Inversions Dominate Evolution in the European Sardine (Sardina pilchardus) Amid Strong Gene Flow.

Abstract

Inversions can play key roles in the genetic architecture of adaptation, but the scale of their effects across different species remains poorly understood. Here, we use whole-genome sequencing and demographic modelling to investigate the influence of inversions on the population genomics of the r-selected European sardine (Sardina pilchardus). Allele frequency differences from millions of SNPs across 34 populations spanning the species' range were analysed. Genomic scans identified several extreme outlier regions overlapping large inversions (29-52 Mbp), collectively representing over half the genome. Our findings suggest these inversions correlate with locally adapted life-history strategies. First, SNPs within outlier regions containing inversions exhibited striking allele frequency differences between Atlantic and Mediterranean sardines, which differ in key adaptive life-history traits. In the Atlantic, inversion allele frequencies varied latitudinally, while in the Mediterranean, they shifted longitudinally, aligning with temperature and oceanographic features that influence sardine life-history strategies. Moreover, adjacent populations in contrasting environments exhibited pronounced differences in inversion allele frequencies, accompanied by a marked reduction in migration between them. In contrast, spatial patterns at neutral loci showed widespread gene flow, isolation by distance within basins, and population structure between Atlantic and Mediterranean basins (except for the Canary Islands). These results suggest that the inversions studied are under selection and demonstrate the capacity of large inversions to shape genome-wide patterns of genetic diversity and population structure in species characterized by widespread gene flow. Our work also offers crucial insights for stock delimitation and management of this commercially valuable species in the face of climate change.