Molecular signatures of adaptive introgression and selection in contact zones of closely related pine species (Pinus genus)

Natural hybridization plays a key role in shaping genetic diversity, local adaptation, and the dynamics of speciation through interspecific gene flow. Hybrid zones serve as valuable natural systems for studying these processes. In this research, we used genotypic data at thousands of nuclear SNPs to investigate genomic outcomes of hybridization and selection across three contact zones of closely related pine species including Scots pine (Pinus sylvestris L.) and dwarf mountain pine (P. mugo T.). Reference allopatric stands of parental species were used to assess introgression dynamics. Individuals from the hybrid zones showed distinct genetic ancestry patterns and were assigned to groups including putative pure species, first-generation hybrids, and advanced backcrosses. Genotypes of the majority of hybrids were shifted towards P. mugo ancestry. Most outlier loci were shared across all sympatric populations, although some were specific to individual contact zones. The identified outliers were mainly associated with regulatory biological processes related to phosphorylation, proteolysis, and transmembrane transport. Signatures of local adaptation varied in different genetic classes in contact zones and they were strongest in pure P. sylvestris and hybrids with a majority of P. sylvestris ancestry. The pattern suggests that it may be driven by adaptation to peat bog habitats situated outside the species’ core ecological niche. Our findings indicate strong selective pressure acting on multiple genes in groups of hybrids and pure Pinus sylvestris individuals across all studied hybrid zones. In contrast, the weaker signal of selection observed in individuals with P. mugo ancestry suggests that relict populations of this species, which historically spread across postglacial peat bogs, were pre-adapted to such environments. While several outlier loci were shared across different contact zones, others were unique for one of them, indicating that local environmental pressures and adaptive introgression shape the genomic composition of the populations. These results highlight the role of hybridization in generating adaptive diversity and emphasize the evolutionary significance of hybrid zones in pines.