Transcriptomic response to heat stress among ecologically divergent populations of redband trout

As ectothermic organisms have evolved to differing aquatic climates, the molecular basis of thermal adaptation is a key area of research. In this study, we tested for differential transcriptional response of ecologically divergent populations of redband trout (Oncorhynchus mykiss gairdneri) that have evolved in desert and montane climates. Each pure strain and their F1 cross were reared in a common garden environment and exposed over four weeks to diel water temperatures that were similar to those experienced in desert climates within the species' range. Gill tissues were collected from the three strains of fish (desert, montane, F1 crosses) at the peak of heat stress and tested for mRNA expression differences across the transcriptome with RNA-seq.

Strong differences in transcriptomic response to heat stress were observed across strains confirming that fish from desert environments have evolved diverse mechanisms to cope with stressful environments. As expected, a large number of total transcripts (12,814) were differentially expressed in the study (FDR ≤ 0.05) with 2310 transcripts in common for all three strains, but the desert strain had a larger number of unique differentially expressed transcripts (2875) than the montane (1982) or the F1 (2355) strain. Strongly differentiated genes (>4 fold change and FDR ≤ 0.05) were particularly abundant in the desert strain (824 unique contigs) relative to the other two strains (montane = 58; F1 = 192).

This study demonstrated patterns of acclimation (i.e., phenotypic plasticity) within strains and evolutionary adaptation among strains in numerous genes throughout the transcriptome. Key stress response genes such as molecular chaperones (i.e., heat shock proteins) had adaptive patterns of gene expression among strains, but also a much higher number of metabolic and cellular process genes were differentially expressed in the desert strain demonstrating these biological pathways are critical for thermal adaptation to warm aquatic climates. The results of this study further elucidate the molecular basis for thermal adaptation in aquatic ecosystems and extend the potential for identifying genes that may be critical for adaptation to changing climates.