Independence of neutral and adaptive divergence in a low dispersal marine mollusc

Abstract

Identifying how the interplay between neutral and adaptive evolutionary processes shapes the spatial structure of natural populations is a central task in ecology and conservation biology. In marine populations, generally characterised by large population sizes and high gene flow, the simultaneous use of multiple descriptors (i.e. genetic, morphological, life-history, etc.) can be particularly helpful in unravelling the often subtle and complex spatial patterns observed. The gastropod Buccinum undatum (common whelk) lacks a planktonic larval stage, which could promote isolation of local populations and lead to phenotypic divergence through genetic drift or local adaptation. Despite the commercial significance of this species, the relative importance of these 2 forces remains unknown. Here, we used microsatellites, geometric morphometrics and shell thickness measurements to investigate the evolutionary dynamics generating spatial variation in 10 whelk populations in coastal waters around Ireland. Genetic diversity was generally high and genetic structure moderate but significant (overall FST = 0.019), in accordance with an isolation-by-distance pattern. Phenotypic divergence, as measured by PST, was uncorrelated with, and much more pronounced than, neutral divergence (FST), indicating that environmental variation rather than population isolation drives phenotypic differentiation. For some traits, at least, diversifying selection is likely to be involved unless additive genetic components of phenotypic variation among populations are very low. Our results document a lack of correspondence between neutral and adaptive divergence, and highlight the need to couple connectivity estimates with the assessment of ecologically relevant traits in fisheries management and conservation.