An integrated, multi-level analysis of thermal effects on intertidal molluscs for understanding species distribution patterns

Elucidating the physiological mechanisms that underlie thermal stress and discovering how species differ in capacities for phenotypic acclimatization and evolutionary adaptation to this stress is critical for understanding current latitudinal and vertical distribution patterns of species and for predicting their future state in a warming world. Such mechanistic analyses require careful choice of study systems (species and temperature-sensitive traits) and design of laboratory experiments that reflect the complexities of in situ conditions. Here, we critically review a wide range of studies of intertidal molluscs that provide mechanistic accounts of thermal effects across all levels of biological organization - behavioural, organismal, organ level, cellular, molecular, and genomic - and show how temperature-sensitive traits govern distribution patterns and capacities for coping with thermal stress. Comparisons of congeners from different thermal habitats are especially effective means for identifying adaptive variation. We employ these mechanistic analyses to illustrate how species differ in the severity of threats posed by rising temperature. Counterintuitively, we show that some of the most heat-tolerant species may be most threatened by increases in temperatures because of their small thermal safety margins and minimal abilities to acclimatize to higher temperatures. We discuss recent molecular biological and genomic studies that provide critical foundations for understanding the types of evolutionary changes in protein structure, RNA secondary structure, genome content, and gene expression capacities that underlie adaptation to temperature. Duplication of stress-related genes, as found in heat-tolerant molluscs, may provide enhanced capacity for coping with higher temperatures. We propose that the anatomical, behavioural, physiological, and genomic diversity found among intertidal molluscs, which commonly are of critical importance and high abundance in these ecosystems, makes this group of animals a highly appropriate study system for addressing questions about the mechanistic determinants of current and future distribution patterns of intertidal organisms.

Automated summary

Understanding the physiological mechanisms of thermal stress and species differences in adaptation and evolution to this stress is crucial for predicting current and future distribution patterns of species in a warming world. Studies on intertidal molluscs provide mechanistic explanations of thermal effects across different levels of biological organization and highlight the importance of temperature-sensitive traits in governing distribution patterns and coping capacities. Comparisons of congeners from different thermal habitats can effectively identify adaptive variations and illustrate the severity of threats posed by rising temperatures.