Comparative transcriptomics across populations offers new insights into the evolution of thermal resistance in marine snails

Abstract

Adaptation to thermal conditions in intertidal ectotherms involves tolerating and surviving frequent and often extreme variations in environmental temperatures. Modulation of gene expression plays an important role in the adaptive evolution of thermal tolerance. To understand such patterns, we investigated the thermal tolerance among three Asian populations (from Xiamen, Hong Kong, and Singapore) of the marine littorinid snail Echinolittorina malaccana and examined gene expression profiles in these populations before, during, and after heat stress using an Illumina RNA-sequencing platform. Analysis of transcriptomic changes between different conditions revealed that a proportion of the differentially expressed genes showed similar expression profiles across all three populations, including many classic molecular chaperones such as HSP70 and HSP90 that may constitute the core of the thermal stress response machinery in marine snails. Meanwhile, population-specific transcriptomic responses to heat stress were also detected. A few genes in particular showed more analogous expression profiles in the more thermally tolerant Hong Kong and Singapore populations, and these genes are likely to contribute, at least in part, to the enhanced thermal tolerance of these populations. We argue that repression of a subset of metabolic genes including several cytochrome P450 gene family members, to minimize energy expenditure and control reactive oxygen species turnover, may underpin the enhanced thermal resistance in these two populations. As such, these findings offer new insights into how marine snails cope with thermal stress and their potential evolutionary trajectory toward adapting to a warming climate.