Evolutionary and acclimation-induced variation in the heat-shock responses of congeneric marine snails (genus Tegula) from different thermal habitats: implications for limits of thermotolerance and biogeography

Abstract

Heat stress sufficient to cause cellular damage triggers the heat-shock response, the enhanced expression of a group of molecular chaperones called heat-shock proteins (hsps). We compared the heat-shock responses of four species of marine snails of the genus Tegula that occupy thermal niches differing in absolute temperature and range of temperature. We examined the effects of short-term heat stress and thermal acclimation on the synthesis of hsps of size classes 90, 77, 70 and 38 kDa by measuring incorporation of (35)S-labeled methionine and cysteine into newly synthesized proteins in gill tissue. Temperatures at which enhanced synthesis of hsps first occurred (T(on)), temperatures of maximal induction of hsp synthesis (T(peak)) and temperatures at which hsp synthesis was heat-inactivated (T(off)) were lowest in two low-intertidal to subtidal species from the temperate zone, T. brunnea and T. montereyi, intermediate in a mid- to low-intertidal species of the temperate zone, T. funebralis, and highest in a subtropical intertidal species from the Gulf of California, T. rugosa. Synthesis of hsps and other classes of protein by T. brunnea and T. montereyi was heat-inactivated at temperatures commonly encountered by T. funebralis during low tides on warm days. In turn, protein synthesis by T. funebralis was blocked at the upper temperatures of the habitat of T. rugosa. Acclimation of snails to 13 degrees C, 18 degrees C and 23 degrees C shifted T(on) and T(peak) for certain hsps, but did not affect T(off). The heat-shock responses of field-acclimatized snails were generally reduced in comparison with those of laboratory-acclimated snails. Overall, despite the occurrence of acclimatory plasticity in their heat-shock responses, genetically fixed differences in T(on), T(peak) and T(off) appear to exist that reflect the separate evolutionary histories of these species and may play important roles in setting their thermal tolerance limits and, thereby, their biogeographic distribution patterns.