Resolving the population structure and demographic history of the European anchovy in the Northeast Atlantic : tracking historical and contemporary environmental changes

Abstract

The spatial distribution of the European anchovy has expanded in the northern part of its range in the Northeast Atlantic in recent decades. However, whether this results from a northward range shift of southern conspecifics or the expansion of a local northern population is unknown. Using for the first time whole-genome sequencing, we explore current patterns of genetic diversity and population sub-structuring of European anchovy in the Northeast Atlantic, with special focus on recently expanded North Sea areas. Genomic data suggested three distinct groups: Northern (North Sea and Kattegat), Southern (Ireland and Central Portugal) and Cadis (South Portugal). Despite most of the genome being homogenised by high levels of gene flow characteristic of small pelagic fish, several large regions of high genetic differentiation were observed. This suggests that genomic population boundaries might be maintained by local adaptation within chromosome structural variants (inversions). Admixture analysis indicates that the ongoing northern range shift involves both migrants of southern origin and expansion of the local North Sea population. Historical demographic inference suggests that anchovies survived the last glacial period with small population sizes, followed by a split into the current Northern and Southern groups at the end of the last glacial maximum. The Southern group then expanded into the North Sea as the ice sheets retreated, in an expansion involving a large number of individuals, which is consistent with the retention of most of the genetic diversity. In comparison with other small pelagic fish, the genetic patterns found in anchovies (deeply divergent groups, no loss of genetic diversity during expansion, mixing between groups) align well with those found in European sprat, while sardines fit the pattern of expansion of a leading-edge population, with reduced genetic diversity and much shallower divergence between populations. This study contributes to a better understanding of population structure, range shifts and local adaptation in small pelagic fish under climate change, informing conservation and management efforts.