Data from: Prenatal stress effects in a wild, long-lived primate: predictive adaptive responses in an unpredictable environment

Prenatal maternal stress affects offspring phenotype in numerous species including humans, but it is debated whether these effects are evolutionarily adaptive. Relating stress to adverse conditions, current explanations invoke either short-term developmental constraints on offspring phenotype resulting in decelerated growth to avoid starvation, or long-term predictive adaptive responses (PARs) resulting in accelerated growth and reproduction in response to reduced life expectancies. Two PAR-subtypes were proposed, acting either on predicted internal somatic states or predicted external environmental conditions, but since both affect phenotypes similarly, they are largely indistinguishable. Only external, but not internal PARs though, rely on high environmental stability particularly in long-lived species. We report on a crucial test case in a wild long-lived mammal, the Assamese macaque (Macaca assamensis) that evolved and lives in an unpredictable environment where external PARs are probably not advantageous. We quantified food availability, growth, motor skills, maternal caretaking style, and maternal physiological stress from faecal glucocorticoid measures. Prenatal maternal stress was negatively correlated to prenatal food availability and led to accelerated offspring growth accompanied by decelerated motor skill acquisition and reduced immune function. These results support the “internal PAR”-theory which stresses the role of stable adverse internal somatic states rather than stable external environments.产前母体应激可影响包括人类在内的诸多物种的后代表型（phenotype），但其效应是否具有进化适应性仍存争议。当前将应激与不良环境条件相关联的主流解释主要有两类：一类认为应激会对后代表型造成短期发育限制，通过减缓生长速率以规避饥饿风险；另一类则提出长期预测性适应性反应（Predictive Adaptive Responses, PARs）理论，认为当个体预期寿命缩短时，后代会通过加快生长与繁殖来应对。现有研究提出了两类PAR亚型：一类针对预测得到的机体内在生理状态，另一类针对预测得到的外部环境条件；但由于二者对表型的影响模式高度相似，因此几乎无法区分。不过，仅针对外部环境的PAR亚型依赖于高度稳定的环境条件，这一点在长寿命物种中尤为关键。本研究以野生长寿命哺乳动物——阿萨姆猕猴（Macaca assamensis）为关键实验模型，该物种演化并栖息于不可预测的环境中，此时针对外部环境的PAR亚型大概率不具备适应性优势。我们通过粪便糖皮质激素（faecal glucocorticoid）检测手段，量化了食物可获得性、个体生长发育、运动技能、母性抚育模式以及母体生理应激水平。研究结果显示，产前母体应激与产前食物可获得性呈负相关，且会导致后代生长速度加快，同时伴随运动技能习得减缓以及免疫功能下降。上述结果支持“内在PAR理论”，该理论强调不良内在生理状态的稳定作用，而非稳定的外部环境条件。