RNA‐seq reveals regional differences in transcriptome response to heat stress in the marine snail Chlorostoma funebralis

Abstract

To investigate the role of gene expression in adaptation of marine ectotherms to different temperatures, we examined the transcriptome-wide thermal stress response in geographically separated populations of the intertidal snail Chlorostoma funebralis. Snails from two southern (heat tolerant) and two northern (heat sensitive) populations were acclimated to a common thermal environment, exposed to an environmentally relevant thermal stress and analysed using RNA-seq. Pooling across all populations revealed 306 genes with differential expression between control and heat-stressed samples, including 163 significantly upregulated and 143 significantly downregulated genes. When considered separately, regional differences in response were widely apparent. Heat shock proteins (Hsps) were upregulated in both regions, but the magnitude of response was significantly greater in northern populations for most Hsp70s, while the southern populations showed greater upregulation for approximately half of the Hsp40s. Of 177 stress-responsive genes in northern populations, 55 responded to heat stress only in northern populations. Several molecular chaperones and antioxidant genes that were not differentially expressed in southern populations showed higher expression under control conditions compared with northern populations. This suggests that evolution of elevated expression of these genes under benign conditions preadapts the southern populations to frequent heat stress and contributes to their higher thermal tolerance. These results indicate that evolution has resulted in different transcriptome responses across populations, including upregulation of genes in response to stress and preadaptation of genes in anticipation of stress (based on evolutionary history of frequent heat exposure). The relative importance of the two mechanisms differs among gene families and among populations.

Untangling the roles of microclimate, behaviour and physiological polymorphism in governing vulnerability of intertidal snails to heat stress

“…Physiological responses of species to thermal stress are also highly variable among populations [38,39]. Whereas relatively few studies have measured intra-population physiological polymorphisms in intertidal species, the few studies that exist also suggest high inter-individual variability in physiological responses to thermal stress [40 -42].…”

Thermal evolution offsets the elevated toxicity of a contaminant under warming: A resurrection study in Daphnia magna

“…This can be expected because when a population evolves tolerance to a certain stressor that environmental condition is no longer experienced as a stressor (Vam Straalen, 2003). With regard to warming, the acquisition of genetic adaptation to higher temperatures has been demonstrated in several taxa and has been linked to changes in gene expressions (e.g., Garvin, Thorgaard, & Narum, 2015; Gleason & Burton, 2015; Narum, Campbell, Meyer, Miller, & Hardy, 2013; Porcelli, Butlin, Gaston, Joly, & Snook, 2015; for the study species: Jansen et al., 2017; Yampolsky et al., 2014). Thermal evolution is expected to reduce the energetic costs of dealing with warming, thus leaving more energy to deal with stressors such as toxicants, thereby potentially offsetting the synergism between the toxicant and warming.…”

Comparative physiological, biochemical, and molecular thermal stress response profiles for two Unionid freshwater mussel species

“…These factors play an important role in developing acute response models related to gene expression patterns (Wu, 1995;Morimoto, 1998). Specifically, thermally tolerant species may possess higher basal transcript levels and a less pronounced induction profile of heat shock proteins compared with thermally sensitive species (Gleason and Burton, 2015). This could allow thermally tolerant species to withstand a strong thermal insult because of the greater standing pool of heat shock proteins resulting from higher transcript levels (Bedulina et al, 2013;Barshis et al, 2013;Fangue et al, 2006;Luo et al, 2014).…”