Developmental temperature drives distinct transcriptomic responses to acute temperatures and correlated differences in thermal tolerance

Abstract

Marine invertebrate populations exhibit varying capacities to withstand rising environmental temperatures, but the genetic basis of this differential tolerance remains an important area of investigation. Plasticity can be a valuable tool in the arsenal of an animal trying to maintain physiological function under rapidly changing conditions and can be an important contributor to thermal tolerance. In this work, we characterized the transcriptomic response to elevated developmental temperature, and subsequent acute exposure to two higher temperatures using the widespread and ecologically important copepod, Acartia tonsa. Using a split brood experimental design, we found that copepods that developed at 22{degrees}C had higher upper lethal temperatures compared to those reared at 18{degrees}C, demonstrating developmental plasticity in thermal tolerance. Transcriptomic analyses revealed that developmental temperature strongly influenced gene expression both at baseline and in response to acute thermal stress. Exposure to a moderate heat challenge (28{degrees}C) elicited divergent transcriptional responses between developmental treatments, suggesting developmental preconditioning, whereas exposure to extreme heat (33{degrees}C) triggered a more conserved stress response across groups. Weighted gene co-expression network analysis (WGCNA) identified gene modules associated with upper lethal temperature, highlighting stress response, cellular regulation, and metabolic pathways as key contributors to thermal tolerance. Together, our results reveal how developmental environments shape gene expression patterns and thermal phenotypes, providing insight into the molecular basis of plasticity and potential resilience to climate change.