Natural Variation in Resistance to Desiccation and Heat Shock Protein Expression in the Land SnailTheba pisanaalong a Climatic Gradient

Abstract

Land snails frequently encounter desiccating conditions, and their survival depends on a suite of morphological, physiological, and molecular adaptations to the specific microhabitat. Strategies of survival can be determined by integrating information from various levels of biological organization. In this study, we used a combination of physiological parameters related to water economy and molecular factors (stress protein expression) to investigate the strategies of survival adopted by seven populations of the Mediterranean-type land snail Theba pisana from different habitats. We analyzed water compartmentalization during aestivation and used experimental desiccation to compare desiccation resistance. We also measured the endogenous levels of heat shock proteins (HSPs) Hsp72, Hsp74, and Hsp90 under nonstress conditions and analyzed the HSP response to desiccation in two populations that differed mostly in their resistance to desiccation. We revealed significant intraspecific differences in resistance to desiccation that seem to be determined by the speed of recruitment of the water-preserving mechanisms. The ability to cope with desiccating conditions was correlated with habitat temperature but not with the rainfall gradient, implying that in the coastal region, temperature is likely to have a major impact on desiccation resistance rather than precipitation. Also, higher desiccation resistance was correlated with higher constitutive levels of Hsp74 in the foot tissue. HSPs were upregulated during desiccation, but the response was delayed and was milder in the most resistant population compared to the most susceptible one. Our study suggests that T. pisana populations from warmer habitats were more resistant to desiccation and developed distinct strategies of HSP expression for survival, namely, the maintenance of high constitutive levels of Hsp70 together with a delayed and limited response to stress.

Geographic variation in thermal tolerance and strategies of heat shock protein expression in the land snail Theba pisana in relation to genetic structure

“…Thus, our study is consistent with previous comparative studies of ectothermic species from different habitats demonstrating a direct relationship between habitat temperature and thermotolerance (Sorte and Hofmann 2005;Stillman and Somero 2000). Importantly, our findings for thermal tolerance limits are consistent with the general hierarchy of desiccation resistance, where the populations of Akko, Achziv, and Kiryat Yam were the most desiccation-resistant, the populations of Ashkelon and Or Akiva were the least resistant, and the Ashdod population having an intermediate response to desiccation stress (Mizrahi et al 2015).…”

“…In our previous study, we found that the ability of T. pisana snails to cope with desiccating conditions was correlated with habitat temperature but not with the rainfall gradient (Mizrahi et al 2015). Our present study in T. pisana demonstrates also a positive correlation between habitat temperature and thermal tolerance, suggesting that temperature plays important roles in determining the ability of T. pisana snails to cope with environmental stress conditions of both heat and aridity.…”

“…In Israel, its distribution is limited to a narrow sandy coastal strip along which there is a north-to-south gradient in mean annual rainfall (700 to 300 mm per year) (Jaffe 1988). Recently, we tested populations of T. pisana along a climatic gradient in rainfall and found significant intraspecific differences in resistance to desiccation (Mizrahi et al 2015). Interestingly, in contradiction to the general assumption that the more arid the habitat, the more adapted to desiccation conditions is the population, the ability of T. pisana snails to cope with desiccating conditions was correlated with habitat temperature but not with the rainfall gradient.…”

“…For testing whether genetic parameters of the studied populations significantly reflect molecular or physiological differences, we conducted a correlation analysis between two genetic parameters, mean diversity (within population differences) and mean divergence from consensus sequence (among population differences) and either HSP levels in field-collected or acclimated snails; habitat temperature; thermal tolerance (LT 50 ); or desiccation tolerance (the percentage of total mass loss after 3 weeks of desiccation, adapted from our previous study in T. pisana (Mizrahi et al 2015)). …”

“…Similarly, in our recent study of T. pisana, we found higher levels of Hsp74 in the foot tissue of populations inhabiting warmer habitats together with a delayed and milder response of HSPs to desiccation stress in the warm-adapted, resistant populations compared to the more susceptible populations. This suggests that T. pisana populations from warmer habitats developed distinct strategies of HSP expression for survival (Mizrahi et al 2015).…”