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

Abstract

Understanding the maintenance of among‐individual behavioral variation in populations and predicting its consequences are key challenges in behavioral ecology. Studying the association between repeatable behaviors and other traits under selection may shed light on the underlying selective pressures. We used the model snail Cepaea nemoralis to examine whether individual behavior is associated with shell morph, a key trait that has been extensively studied in the context of 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 habitats with different thermal contexts. We show that both behaviors were repeatable at the among‐individual level (within‐state Rboldness = 0.22 [95% credible interval: 0.15; 0.29]; Rexploration = 0.20 [0.15; 0.25]). Behavior was associated with shell morph, with the darker morph (five‐banded) being consistently shyer and slower to explore. There was no evidence that thermal environment of origin influenced behavior. Snails became faster when test temperature increased; we found no evidence morphs differed in their thermal response. Boldness and exploration were correlated among individuals, forming a syndrome (r = 0.28 [0.10; 0.46]). The link we find between morph and boldness is compatible with visual selection by avian predators, assuming a positive association between boldness and morphological defense (phenotypic compensation hypothesis). The fact morph‐behaviors associations are consistent across environments, despite selection on morph, hint to a possible underlying genetic origin. Finally, we discuss how our findings combined with decades of evolutionary research make C. nemoralis a very valuable model to study the evolution of behavior in response to environmental changes.

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

“…This difference may be especially relevant: winter or summer dormancy can lead to sharp decreases in parasite infection in several parasite-snail systems (Haeussler et al, 2012;Segade et al, 2013;Solomon et al, 1996). We can thus reconcile the behavioural results from Dahirel et al (2021) with 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.…”

“…One key difference 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.…”

“…at the parasite species level; Morand et al, 2004), this would allow us to understand better how parasites with similar or different niches within snails interact. We found that movement behaviour in C. nemoralis was morph-dependent, but that this dependency varied between populations: five-banded morphs were less mobile, but contrary to Dahirel et al (2021), this was only the case in the shaded population (Fig. 4).…”

“…While here snails were collected several weeks after the onset of spring activity and kept active throughout, in Dahirel et al. (2021) they were collected in late fall and stored at cold temperatures inducing dormancy for months before being tested. This difference may be especially relevant: winter or summer dormancy can lead to sharp decreases in parasite infection in several parasite‐snail systems (Haeussler et al., 2012; Segade et al., 2013; Solomon et al., 1996).…”

“…at most ≈1.5 months after hibernation) from two contrasted sites in and near the village of Arc ¸ais, France. From previous studies, we know that snail parasites are present, albeit in another species (Cornu aspersum, Gérard et al, 2020), and that environmental differences between the sites are linked to differences in the frequency of darker C. nemoralis morphs (Dahirel et al, 2021).…”