood vessel branching in the chest skin, providing a potential link between male chest redness and current condition as increased blood circulation to exposed skin could lead to heat loss in the cold, high‐altitude environment of geladas. 

Abstract Understanding how ecology and phylogeny shape parasite communities can inform parasite control and wildlife conservation initiatives while contributing to the study of host species evolution.We tested the relative strengths of phylogeny and ecology in driving parasite community structure in a host whose ecology diverges significantly from that of its closest phylogenetic relatives.We characterized the gastrointestinal (GI) parasite community of wild geladasTheropithecus gelada, primates that are closely related to baboons but specialized to graminovory in the Ethiopian Highlands.Geladas exhibited very constrained GI parasite communities: only two genera (OesophagostomumandTrichostrongylus) were identified across 305 samples. This is far below the diversity reported for baboons (Papiospp.) and at the low end of the range of domestic grazers (e.g.Bos taurus,Ovis aries) inhabiting the same region and ecological niche.Using deep amplicon sequencing, we identified 15 amplicon sequence variants (ASVs) within the two genera, seven of which matched toOesophagostomumsp., seven toTrichostrongylussp., and one toT. vitrinus.Population was an important predictor of ASV richness. Geladas in the most ecologically disturbed area of the national park exhibited approximately four times higher ASV richness than geladas at a less disturbed location within the park.In this system, ecology was a stronger predictor of parasite community structure than was phylogeny, with geladas sharing more elements of their parasite communities with other grazers in the same area than with closely related sister taxa. A freePlain Language Summarycan be found within the Supporting Information of this article.