Warming Accelerates the Onset of the Molecular Stress Response and Increases Mortality of Larval Atlantic Cod

Abstract

Synopsis Temperature profoundly affects ectotherm physiology. Although differential thermal responses influence fitness, thus driving population dynamics and species distributions, our understanding of the molecular architecture underlying these responses is limited, especially during the critical larval stage. Here, using RNA-sequencing of laboratory-reared Atlantic cod (Gadus morhua) larvae of wild origin, we find changes in gene expression in thousands of transcripts consistent with a severe cellular stress response at both ambient and projected (+2°C and +4°C) temperatures. In addition, specific responses to stress, heat, and hypoxia were commonly identified in gene ontology enrichment analyses and 33 of the 44 genes comprising the minimum stress proteome of all organisms were upregulated. Earlier onset of the stress response was evident at higher temperatures; concomitant increased growth and mortality suggests a reduction in fitness. Temporal differences in gene expression levels do not correspond to differences in growing degree days, suggesting negative physiological consequences of warming beyond accelerated development. Because gene expression is costly, we infer that the upregulation of thousands of transcripts in response to warming in larval cod might act as an energetic drain. We hypothesize that the energetically costly stress response, coupled with increased growth rate at warmer temperatures, leads to faster depletion of energy reserves and increased risk of mortality in larval cod. As sea surface temperatures continue to rise over the next century, reduced fitness of Atlantic cod larvae might lead to population declines in this ecologically and socioeconomically important species. Further, our findings expand our understanding of transcriptomic responses to temperature by ectothermic vertebrate larvae beyond the critical first-feeding stage, a time when organisms begin balancing the energetic demands of growth, foraging, development, and maintenance. Linking the molecular basis of a thermal response to key fitness-related traits is fundamentally important to predicting how global warming will affect ectotherms.