Abstract
In neo-Darwinian theory, adaptation results from a response to selection on relatively slowly accumulating genetic variation. However, more rapid adaptive responses are possible if selectable or plastic phenotypic variation is produced by epigenetic differences in gene expression. This rapid path to adaptation may prove particularly important when genetic variation is lacking, such as in small, bottlenecked, or asexual populations. To examine the potential for an epigenetic contribution to adaptive variation, we examined morphological divergence and epigenetic variation in genetically impoverished asexual populations of a freshwater snail, Potamopyrgus antipodarum, from distinct habitats (two lakes versus two rivers). These populations exhibit habitat specific differences in shell shape, and these differences are consistent with adaptation to water current speed. Between these same habitats, we also found significant genome wide DNA methylation differences. The differences between habitats were an order of magnitude greater than the differences between replicate sites of the same habitat. These observations suggest one possible mechanism for the expression of adaptive shell shape differences between habitats involves environmentally induced epigenetic differences. This provides a potential explanation for the capacity of this asexual snail to spread by adaptive evolution or plasticity to different environments.
Highlights
Genetic variation is classically considered a pre-requisite to heritable phenotypic variation, the raw material of adaptation by natural selection[1,2,3,4]
To examine morphological divergence and methylation differences associated with different current speed habitats, we sampled snails from two rivers representing fast current speed habitat (River 1 site: main stem Snake River, ID at Ritter Island; River 2 site: a nearby tributary spring stream), and two lakes with no current (Lake 1 site: Lake Lytle, Rockaway Beach, OR; Lake 2 site: Lake Washington, Seattle, WA)
In concordance with earlier results, we found that the snails exhibited the expected adaptive pattern in shell shape and that these differences were statistically significant (Table 1); river snails had a significantly smaller overall spire height than the lake snails (Fig. 1A), and a significantly larger aperture opening for a given spire height (Fig. 1B)
Summary
Genetic variation is classically considered a pre-requisite to heritable phenotypic variation, the raw material of adaptation by natural selection[1,2,3,4]. Induced DNA methylation that produces adaptively biased phenotypic variation can provide the basis of an adaptive plastic response[27]. In the absence of genetic diversity in asexuals, the contribution of epigenetic diversity to the generation of a range of different phenotypes may provide an alternative pathway to adaptation by natural selection or plasticity[29]. Snail foot muscle size is well known to correlate with the aperture height of the shell[32,33,34] These shell shape responses concord with adaptive differences observed in other snails[34,35,36]. The same pattern of shell shape variation across current speed regimes was observed in a native congener, which has a long evolutionary history in the same geographic region[37]
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