Temporal compression of gonadal growth preserves reproductive timing and soma-to-germline scaling under stress

Abstract

How organisms maintain timely reproduction under stress is central to life history plasticity and remains an unmet challenge in biomedicine. Life history theory predicts that organisms preserve fitness across environments by reallocating resources between somatic and reproductive growth, yet direct tests of this prediction have been limited by the lack of longitudinal life history data. Here, using Caenorhabditis elegans, we combine longitudinal video microscopy of gonadal growth, mathematical modelling, and genetic perturbations to show that reproductive timing is preserved through temporally dynamic control of reproductive organ growth. Under stress, the onset of gonad growth was delayed early in development but later accelerated relative to somatic growth, thereby preserving reproductive-to-somatic size ratios at adulthood. Modelling suggests this delay-and-acceleration strategy to minimize the time to maturity under stress. Consistently, disrupting compensatory gonadal growth acceleration, either through genetic perturbation of the JNK/p38 stress signalling pathway or by uncoupling of reproductive and somatic development, reduced gonad size and delayed reproduction. Together, our results show that reproductive robustness under stress arises from dynamic regulation of reproductive growth rather than a fixed shift in resource allocation, defining a previously unrecognized mechanistic principle for environmentally plastic sexual maturation.