Epistasis, phenotypic disequilibrium and contrasting associations with climate in the land snail Theba pisana

Abstract

Hotter conditions favour effectively unbanded (EUB) shells in the snail Theba pisana. T. pisana is also polymorphic for colour of the shell's apex, determined by a pair of alleles at a locus linked to the banding locus. Apex colour is epistatic to shell banding, such that banded snails with a dark apex have darker bands. Annual censuses over 22 years across an ecotone between a sheltered Acacia thicket and open dune vegetation showed a persistent association of both EUB shells and pale apex with the Open habitat. The parallel variation was due partly to strong phenotypic disequilibrium, as the combination of EUB with dark apex was rare. Nevertheless, in fully banded shells the frequency of pale apex was also higher in the Open habitat, confirming independent, parallel associations of the two contributors to paleness. Within the Acacia habitat, temporal variation of the frequencies of banding morphs was much greater than for apex colour, and EUB shells were associated with hotter summers. Consistent with its primary effect only on the very small snails, apex colour did not vary with summer conditions, but instead, higher frequencies of pale apices were associated with sunnier winters. The intensity of selection was lower on apex colour than shell banding, due partly to the constraint of phenotypic disequilibrium. The shell traits in T. pisana are an example of complex responses to climatic variation, in which phenotypic disequilibrium constrains evolution of apex colour, but separate mechanisms of selection are evident.

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

“…The banding of shells has a well‐characterized genetic background (Cowie, ; Jones et al, ; Murray, ) but suppression of pigmented bands in Cepaea nemoralis by expression of the hyalozonate gene is a long‐known phenomenon by which the phenotype of the shell can be modified (Cain, Sheppard, & King, ). In contrast to a directed selection (Johnson, , ), Köhler et al () who used a dataset of Cowie () showed high winter and spring temperatures to be associated with high variation in morph frequencies but not with the frequency of a particular morph. Also, a study on the phenotypic disequilibrium in a large dataset obtained for Cepaea nemoralis suggested that selection has favored combinations of common morphs, whichever they were (Cook, ).…”

“…This mechanism, however, cannot explain the maintenance of variation in uniformly hot habitats. Although to date there are not many studies statistically linking morph frequencies of snails to environmental parameters such as heat, three of them (Johnson, , ; Köhler et al, ) have identified moderately elevated temperatures acting on free‐living populations of Theba pisana in the middle of their lifetime as a key element for the variation in shell coloration. The studies of Johnson (, ) found hot summer conditions to increase the frequency of unbanded morphs in T heba pisana , attributing this phenomenon to climate selection.…”

“…Although to date there are not many studies statistically linking morph frequencies of snails to environmental parameters such as heat, three of them (Johnson, , ; Köhler et al, ) have identified moderately elevated temperatures acting on free‐living populations of Theba pisana in the middle of their lifetime as a key element for the variation in shell coloration. The studies of Johnson (, ) found hot summer conditions to increase the frequency of unbanded morphs in T heba pisana , attributing this phenomenon to climate selection. The very same phenomenon was observed by Dieterich et al () for X eropicta derbentina ; however, it remains to be clarified by further studies whether this is due to selection or shell bleaching, the latter eventually resulting from the inhibition of the melanin synthesis via oxidative stress/metallothionein‐induced stress proteins (Hsp70) as it has been observed for human or mouse melanocytes (Hoshino et al, ; Sasaki et al, ).…”

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

“…This might be particularly true for populations subjected to strong bottle-necks caused by, for example, high ambient temperatures. In T. pisana, high temperatures emerged either as a selective force or an epigenetically acting component of the environment (Johnson 2011(Johnson , 2012Köhler et al 2013): organisms possess various mechanisms to deal with high temperatures.…”

Historic data analysis reveals ambient temperature as a source of phenotypic variation in populations of the land snailTheba pisana

“…By contrast to other helicid snails such as Cepaea , which display distinct coloration and banding patterns, the polymorphism of T. pisana is multiform, with lots of variation within morphs, especially of the intensity of coloration of the bands. The interplay of genetic variation and presumed phenotypic plasticity leads to almost every individual expressing an apparently unique banding pattern as documented by Cowie () and Cain (), and as recently quantified by Johnson () for the intensity of banding. Even though Cowie (, ) scored all morphs on the ‘juvenile’ part of their shells, he pointed out that ‘virtually all shells’, also those scored as ‘unbanded’, ‘acquire some banding on later whirls.…”