Anchovies go north and west without losing diversity: post-glacial range expansions in a small pelagic fish

Aim As part of an emerging effort to understand the role played by climatic fluctuations in shaping the geographical distributions and abundances of marine organisms, we examined the genetic patterns of leading-edge populations in the European anchovy, Engraulis encrasicolus, and its American counterpart, the morphologically similar silver anchovy, Engraulis eurystole, in the North Atlantic Ocean. Location Adults were collected from the western Atlantic, eastern Atlantic (from Norway to Ghana) and western Mediterranean. Methods A 1045bp fragment of the mtDNA cytochrome b gene was sequenced (n=312) and nine microsatellite loci were genotyped (n=462) for anchovies from 13 locations across the temperate North Atlantic. Populations were surveyed for diversity and differentiation with a range of summary statistics. Multivariate discriminant analysis of principal components was employed to detect the number of genetic clusters in the data and assign individuals to populations based on their microsatellite genotypes. Historical demographic inferences - mismatch distributions and Bayesian skyline plots - were used to observe population size changes relating to climatic oscillations. Results Two mitochondrial clades were recovered, consistent with previous studies of E. encrasicolus, in which the frequency of each clade varied by latitude. Four genetic clusters corresponding loosely to large geographical regions were identified with microsatellite data. The north-western Atlantic E. eurystole was not reciprocally monophyletic for either mtDNA or microsatellite analyses and is probably conspecific with E. encrasicolus. Genetic diversity peaked in Iberian populations, but differences in genetic diversity were only statistically significant for the least diverse population, Tangier. The indications of demographic expansion were more pronounced in the southern clade and both mtDNA clades exhibited genetic diversity and expansion imprints that are likely to be older than climatic oscillations of the recent Pleistocene. Main conclusions The highly mobile nature of anchovies has allowed them to track their optimal thermal physiological conditions during the extreme climate shifts of the Last Glacial Maximum and avoid wholesale population reductions and genetic bottlenecks. Both north-eastern and north-western Atlantic were probably rapidly recolonized after the Last Glacial Maximum by large numbers of anchovies, such that leading-edge populations retained the genetic diversity of parent populations.