Boldness and exploration vary between shell morphs but not environmental contexts in the snailCepaea nemoralis

Abstract

Understanding the maintenance of individual behavioural variation (or animal personalities) in populations, and predicting its consequences, are key challenges in behavioural ecology. As individuals vary in their phenotype and experienced environment, they may experience different selective pressures favouring different optimal behaviours. Studying the (genetic) association between repeatable behaviour and other traits under selection may shed light on these selective pressures. We used the model snail Cepaea nemoralis to examine whether individual behavioural variation is associated with variation in shell morph, a key trait that has been extensively studied in relation to thermal tolerance and predator avoidance, and which is known to be under strict genetic control in this species. We quantified proxies of boldness and exploration in snails of three morphs coming from two contrasted thermal environments. We show that there are animal personalities in C. nemoralis, as both behaviours were repeatable at the individual level. Behavioural variation was associated with shell morph, with the darker morph (five-banded) being consistently shyer and slower to explore. There was no evidence that experienced thermal environment influenced behaviour at the individual level, whether we considered past environment or experimental temperature. Boldness and exploration were correlated at the individual level in a common syndrome. We discuss how these results are compatible with (but do not confirm) the pace of life syndrome hypothesis, and what they tell us about the type of selection exerted by predators. We also detail how our results hint to a genetic link between shell morph and behaviour, and the evolutionary implications of such a link. Finally, we discuss how our results combined with decades of evolutionary research make C. nemoralis a very valuable model to study the evolution of behaviour in response to environmental changes.

Morph-dependent nematode infection and its association with host movement in the land snail Cepaea nemoralis (Mollusca, Gastropoda)

“…from Dahirel et al (2021) from those of the present study if we assume that in the former experiment, hibernation reduced parasite load across all morphs and populations, and that in the present study, lower temperatures in the shaded habitat led to longer hibernation. We can then interpret population differences in the present study in the light of their different infection patterns.…”

“…4). One of the main differences between the present study and Dahirel et al (2021) is the collection date. While here snails were collected several weeks after the onset of spring activity and kept active throughout, in Dahirel et al (2021) 2020 for a species-specific possible counter-example), or mite infection in Arianta arbustorum (Haeussler et al, 2012).…”

“…One of the main differences between the present study and Dahirel et al (2021) is the collection date. While here snails were collected several weeks after the onset of spring activity and kept active throughout, in Dahirel et al (2021) 2020 for a species-specific possible counter-example), or mite infection in Arianta arbustorum (Haeussler et al, 2012). Aestivation also slows down parasite development in two smaller species of land snails (Theba pisana and Trochoidea seetzenii), and reduces parasite numbers in the latter (Solomon, Paperna & Matkovics, 1996).…”

“…Based on the expected link between pigments and immune defence outlined above, we expected snails with more dark bands hosted fewer parasites. Since darker snails are less mobile (Dahirel et al ., 2021), that expectation is also in line with some predictions from the pace-of-life syndrome hypothesis, namely that fast active individuals have lower immune responses (Réale et al ., 2010; but see Royauté et al ., 2018). We also hypothesized that metazoan parasites would have notable negative effects on snail performance (McElroy & de Buron, 2014), leading to slower behaviours and changed food intake in more infected snails (both at the morph level and within morphs).…”

“…These differences are genetically determined, and decades of research have aimed to disentangle the roles of thermal selection, predation risk and neutral processes in driving variation in morph frequencies (Cain & Sheppard, 1954; Lamotte, 1959; Jones et al ., 1977; Schilthuizen, 2013; Ożgo et al ., 2017; Kerstes et al ., 2019). These color differences are associated with behavioural and physiological differences (Kavaliers, 1992; Rosin et al ., 2018; Dahirel, Gaudu & Ansart, 2021), as well as other morphological differences (e.g. shell strength, Rosin et al ., 2013), leading to potentially adaptive phenotypic syndromes.…”