Early‐life adversity predicts performance and fitness in a wild social carnivore

Abstract

1. Studies on humans indicate that encountering multiple sources of adversity in childhood increases the risk of poor long-term health and premature death. Far less is known about cumulative effects of adversity during early life in wildlife.2. Focusing on the spotted hyena Crocuta crocuta, a social mammal with small litters, extensive maternal care, slow development and access to resources determined by social rank, we determined the contribution of ecological, maternal, social and demographic factors during early life on performance and fitness, and tested whether the impact of early-life adversity is cumulative.3. Using longitudinal data from 666 female hyenas in the Serengeti National Park, we determined the early growth rate, survival to adulthood, age at first reproduction (AFR), lifetime reproductive success (LRS) and longevity. We fitted multivariate models in which we tested the effects of environmental factors on these performance measures. We then constructed a cumulative adversity index and fitted models to test the effect of this index on each performance measure. Finally, the value of cumulative adversity models was tested by comparing them to multivariate and single-effect models in which the effect of each environmental factor was considered separately. 4. High maternal rank decreased the AFR of daughters. Singleton and dominant cubs had higher growth rate than subordinate cubs, and singletons also had a higher survival chance to adulthood than subordinates. Daughters of prime age mothers had a higher growth rate, longevity and LRS. Little and heavy rainfall decreased survival to adulthood. Increasing numbers of lactating female clan members decreased growth rate, survival to adulthood and LRS. Cumulative adversity negatively affected short-term performance and LRS. Multivariate models outperformed cumulative adversity and single-effect models for all measures except for AFR and longevity, for which single-effect models performed better. 5. Our results suggest that in some wildlife populations the combination of specific conditions in early life may matter more than the accumulation of adverse conditions as such.

Early life adversity has sex-dependent effects on survival across the lifespan in rhesus macaques

“…The survival effects of some forms of early life adversity were sex-dependent. Studies of early life adversity in long-lived animals have typically only been assessed in one sex, the non-dispersing sex (e.g., Gicquel et al, 2022;Patterson et al, 2022;Tung et al, 2016), but studies that have examined males and females produced mixed results.…”

“…The survival effects of some forms of early life adversity were sex-dependent. Studies of early life adversity in long-lived animals have typically only been assessed in one sex, the non-dispersing sex (e.g., Gicquel et al, 2022; Patterson et al, 2022; Tung et al, 2016), but studies that have examined males and females produced mixed results. While male red deer are more negatively impacted by maternal death than female deer (Andres et al, 2013), there do not appear to be any sex-based differences in susceptibility to the survival costs of cumulative early life adversity in gorillas (Morrison et al, 2023), though males and females might vary in their responses to specific types of adversity.…”

“…Some studies of early life adversity use broad, cumulative measures of adversity, while others focus on different forms of adversity separately (Gunnar, 2020; Smith & Pollak, 2020). Empirical evidence suggests that the accumulation of multiple adversities is a better predictor of adult outcomes than any particular form of adversity, but there is also evidence that specific forms of adversity lead to different outcomes (Gicquel et al, 2022; Gunnar, 2020; Tung et al, 2016). Here, we examine cumulative adversity measures and then examine individual forms of adversity separately.…”

“…Females who live longer have a longer reproductive span, and are able to produce more offspring. Long-term studies have shown that early life adversity is associated with reduced survival in adult female baboons and hyenas ( Crocuta crocuta ) (Gicquel et al, 2022; Lange et al, 2023; Strauss et al, 2020; Tung et al, 2016). In populations characterized by high mortality rates prior to reproductive maturity, LRS based on the total number of offspring reaching reproductive maturity is the best proxy for fitness (e.g., Alif et al 2022).…”

A future food boom rescues the negative effects of early-life adversity on adult lifespan in a small mammal

“…Among non-human animals, a harsh developmental environment can have similar far-reaching effects. Challenging ecological conditions during early life have been associated with higher adult parasite load in rabbits [6], inflammation in birds [7] and poor reproductive performance in hyenas [8]. Most consistently, both ecological and maternal challenges appear to independently and additively predict reduced adult lifespan across taxa [9][10][11][12].…”