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. 2024 Dec 28;14(1):30977.
doi: 10.1038/s41598-024-82054-x.

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

Ana Rita Vieira #  1   2 , Filipe de Sousa #  3   4 , João Bilro  4 , Mariana Bray Viegas  4 , Richard Svanbäck  5 , Leonel S Gordo  6   3 , Octávio S Paulo  3   4
Affiliations

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

Ana Rita Vieira et al. Sci Rep. .

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.

Keywords: Geographic structure; Late Miocene cooling; Mid-Pliocene warm period; Mitogenome; Positive selection; Small pelagic fish.

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Conflict of interest statement

Declarations. Competing interests: The authors declare no competing interests. Ethics statement: Sampling for the present study focused on the European sardine from almost the entire species distribution range. Ethical or government approval, specific permissions or licenses for sample collection were not required for this study, as all specimens were collected as part of routine fishing procedures by fishermen of commercial fleets or scientific research campaigns. Fish are killed during the hauling of fishing gears due to differences in atmospheric pressure and fishing procedures. The experiments were conducted on dead animals, hence, no animal welfare or animal use permits were required for this study. Sardina pilchardus is not an endangered or protected species.

Figures

Fig. 1
Fig. 1
Sampling map. Sampling locations of the European sardine (Sardina pilchardus) across the species’ distribution geographic area. Produced with R Statistical Software (version 4.3.0 – https://www.R-project.org/). Sampling points coloured following the population clusters with maximum differentiation in AMOVA analysis (Fig. 2). Correspondence of each sampling point given in Table 1.
Fig. 2
Fig. 2
Haplotype median-joining network. Haplotype median-joining network calculated from the 13 gene alignment using PopArt. Samples coloured according to the population clusters with maximum differentiation in AMOVA analysis.
Fig. 3
Fig. 3
Principal components analysis. PCA of the whole mitochondrial genome dataset with 139 samples; (A) PC1 + PC2; (B) PC1 + PC3. Principal components 1, 2 and 3 explain 19%, 9% and 5% of the variance, respectively.
Fig. 4
Fig. 4
Time-calibrated phylogenetic reconstruction of Sardina pilchardus haplotypes. Tree showing the phylogenetic reconstruction obtained with a time-calibrated analysis of 63 haplotypes in BEAST2. The inferred tree is scaled to geological time in units of million years (Ma). Node support values represent posterior probabilities. Ple. – Pleistocene.
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