Rhesus macaques compensate for reproductive delay following ecological adversity early in life

Adversity early in life can shape the reproductive potential of
individuals through negative effects on health and life span. However,
long-lived populations with multiple reproductive events may present
alternative life history strategies to optimize reproductive schedules and
compensate for shorter life spans. Here, we quantify the effects of major
hurricanes and density dependence as sources of early-life ecological
adversity on Cayo Santiago rhesus macaque female reproduction and
decompose their effects onto the mean age-specific fertility, reproductive
pace, and lifetime reproductive success (LRS). Females experiencing major
hurricanes exhibit a delayed reproductive debut but maintain the pace of
reproduction past debut and show a higher mean fertility during prime
reproductive ages, relative to unaffected females. Increasing density at
birth is associated to a decrease in mean fertility and reproductive pace,
but such association is absent at intermediate densities. When combined,
our study reveals that hurricanes early in life predict a delay-overshoot
pattern in mean age-specific fertility that supports the maintenance of
LRS. In contrast to predictive adaptive response models of accelerated
reproduction, this long-lived population presents a novel reproductive
strategy where females who experience major natural disasters early in
life ultimately overcome their initial reproductive penalty with no major
negative fitness outcomes. Density presents a more complex relation with
reproduction that suggests females experiencing a population regulated at
intermediate densities early in life will escape density dependence and
show optimized reproductive schedules. Our results support hypotheses
about life history trade-offs in which adversity-affected females ensure
their future reproductive potential by allocating more energy to growth or
maintenance processes at younger adult ages.

生命早期的逆境可通过对健康与寿命的负面影响，塑造个体的繁殖潜能。然而，具备多次繁殖事件的长寿种群，或许存在可优化繁殖时序、弥补较短寿命的替代生活史策略。本研究量化了严重飓风与密度制约作为早期生态逆境来源，对圣地亚哥岛（Cayo Santiago）恒河猴雌性繁殖的影响，并将其效应分解至特定年龄生育率均值、繁殖节奏与终身繁殖成功率（Lifetime Reproductive Success, LRS）三个维度。相较于未受影响的雌性个体，经历过严重飓风的雌性表现出繁殖起始延迟，但在首次繁殖后仍维持稳定的繁殖节奏，且在核心繁殖年龄段的平均生育率更高。出生时种群密度升高与平均生育率及繁殖节奏下降存在关联，但该关联在中等密度条件下并不存在。综合来看，本研究揭示：生命早期经历的飓风会导致特定年龄生育率呈现“延迟-超调”模式，该模式有助于维持终身繁殖成功率。与加速繁殖的预测性适应反应模型不同，该长寿种群展现出一种全新的繁殖策略：生命早期经历重大自然灾害的雌性，最终可克服初始的繁殖劣势，且未出现显著的适合度负面后果。种群密度与繁殖的关联更为复杂，这表明生命早期经历中等密度调控种群的雌性，可摆脱密度制约效应，并展现出优化的繁殖时序。本研究结果支持生活史权衡相关假说，即受逆境影响的雌性会在年轻成年阶段将更多能量分配至生长或维持过程，以此保障未来的繁殖潜能。