Adverse ecological and social conditions during early life are known to influence development, with rippling effects that may explain variation in adult health and fitness. The adaptive function of such developmental plasticity, however, remains relatively untested in long‐lived animals, resulting in much debate over which evolutionary models are most applicable. Furthermore, despite the promise of clinical interventions that might alleviate the health consequences of early‐life adversity, research on the proximate mechanisms governing phenotypic responses to adversity have been largely limited to studies on glucocorticoids. Here, we synthesize the current state of research on developmental plasticity, discussing both ultimate and proximate mechanisms. First, we evaluate the utility of adaptive models proposed to explain developmental responses to early‐life adversity, particularly for long‐lived mammals such as humans. In doing so, we highlight how parent‐offspring conflict complicates our understanding of whether mothers or offspring benefit from these responses. Second, we discuss the role of glucocorticoids and a second physiological system—the gut microbiome—that has emerged as an additional, clinically relevant mechanism by which early‐life adversity can influence development. Finally, we suggest ways in which nonhuman primates can serve as models to study the effects of early‐life adversity, both from evolutionary and clinical perspectives.
Aggression rarely escalates to physical conflict because doing so puts individuals at risk of injury. Escalation only pays off when the potential benefits outweigh the potential costs, that is, when resources critical to fitness are at stake. Here, we investigated the occurrence of injury in 2 Asian colobine species: Nepal gray langurs (Semnopithecus schistaceus) and Phayre’s leaf monkeys (Trachypithecus phayrei crepusculus). In both species, younger individuals are higher-ranking and might have greater incentive to fight. However, Nepal gray langurs have a strict breeding season, which may magnify male mating competition, and Phayre’s leaf monkeys, unlike Nepal gray langurs, have female-biased dispersal, which may increase female injury risk during subadulthood. Using long-term data on observed injuries (Nepal gray langurs: n = 208; Phayre’s leaf monkeys: n = 225), we modeled the monthly occurrence of injury (Y/N) and found that males received more injuries than females in both species. Also, subadults generally experienced frequent injury, as young individuals likely face challenges when competing for group membership and/or establishing rank. In Nepal gray langurs, males received 3 times more injuries during the mating season, suggesting strong competition for mates during this period, and females experienced more injuries before conception, suggesting competition to meet the nutritional requirements for reproduction. Unexpectedly, females in smaller groups received more injuries in Nepal gray langurs. Overall, these results indicate that injuries are most likely when fighting may aid in establishing group membership, achieving high rank, and reproducing. Future research should investigate the influence of injuries on fitness outcomes.
In humans, a controversial hypothesis suggests that father absence promotes early puberty in daughters. Data from rodents confirm females accelerate maturation with exposure to novel males (“Vandenbergh effect”) and delay it with exposure to male relatives. Here, we report the first case of male-mediated maturation in a wild primate, geladas (Theropithecus gelada). Females were more likely to mature after a change in the reproductive male: some matured earlier than expected (Vandenbergh effect) and some later (due to father presence). Novel males stimulated a surge in estrogens for all immature females - even females too young to mature. Although male-mediated puberty accelerated first births, the effect was modest, suggesting that alternative scenarios, such as co-evolution with the Bruce effect (male-mediated fetal loss) may explain this phenomenon.One Sentence SummaryNovel males induce an estrogen surge, male-mediated puberty, and a head-start on reproduction for immature female geladas.
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.
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