Phenotypic diversity, population structure and stress protein-based capacitoring in populations of Xeropicta derbentina, a heat-tolerant land snail species

Abstract

The shell colour of many pulmonate land snail species is highly diverse. Besides a genetic basis, environmentally triggered epigenetic mechanisms including stress proteins as evolutionary capacitors are thought to influence such phenotypic diversity. In this study, we investigated the relationship of stress protein (Hsp70) levels with temperature stress tolerance, population structure and phenotypic diversity within and among different populations of a xerophilic Mediterranean snail species (Xeropicta derbentina). Hsp70 levels varied considerably among populations, and were significantly associated with shell colour diversity: individuals in populations exhibiting low diversity expressed higher Hsp70 levels both constitutively and under heat stress than those of phenotypically diverse populations. In contrast, population structure (cytochrome c oxidase subunit I gene) did not correlate with phenotypic diversity. However, genetic parameters (both within and among population differences) were able to explain variation in Hsp70 induction at elevated but nonpathologic temperatures. Our observation that (1) population structure had a high explanatory potential for Hsp70 induction and that (2) Hsp70 levels, in turn, correlated with phenotypic diversity while (3) population structure and phenotypic diversity failed to correlate provides empirical evidence for Hsp70 to act as a mediator between genotypic variation and phenotype and thus for chaperone-driven evolutionary capacitance in natural populations.

Snails in the sun: Strategies of terrestrial gastropods to cope with hot and dry conditions

“…Furthermore, the capacity to induce Hsp70 depends on the physiological status of an individual, as warm‐adapted Theba pisana showed maximal hsp70 ‐mRNA induction at higher temperatures and also higher upper thermal limits of hsp mRNA synthesis (Mizrahi, Goldenberg, Heller, & Arad, ). Thus, different species or populations seem to differ in their strategies to cope with heat stress at the molecular level, a finding that has also been confirmed by Di Lellis et al (). Concerning temperature‐correlated seasonal variability of Hsp70 levels in Xeropicta derbentina in the field, Dieterich et al () found the Hsp70 level to be positively correlated with shell surface temperature in April, June, and August only, while a negative correlation was observed in October.…”

“…Thus, even within a species, apparent local ecological peculiarities seem to result in microevolutionary consequences regarding snails' molecular adaptations to heat. Interestingly, these interpopulation differences in the constitutive and maximal Hsp70 levels correlated with the variation in the shell coloration pattern in these Xeropicta populations (Di Lellis et al, ) which, in turn, may have consequences for the average thermal capacity of individuals from these populations (if intensely pigmented shells actually lead to higher body temperature). Furthermore, this observation strengthened the concept of Hsps as epigenetic capacitors of phenotypic variation (Di Lellis et al, ) as variation in coloration correlated inversely with the Hsp70 level in a number of Xeropicta derbentina populations from southern France: There was little color variation in populations exhibiting high Hsp70 levels and greater color variation in populations with low Hsp70 levels.…”

“…Interestingly, these interpopulation differences in the constitutive and maximal Hsp70 levels correlated with the variation in the shell coloration pattern in these Xeropicta populations (Di Lellis et al, ) which, in turn, may have consequences for the average thermal capacity of individuals from these populations (if intensely pigmented shells actually lead to higher body temperature). Furthermore, this observation strengthened the concept of Hsps as epigenetic capacitors of phenotypic variation (Di Lellis et al, ) as variation in coloration correlated inversely with the Hsp70 level in a number of Xeropicta derbentina populations from southern France: There was little color variation in populations exhibiting high Hsp70 levels and greater color variation in populations with low Hsp70 levels. The capacitoring concept has originally been suggested in nonmolluskan species by Rutherford and Lindquist (), Roberts and Feder (), Queitsch, Sangster, and Lindquist () and Rutherford (), primarily for Hsp90 and traits other than pigmentation.…”

Experimental simulation of environmental warming selects against pigmented morphs of land snails

“…As protein integrity is mandatory for a cell's survival, a biochemical chaperoning machinery that assists in protein (re)folding has been established early in the evolution of life. A central component of this machinery is the Hsp70 protein family, whose induction by heat and drought has been well characterized in land snails (Arad et al., 2010; Di Lellis et al., 2014; Dieterich et al., 2013, 2015; Gaitán‐Espitia et al., 2013; Köhler et al., 2009; Kotsakiozi et al., 2015; Mizrahi et al., 2010, 2011, 2012a, 2012b, 2015, 2016; Scheil et al., 2011; Troschinski, et al., 2014). As long as an induction of Hsp70 may compensate for the proteotoxic impact of body temperature elevation, organisms can limit pathologies and ensure survival.…”

Intermediate hosts of Protostrongylus pulmonalis (Frölich, 1802) and P. oryctolagi Baboš, 1955 under natural conditions in France

“…Similarly, species identification of snails is not so trivial, when based essentially on morphological criteria. The morphological polymorphism, inter and intra-specific, is extremely important in terrestrial snails depending on many parameters such as age, season, environmental conditions and biochemical factors [ 42 - 47 ]. Recently, using of molecular tools, by studying domains such as internal transcribed spacer and 18S rDNA or the COI and 16S mDNA, have facilitated the recognition of snails at a specific level.…”