Land snails are subject to daily and seasonal variations in temperature and in water availability and depend on a range of behavioral and physiological adaptations for coping with problems of maintaining water, ionic, and thermal balance. Heat shock proteins (HSPs) are a multigene family of proteins whose expression is induced by a variety of stress agents. We used experimental desiccation to test whether adaptation to different habitats affects HSP expression in two closely related Sphincterochila snail species, a desiccation-resistant, desert species Sphincterochila zonata, and a Mediterranean-type, desiccation-sensitive species Sphincterochila cariosa. We examined the HSP response in the foot, hepatopancreas, and kidney tissues of snails exposed to normothermic desiccation. Our findings show variations in the HSP response in both timing and magnitude between the two species. The levels of endogenous Hsp72 in S. cariosa were higher in all the examined tissues, and the induction of Hsp72, Hsp74, and Hsp90 developed earlier than in S. zonata. In contrary, the induction of sHSPs (Hsp25 and Hsp30) was more pronounced in S. zonata compared to S. cariosa. Our results suggest that land snails use HSPs as part of their survival strategy during desiccation and as important components of the aestivation mechanism in the transition from activity to dormancy. Our study underscores the distinct strategy of HSP expression in response to desiccation, namely the delayed induction of Hsp70 and Hsp90 together with enhanced induction of sHSPs in the desert-dwelling species, and suggests that evolution in harsh environments will result in selection for reduced Hsp70 expression.
With 4 figures in the text)Land snails are subject to desiccating conditions in their terrestrial habitat. Our previous studies have revealed significant difercnces in resistance to desiccation among closely related species and among genera that share a similar life style. suggesting that the distribution pattern is correlated with the abiotic regime in its specific habitat. Our present study extends the scope of comparison to the intraspecific level, by examining the resistance to desiccation in five populations of Xeropicm rv.s/u/i.s. a Mediterranean-dwelling species that ranges from the 1000 mm to the 200 mm isohyet.The resistance to desiccation varied among populations in correlation with the specific habitat of each population and with the north-to-south and the west-to-east climatic gradients. Furthermore. in one case it exceeded the resistance of other. desert-dwelling species (Trochoideu ,sin~u/uiu. Spkincrc~rochi/u zonuiu). We suggest that. in spite of its physiological capacity to invade deserts, X. twsrulis is prevented from doing so because it is an annual, semelparous species. The Negev Desert is an unpredictable environment. susceptible to year-to-year fluctuations to such an extent that one rainless year would wipe out all its populations.
SUMMARYLand snails are subject to daily and seasonal variations in temperature and in water availability, and have evolved annual cycles of activity and aestivation as part of their survival strategy. We tested in the field whether adaptation to different habitats affects the endogenous levels of heat shock proteins (HSPs) in two closely related Sphincterochila snail species, a desiccation-resistant desert species, Sphincterochila zonata, and a Mediterranean-type, desiccation-sensitive species, S. cariosa. We examined HSP levels in various tissues of snails during aestivation and after resumption of activity. Our study shows that, during aestivation, S. cariosa had higher standing stocks of Hsp70 in the foot and the hepatopancreas, and of small HSPs (sHSPs) in all the examined tissues, whereas S. zonata had higher stocks of Hsp70 in the kidney and of Hsp90 in the kidney and in the hepatopancreas. Arousal induced a general upregulation of HSPs, except for Hsp90, the expression of which in the foot was higher during aestivation. We suggest that the stress protein machinery is upregulated during arousal in anticipation of possible oxidative stress ensuing from the accelerating metabolic rate and the exit from the deep hypometabolic state. Our findings support the concept that, in land snails, aestivation and activity represent two distinct physiological states, and suggest that land snails use HSPs as important components of the aestivation mechanism, and as part of their survival strategy during and after arousal. Our study also indicates that adaptation to different habitats results in the development of distinct strategies of HSP expression with likely consequences for the ecology and distribution of land snails. Supplementary material available online at
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.
We have examined the resistance to desiccation among rock-dwelling land snails of various phylogenetic groups: Cristataria genezarethana (Clausiliidae), Rupestrella rhodia (Chondrinidae) and Levantina caesareana (Helicidae), all from the same location in Israel. L. caesareana was the most resistant and R. rhodia the least resistant to desiccation and C. genezarethana was of intermediate resistance. Differences in the rates of water loss during desiccation were determined mainly by rate of water loss during the first 2 days of desiccation. The high rates of water loss in rock-dwelling species exceed those of other snails in the Mediterranean habitat of Israel. However, snails collected in the field at the end of aestivation were in only a mild state of dehydration, suggesting that the rocky habitat protects its occupants against desiccation. We also suggest that among the rock-dwelling species, the protective role of the rock is more important in the more evolutionarily primitive genera (the chondrinid Rupestrella and the clausiliid Cristataria) and that physiological capacities are more effective in the more highly evolved helicid Levantina.
Resistance to desiccation was examined in six populations of the Israeli bush‐dwelling snail Trochoidea simulata, a desert species distributed mainly between the 100–200 mm isohyets. The present study revealed significant intraspecific differences in resistance to desiccation which are correlated with habitat and climatic gradients within the distribution range of the species. Populations from more arid sites were more resistant to desiccation and heat exposure than those from more mesic areas. However, the population from the Rift Valley (an extremely arid region) was surprisingly poorly resistant. Rates of population water loss under the controlled experimental conditions in the laboratory generally matched the calculated water losses during natural summer aestivation.
Theba pisana is a bush-dwelling snail with a circum-Mediterranean distribution. In Israel it is limited to a narrow coastal strip, along which there is a north-tosouth gradient in mean annual rainfall (700-300 mm per year). In this study we found significant intraspecific differences among populations of T. pisana in resistance to desiccation along this gradient, and in a population from Greece, which may be grossly correlated with the climatic gradient. The Greek population was the least resistant to desiccation with an extremely high rate of water loss. The differences in total mass loss were mainly determined by the rate of water loss during the first 4 days of desiccation. A general phenomenon during desiccation was the close regulation of the soft body water content at the expense of the extra-pallial fluid compartment.
Polmunate land snails are subject to stress conditions in their terrestrial habitat, and depend on a range of behavioural, physiological and biochemical adaptations for coping with problems of maintaining water, ionic and thermal balance. The involvement of the heat shock protein (HSP) machinery in land snails was demonstrated following short-term experimental aestivation and heat stress, suggesting that land snails use HSPs as part of their survival strategy. As climatic variation was found to be associated with HSP expression, we tested whether adaptation of land snails to different habitats affects HSP expression in two closely related Sphincterochila snail species, a desert species Sphincterochila zonata and a Mediterranean-type species Sphincterochila cariosa. Our study suggests that Sphincterochila species use HSPs as part of their survival strategy following desiccation and heat stress, and as part of the natural annual cycle of activity and aestivation. Our studies also indicate that adaptation to different habitats results in the development of distinct strategies of HSP expression in response to stress, namely the reduced expression of HSPs in the desert-inhabiting species. We suggest that these different strategies reflect the difference in heat and aridity encountered in the natural habitats, and that the desert species S. zonata relies on mechanisms and adaptations other than HSP induction thus avoiding the fitness consequences of continuous HSP upregulation.
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