Adaptive introgression and maintenance of a trispecies hybrid complex in range-edge populations of Populus

In hybrid zones occurring in marginal environments, adaptive introgression from one species into the genomic background of another may constitute a mechanism facilitating adaptation at range limits. Although recent studies have improved our understanding of adaptive introgression in widely distributed tree species, little is known about the dynamics of this process in populations at the margins of species ranges. We investigated the extent of introgression between three species of the genus Populus sect. Tacamahaca (P. balsamifera, P. angustifolia and P. trichocarpa) at the margins of their distributions in the Rocky Mountain region of the United States and Canada. Using genotyping by sequencing (GBS), we analysed ~ 83,000 single nucleotide polymorphisms genotyped in 296 individuals from 29 allopatric and sympatric populations of the three species. We found a trispecies hybrid complex present throughout the zone of range overlap, including early as well as advanced generation backcross hybrids, indicating recurrent gene flow in this hybrid complex. Using genomic cline analysis, we found evidence of non-neutral patterns of introgression at 23% of loci in hybrids, of which 47% and 8% represented excess ancestry from P. angustifolia and P. balsamifera, respectively. Gene ontology analysis suggested these genomic regions were enriched for genes associated with photoperiodic regulation, metal ion transport, maintenance of redox homeostasis and cell wall metabolites involved in regulation of seasonal dormancy. Our study demonstrates the role of adaptive introgression in a multispecies hybrid complex in range-edge populations and has implications for understanding the evolutionary dynamics of adaptation in hybrid zones, especially at the margins of species distributions.