Local adaptation along a continuous coastline: prey recruitment drives differentiation in a predatory snail

Recent work demonstrates that nearshore oceanography can generate strong variation in the delivery of resources (nutrients and larvae) to benthic marine communities over spatial scales of tens to hundreds of kilometers. Moreover, variation in the strength of these bottom-up inputs is often spatially consistent, linked to regional centers of upwelling, coastal topography, and other stable features of the coastline. Whereas the ecological effects of these oceanographic links are increasingly clear, the possibility that these same bottom-up forces might impose spatially varying selection on consumers has not been addressed. Here, we test the hypothesis that a carnivorous snail (Nucella canaliculata) with direct development is locally adapted to persistent differences in prey recruitment within two adjacent oceanographic regions (northern California and Oregon, USA). Previous laboratory studies demonstrated that snails from Oregon rarely drilled the thick-shelled mussel Mytilus californianus, whereas snails from California readily drilled this prey. To test whether these differences reflect local adaptation, snails from two populations in each region were raised through two laboratory generations to minimize the potential influence of nongenetic effects. We then reciprocally outplanted these F2 generation snails to field enclosures at each of the four sites and monitored their growth for 11 months. Recruitment and availability of preferred prey (the acorn barnacle Balanus glandula and blue mussel Mytilus trossulus) at the experimental sites were 1-3 orders of magnitude lower in California than in Oregon. At the California sites, snails that originated from Oregon sources failed to drill larger M. californianus, encountered few alternative prey, and showed almost no growth. In contrast, snails from California drilled M. californianus and showed substantial growth. These results strongly suggest that the capacity of California snails to drill M. californianus allows these snails to succeed in an oceanographic region where the recruitment of alternative, preferred prey is low. More broadly, our results suggest that persistent spatial variation in recruitment and other oceanographically mediated processes may lead to adaptive differentiation among populations of consumers in adjacent coastal regions.