Discrete or indiscrete? Redefining the colour polymorphism of the land snailCepaea nemoralis

Abstract

6Running head: Redefining a snail colour polymorphism 7 2 Biologists have long tried to describe and name the different phenotypes that make 8 up the exuberant colour polymorphism of the land snail Cepaea nemoralis. 9 Traditionally, the view is that the ground colour is one of a few major colour classes, 10 either yellow, pink or brown, but in practise it is frequently difficult to distinguish the 11 colours, and consistently define different shades of the same colour. To understand 12 whether colour variation is continuous, and to investigate how the variation may be 13 perceived by an avian predator, we applied psychophysical models of colour vision 14 to shell reflectance measures. The main finding is that both achromatic and 15 chromatic variation are indiscrete, being continuously distributed over many 16 perceptual units, with the major axis of chromatic variation representing differences 17 in saturation, or purity of colour. Nonetheless, clustering analysis based on the 18 density of the distribution revealed three groups, roughly corresponding to human-19 perceived yellow, pink and brown shells. There is also large-scale geographic 20 variation between these morphs across Europe, and some covariance between shell 21 colour and banding patterns. Although further studies are necessary to understand 22 the evolutionary origins and impact of natural selective upon this variation, the 23 observation of continuous variation in colour is intriguing, given that the underlying 24 supergene that determines colour should prevent phenotypes from "dissolving" into 25 continuous trait distributions. 26 27 3 Throughout the past century, the study of animal colour has been critical in making 28 progress in understanding the principles of biology, especially with respect to 29 genetics and evolution (McKinnon and Pierotti 2010; McLean and Stuart-Fox 2014; 30 Cuthill et al. 2017; San-Jose and Roulin 2017). For instance, early studies on the 31 inheritance of colour traits were important in establishing an understanding of basic 32 Mendelian genetics (Wheldale 1907; Staples-Browne 1908). Subsequently, studies 33 of the distribution and predation of colour morphs have and continue to shape our 34 understanding of how natural and sexual selection operate in wild populations 35 (Hugall and Stuart-Fox 2012; Dale et al. 2015; Delhey et al. 2017). Most recently, 36 candidate gene and latterly genomic approaches have been used to identify the 37 underlying genes that determine the colour differences (references in Hoekstra 2006; 38 McLean and Stuart-Fox 2014; San-Jose and Roulin 2017).39For practical reasons, many of these prior studies have taken advantage of 40 traits that exhibit relatively simple, discrete variation and straightforward inheritance 41 patterns, but this risks missing the extraordinary variation of life forms and colour 42 traits. It is also likely that in nature discrete variation is the exception rather than the 43 ruleand this is becoming more evident as researchers increasingly use 44 instrument...

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

“…It has a long history as a model in evolutionary biology, due to its conspicuous shell polymorphism (reviewed by Jones et al, 1977; Ożgo, 2009)(Figure 1A‐B). Genetic variation in shell background color (from pale yellow to brown, but usually divided in yellow, pink, and brown; Davison et al, 2019) and in the number or width of dark bands has been well described (Jones et al, 1977). Shell polymorphism is governed by a limited number of loci with a limited number of alleles (Richards et al, 2013), and by all evidence shows no phenotypic plasticity.…”

Recombination within theCepaea nemoralissupergene is confounded by incomplete penetrance and epistasis

“…We have previously shown that colour variation is multimodal but continuously variable in natural populations, necessitating the use of quantitative methods to measure it (Davison et al 2018). However, in simple crosses it is straightforward to bin the individuals into one of two types; quantitative measures are not necessary.…”

Qualitative and quantitative methods show stability in patterns of Cepaea nemoralis shell polymorphism in the Pyrenees over five decades

“…The ground color of adult snail shells from Vielha and Jueu valley was measured using an Ocean Optics spectrometer (model USB2000 + UV-VIS-ES) and a Xenon light source (DT-MINI-2-GS UV-VIS-NIR), as described previously (Davison et al, 2019). Briefly, the shell underside was used because it is generally unbanded and the least damaged/ F I G U R E 2 Overview of sampling locations in the Pyrenees, including this work, and previous work by others in the 1960s (Arnold, 1968;Cameron et al, 1973) exposed to sunlight, holding the probe at a 45° incident angle, ~2 mm from the shell.…”

“…In practise, it is frequently difficult to distinguish the colors, and define different shades of the same color. Therefore, to understand whether color variation is in reality continuous, and to investigate how the variation may be perceived by an avian predator, psychophysical models of color vision were applied to shell reflectance measures, finding that both achromatic and chromatic variation are continuously distributed over many perceptual units in indiscrete in Cepaea nemoralis (Davison et al, 2019). Nonetheless, clustering analysis based on the density of the distribution did reveal three groups, roughly corresponding to human-perceived yellow, pink, and brown shells.…”