Mitochondrial genomes of the European sardine (Sardina pilchardus) reveal Pliocene diversification, extensive gene flow and pervasive purifying selection

Abstract

The development of management strategies for the promotion of sustainable fisheries relies on a deep knowledge of ecological and evolutionary processes driving the diversification and genetic variation of marine organisms. Sustainability strategies are especially relevant for marine species such as the European sardine (Sardina pilchardus), a small pelagic fish with high ecological and socioeconomic importance, especially in Southern Europe, whose stock has declined since 2006, possibly due to environmental factors. Here, we generated sequences for 139 mitochondrial genomes from individuals from 19 different geographical locations across most of the species distribution range, which was used to assess genetic diversity, diversification history and genomic signatures of selection. Our data supported an extensive gene flow in European sardine. However, phylogenetic analyses of mitogenomes revealed diversification patterns related to climate shifts in the late Miocene and Pliocene that may indicate past divergence related to rapid demographic expansion. Tests of selection showed a significant signature of purifying selection, but positive selection was also detected in different sites and specific mitochondrial lineages. Our results showed that European sardine diversification has been strongly driven by climate shifts, and rapid changes in marine environmental conditions are likely to strongly affect the distribution and stock size of this species.