The traditional paradigm of open marine populations has been challenged by the growing recognition that many marine species are comprised of weakly connected, genetically differentiated populations. Although low gene flow among populations increases the potential for species to respond to spatial variation in selection, local adaptation continues to receive surprisingly little attention in marine systems. Here, we document adaptive differentiation in the response of a carnivorous snail (Nucella canaliculata) to an intertidal mussel (Mytilus californianus) along a gradient of oceanographic conditions. Based on our previous observations, we hypothesized that snails in a region of lower recruitment (northern California, USA) have less access to preferred prey (the blue mussel M. trossulus and acorn barnacle B. glandula) than snails in Oregon, and have evolved a greater capacity to drill the thick-shelled M. californianus, a species that is common in both regions. To test this hypothesis, snails from 8 populations in California and Oregon were raised through two generations under common conditions and tested for their capacity to drill M. californianus in the laboratory. We also reciprocally outplanted laboratory-reared, F2 generation snails from two populations in each region to field enclosures at each site to test whether snail populations were locally adapted to the prey assemblages in their region of origin.  

Results/Conclusions

Remarkably, laboratory trials indicated that F2 generation snails from Oregon sources were generally unable to drill mid-sized M. californianus (5–7 cm long), whereas snails from California readily drilled this prey. Because snails were raised through two generations on a common diet, these differences among populations likely have a genetic basis. Our reciprocal outplant of laboratory-reared, F2 generation snails to field enclosures indicated that the capacity to drill these thick-shelled mussels allows snails from California to succeed in an oceanographic region where the recruitment of alternative, preferred prey is low. At sites in California, snails that originated from Oregon sources were unable to drill mid-sized M. californianus, encountered few alternative prey, and showed almost no growth. In contrast, snails from California drilled M. californianus and experienced substantial growth at these sites. This empirical evidence of local adaptation suggests that persistent spatial variation in prey recruitment and other bottom-up processes can drive adaptive differentiation in some marine consumers, leaving an unrecognized evolutionary signature on the strength of species interactions within adjacent regions of coastline.