Phylogeography and historical introgression in smoothtail nine-spined sticklebacks, Pungitius laevis (Gasterosteiformes: Gasterosteidae)

Abstract

Pleistocene glaciations have strongly affected the biogeography of many species residing in periglacial and previously glaciated regions. Smoothtail nine-spined sticklebacks (Pungitius laevis) have three highly divergent mitochondrial lineages in France, one of which shares the same mitochondrial cluster with a congener P. pungitius. To understand if interspecific introgression has happened between the two species, we carried out phylogeographic and population genetic analyses using mitochondrial and nuclear gene sequences. Our results indicated asymmetric mitochondrial introgression from P. pungitius to P. laevis and genetic admixture of these species in one of the P. laevis lineages, suggesting historical hybridization. Deep intraspecific mitochondrial divergence within P. laevis in central and southern France mostly coinciding with major drainages suggests that these areas were important glacial refugia for the species explaining the observed intraspecific divergence. The historical hybridization between P. laevis and P. pungitius likely occurred in a refugium at central France, and the newly formed P. laevis lineage spread northward during postglacial recolonization. The study adds to the long list of species showing complete mitogenome capture owing to historical hybridizations, and highlights the reticulate nature of population differentiation in taxa subject to postglacial range-expansions.