Cardiac performance and heat shock response variation related to shell colour morphs in the mudflat snail Batillaria attramentaria

Abstract

ABSTRACT Gastropods exhibit remarkable variation in shell colour within and among populations, but the function of shell colour is often not clear. In the present study, body temperature in the field and physiological and transcriptomic responses to thermal stress were investigated in different shell colour morphs of the mudflat snail Batillaria attramentaria. Using biomimetic models, we found that the body temperature of snails with a dark unbanded shell (D-type morph) was slightly higher than that of snails with a white line on the upper side of each whorl (UL-type morph) when exposed to sunlight. Despite no differences in upper lethal temperature among shell colour morphs, their Arrhenius breakpoint temperature (ABT) for cardiac thermal performance differed significantly, and the ABT of snails with the D-type morph was higher than that of snails with the UL-type morph. Transcriptomic analysis showed that D-type snails exhibit higher levels of four heat shock proteins (HSPs) than UL-type snails at control temperature. The unfolded protein response was activated in UL-type snails but not in D-type snails under moderate thermal stress. And 11 HSPs showed an increase in UL-type snails in contrast to 1 HSP in D-type snails, suggesting a ‘preparative defence’ strategy of the heat shock response in D-type snails under moderate thermal stress. When exposed to sublethal temperature, eight molecular chaperones were uniquely upregulated in D-type snails, suggesting these genes may allow D-type snails to improve their cardiac thermal tolerance. Our results suggest that the preparative defence strategies and higher ABT for cardiac thermal performance may allow the dark shell snails to adapt to rapid and stronger thermal stress in the field.