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While strong maternal relationships have been linked with improved offspring survival in many mammals, maternal sociality appears to provide little protection against infanticidal males. Here, we evaluated whether maternal social integration predicts offspring survival to adulthood in geladas (Theropithecus gelada), a non-human primate that faces frequent alpha male takeovers coupled with high rates of infanticide. Mothers that formed stronger grooming relationships with their female and male groupmates showed higher offspring survival on average. However, when their infants experienced early-life takeovers and faced elevated infanticide risk, these survival advantages were weaker, delayed to juvenility and linked only to female–female grooming relationships. Thus, long-term social integration was not associated with reduced infanticide risk. Given this, we then examined whether females engaged in short-term social strategies that might provide more targeted protection against would-be male attackers. Following takeovers, females—particularly those with young, vulnerable infants—groomed males less frequently and prioritized deposed, protective males (i.e. their infants’ presumed fathers) over new, potentially infanticidal males. Taken together, these data suggest that gelada mothers: (i) form long-term social relationships that might improve net offspring survival and (ii) implement short-term social strategies that might protect their offspring in ways that long-term relationships cannot. 

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. 

ABSTRACT Over six decades of research on wild baboons and their close relatives (collectively, the African papionins) has uncovered substantial variation in their behavior and social organization. While most papionins form discrete social groups (single-level societies), a few others form small social units nested within larger aggregations (multi-level societies). To understand the social processes that shape this variation, a more systematic, comparative analysis of social structure is needed. Here, we constructed a database of behavioral and demographic records spanning 135 group-years across 13 long-term papionin field studies to (i) quantify variation in grooming network structure, and (ii) identify the factors (e.g., sex, kinship, and social status effects) that underlie these differences. We detected considerable variation in grooming network structure across the papionins, even within the classic single-level societies. The papionins could be best divided into three broad categories: single-levelcohesive, single-levelcliquish, andmulti-level. The cohesive single-level societies formed networks that were dense, moderately kin-biased, and weakly rank-structured, while the cliquish single-level societies formed networks that were relatively modular, highly kin-biased, and more strongly rank-structured. As expected, multi-level networks were highly modular and shaped by females’ ties to specific dominant males but varied in their kin biases. Taken together, these data suggest that: (i) discrete typologies obscure variation in social structure; and (ii) similarities in social structure are sometimes, but not always, shaped by similar social processes. SIGNIFICANCE STATEMENTDo all primate groups fit the same social mold? While factors like kinship and dominance shape the social lives of many of our close relatives, it remains unclear how their effects differ across species. Using a new database representing decades of field research, we found that baboons and their close relatives fell into one of three general patterns: one in which groups were cohesive and only somewhat nepotistic (i.e., kin- and rank-biased), another in which groups were more cliquish and nepotistic, and a final pattern in which groups were divided into clusters centered on dominant males. Distinct primate societies may thus reflect differences in the strength of females’ social biases towards kin and the degree of males’ social influence. 

Abstract Female social relationships are often shaped by the distribution of dietary resources. Socioecological models predict that females should form strict linear dominance hierarchies when resources are clumped and exhibit more egalitarian social structures when resources are evenly distributed. While many frugivores and omnivores indeed exhibit dominance hierarchies accompanied by differential resource access, many folivores deviate from the expected pattern and display dominance hierarchies despite evenly distributed resources. Among these outliers, geladas (Theropithecus gelada) present a conspicuous puzzle; females exhibit aggressive competition and strict dominance hierarchies despite feeding primarily on non-monopolizable grasses. However, these grasses become scarce in the dry season and geladas supplement their diet with underground storage organs that require relatively extensive energy to extract. We tested whether female dominance hierarchies provide differential access to underground storage organs by assessing how rank, season, and feeding context affect aggression in geladas under long-term study in the Simien Mountains National Park, Ethiopia. We found that the likelihood of receiving aggression was highest when feeding belowground and that the inverse relationship between rank and aggression was the most extreme while feeding belowground in the dry season. These results suggest that aggression in geladas revolves around belowground foods, which may mean that underground storage organs are an energetically central dietary component (despite being consumed less frequently than grasses), or that even “fallback” foods can influence feeding competition and social relationships. Further work should assess whether aggression in this context is directly associated with high-ranking usurpation of belowground foods from lower-ranking females following extraction. 

Abstract 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. 

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.