Urinary neopterin reflects immunological variation associated with age, helminth parasitism, and the microbiome in a wild primate.

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.

Social drivers of maturation age in female geladas.

Female reproductive maturation is a critical life-history milestone, initiating an individual's reproductive career. Studies in social mammals have often focused on how variables related to nutrition influence maturation age in females. However, parallel investigations have identified conspicuous male-mediated effects in which female maturation is sensitive to the presence and relatedness of males. Here, we evaluated whether the more "classic" socioecological variables (i.e., maternal rank, group size) predict maturation age in wild geladas-a primate species with known male-mediated effects on maturation and a grassy diet that is not expected to generate intense female competition. Females delayed maturation in the presence of their fathers and quickly matured when unrelated, dominant males arrived. Controlling for these male effects, however, higher-ranking daughters matured at earlier ages than lower-ranking daughters, suggesting an effect of within-group contest competition. However, contrary to predictions related to within-group scramble competition, females matured earliest in larger groups. We attribute this result to either: 1) a shift to "faster" development in response to the high infant mortality risk posed by larger groups; or 2) accelerated maturation triggered by brief, unobserved male visits. While earlier ages at maturation were indeed associated with earlier ages at first birth, these benefits were occasionally offset by male takeovers, which can delay successful reproduction via spontaneous abortion. In sum, rank-related effects on reproduction can still occur even when socioecological theory would predict otherwise, and males (and the risks they pose) may prompt female maturation even outside of successful takeovers.

The Goldilocks effect: female geladas in mid-sized groups have higher fitness.

The cost-benefit ratio of group living is thought to vary with group size: individuals in 'optimally sized' groups should have higher fitness than individuals in groups that are either too large or too small. However, the relationship between group size and individual fitness has been difficult to establish for long-lived species where the number of groups studied is typically quite low. Here, we present evidence for optimal group size that maximizes female fitness in a population of geladas (Theropithecus gelada). Drawing on 14 years of demographic data, we found that females in small groups experienced the highest death rates, while females in mid-sized groups exhibited the highest reproductive performance. This group size effect on female reproductive performance was largely explained by variation in infant mortality (and, in particular, by infanticide from immigrant males) but not by variation in reproductive rates. Taken together, females in mid-sized groups are projected to attain optimal fitness due to conspecific infanticide and, potentially, predation. Our findings provide insight into how and why group size shapes fitness in long-lived species.

Male-Mediated Maturation in Wild Geladas.

The timing of female maturation in wild mammals is often constrained by ecological variables that relate to food acquisition. However, maturational timing in female mammals can also respond to social variables. Specifically, the arrival of novel males can accelerate maturation while the presence of related males can inhibit it. Despite studies on more than two dozen mammalian taxa in captivity, evidence for male-mediated maturation has not been systematically demonstrated in any wild population. Here, we report the first evidence of male-mediated maturation in a wild primate, the gelada (Theropithecus gelada). After the arrival of a new breeding male in the group (a male takeover), young females were three times more likely to mature. We then examined these takeover-associated maturations in more detail: some were earlier than expected (a presumptive "Vandenbergh effect," or male-accelerated maturation), some were at the expected age for the average female gelada, and some were later than expected (a presumptive "inbreeding avoidance delay," or father-induced reproductive suppression). An examination of fecal estrogens, which rise just before visible signs of maturation in this species, revealed that male takeovers induced a surge in estrogens for immature females of all ages-even females that did not mature. These are the first data to demonstrate that specific males are associated with the onset of maturation in a wild primate and to provide a possible mechanism for this change. These results suggest that all male-mediated maturation (whether accelerated, on-time, or delayed) may be governed by similar neuroendocrine processes.