Developmental environment and age shape macronutrient allocation to eggs and ejaculates

Abstract Environmental conditions during development can have lasting effects on reproductive investment, but the sex‐ and age‐specific nature of such effects remains poorly understood. Fluctuations in environmental stressors are now increasingly common under global change. Fluctuating and stable environmental stressors may differ in how they affect the allocation of energy resources to reproduction, thereby reshaping reproductive trade‐offs. In this study, we test the hypothesis that the fluctuation of an early‐life stressor affects sex‐ and age‐specific trade‐offs in reproductive allocation. To understand reproductive investment in responses to the salinity of the developmental environment, we used a split‐brood design to raise eastern mosquitofish ( Gambusia holbrooki ) from birth to maturity under three treatments: a freshwater control, a stable saline stress (10‰) and a fluctuating saline stress (0‰–20‰, mean 10‰). Upon maturity, we quantified the reproductive investment of females by measuring the protein, lipid and glycogen content of their eggs. For males, we measured the same macronutrients in their ejaculates when both young and old (following 12 weeks of reproductive activity) to investigate whether the juvenile environment affects the rate of reproductive senescence. The juvenile environment had distinct effects on reproductive allocation in both males and females. Females exposed to fluctuating salinity produced eggs with significantly lower protein content than females from stable or control environments. In males, there was a significant interaction between adult age and the juvenile environment that affected ejaculate investment. Old males that developed in a fluctuating environment produced ejaculates with significantly higher glycogen content than old males from the other treatments and all young males. Our results demonstrate that the fluctuation of an environmental stressor can alter reproductive investment in both sexes. The reduction in protein content of eggs suggests a direct energetic cost of environmental variability. In males, the age‐dependent shift towards a glycogen‐rich ejaculate under fluctuating environments is consistent with a terminal reproductive investment hypothesis, whereby individuals facing environmental uncertainty and senescence may increase the ejaculate quality of their final reproductive attempts. Our study highlights that considering the interplay between age and environmental variability is crucial to understanding the mechanisms of reproductive investment in a changing world. Read the free Plain Language Summary for this article on the Journal blog.