Nucella lapillus ecotypes at the southern distributional limit in Europe: variation in shell morphology is not correlated with chromosome counts on the Portuguese Atlantic coast

Abstract

Nucella lapillus (L.) is a gastropod widely distributed along North Atlantic rocky shores (Crothers, 1985a; Tyler-Walters, 2008). Individuals are found from extremely exposed places to the most sheltered inlets, which is considered to be the main reason for the high variability in shell appearance (Crothers, 1985b). This plasticity of shell shape and size has been extensively studied in relation to selection by both wave exposure and predation pressure (see review by Crothers, 1985b). Two specific morphs or ecotypes are defined: the sheltered and the exposed morph (Rolan et al., 2004). Briefly, N. lapillus specimens grow faster and have taller shells on sheltered shores than at wave exposed sites (Crothers, 1985a). Under sheltered conditions heavy crab predation is probably responsible for the selection of stronger and thickened shells (Currey & Hughes, 1982), smaller apertures (Etter, 1989) and sometimes toothed lips (Cowell & Crothers, 1970). In contrast, individuals on exposed shores normally have thinner shells and wider apertures to accommodate a larger foot for increased pedal adhesion to the rock surface under rough wave conditions (Currey & Hughes, 1982). A progression from the elongated (sheltered) to the squat (exposed) ecotype is found across increasing wave-exposure gradients and, therefore, a range of intermediate forms can also be observed (Crothers, 1985a, b; Etter, 1989). Analysis of N. lapillus shell-shape has therefore been used as a way to classify wave exposure of a given shore. Crothers (1985b) found a linear relation between N. lapillus shell-shape, expressed by the ratio between shell height (SH or length) and aperture height (AH), and the classical Ballantine biologically defined wave exposure scale (Ballantine, 1961). This scale was developed to measure the degree of exposure to wave action based on the local fauna and flora communities, allowing the direct classification of wave exposure in eight different stages (from 1, ‘extremely exposed’ to 8, ‘extremely sheltered’; Ballantine, 1961), subsequently extended to a 10-point scale (from 0, ‘ultimately exposed’ to 9, ‘ultimately sheltered’; Dalby et al., 1978). Instead of looking at the entire biological community, Crothers developed a way to relate a single variable (N. lapillus shell-shape) to wave exposure, by regression analysis of the shell-shape ratio and the exposure degree given by the Ballantine scale, maintaining its quantification ability (see review by Crothers, 1985b). The method was applied throughout both eastern and western North Atlantic coasts, although some adjustments to the initial regression were made due to some exceptions to the shell-shape variation of N. lapillus in different regions (Crothers, 1983, 1985b). In addition to the widely reported phenotypic variation, differences in chromosome numbers are also present in this species (Bantock & Cockayne, 1975; Pascoe & Dixon, 1994). Nucella lapillus is the only muricid in which karyotype variations by intraspecific Robertsonian chromosomal translocations have been described (Bantock & Cockayne, 1975; Pascoe & Dixon, 1994; Pascoe et al., 1996; Pascoe, Jha & Dixon, 2004). These karyotypical differences were first described for populations around Roscoff, Brittany, where they were associated with variations in shell thickness among sites (Staiger, 1957 in Crothers, 1985a). A link between chromosome number and the degree of wave exposure was then proposed and broadly reported (Bantock & Cockayne, 1975; Crothers, 1985a; Kirby, Bayne & Berry, 1994; Pascoe & Dixon, 1994; Pascoe et al., 1996, 2004; Kirby, 2004). A karyotype of 2n 1⁄4 26 has been reported over much of the wide geographic distribution of N. lapillus but, in a restricted part of its range (southwestern Cornwall and northwestern Brittany, on directly opposite shores of the English Channel) chromosome counts of a maximum of 2n 1⁄4 36 are common (Bantock & Cockayne, 1975; Pascoe & Dixon, 1994; Pascoe, 2006). The 2n 1⁄4 26 morph was initially associated with exposed shores with high levels of wave action, while the 2n 1⁄4 36 morph was observed exclusively in sheltered bays and harbours (Kirby et al., 1994; Pascoe & Dixon, 1994; Pascoe et al., 2004). However, the 2n 1⁄4 26 form was subsequently found to be widely distributed (Norfolk and Cornwall in the UK, Norway, France and Spain) on differing shore types and to have a remarkably stable karyotype between populations (Pascoe, 2006). Although these variations have been extensively reported, there is a lack of information on the ecotype(s) present at the southern distributional limit of the species in Europe. There is a single literature record of N. lapillus chromosome number (2n 1⁄4 26) at one sample site for the whole mainland coast of Portugal (Pascoe, 2006). In order to discover the ecotype(s)