International Lectures on Nature and Human Ecology

Steve Jones
Interactions between genes and the environment in land snails

C H Waddington's interests extended far beyond the experiments on canalization of development for which he is most remembered. In fact Wad taught me when I was an undergraduate in Edinburgh, and my main memory of his lectures is of a fascinating account of the development of shell patterns in the marine snail Conus, which has subsequently become a minor model organism in the world of developmental genetics. I myself have spent most of my career working on snails, not on development but on their interactions with the environment, and almost inadvertently my research has had a considerable overlap with Waddington's interests, as outlined in the introductory paper of the symposium, on the behavioural responses of individuals of different genotype with the habitat in which they live. The land snail Cepaea nemoralis has a striking system of diversity in shell pattern, with a variety of loci controlling colour and the degree of shell banding to generate a range of phenotypes in effect from black to white. Fifty years ago, when I started my research, it was one of the few creatures in which it is possible to count genes in natural populations, although with the advent of DNA sequencing that has become commonplace.

The first, and easiest, task is to ask why allele frequencies vary from place to place. Over many years we have shown that both on the large scale across Europe, and – at least in some places such as mountain ranges – there is often a striking tendency for relatively light coloured shells to be common in places with high levels of solar energy, and for the opposite to be true. There are exceptions, and no doubt founder effects and predator pressure has some influence, but these are in general minor. This is also manifest in behaviour. It has long been known that the temperature at the ground surface on a sunny day is far higher than that just a few centimetres higher. Snails climb to escape this: and simple experiments show that southern European individuals do so much more actively than those from Scotland, where the sun rarely shines. What is more, experiments on pain perception in high temperatures, using a heated plate, show that southern populations are less responsive to a heat stimulus than are those from the north.

The more interesting, and more difficult, question – and one raised by Waddington – asks why, given that there is such good evidence of local climate alters gene frequencies for shell colour, nealy all C nemoralis populations, from Scotland to Spain, retain genetic diversity. Might it be that animals of different phenotype choose different parts of their environment to match their genes, and their thermal balance, to differences in temperature within the bush or sward within which they live? We approached this problem by developing a method of measuring long-term solar exposure with a paint based on a stable yellow base and an unstable blue dye. The resulting green paint fades to yellow over several weeks or months of exposure. Thousands of snails were marked on a "snail ranch" on Wytham Hill near Oxford, and marked differences in individual exposure to sunshine were found between dark- and light-coloured snails. These could be reversed with simple experiments with black and white paint. Waddington's radical suggestion that genotypes can match themselves to their environment has been, like so many of his ideas, tested and in this system at least found to be correct: once again he is proved to have been well before his time in his scientific ideas.

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