Scale and direction of adaptive introgression between black cottonwood (Populus trichocarpa) and balsam poplar (P. balsamifera)

Abstract

Introgression can introduce novel genetic variation at a faster rate than mutation alone and result in adaptive introgression when adaptive alleles are maintained in the recipient genome over time by natural selection. A previous study from our group demonstrated adaptive introgression from Populus balsamifera into P. trichocarpa in a target genomic region. Here we expand our local ancestry analysis to the whole genome of both parents to provide a comprehensive view of introgression patterns and to identify additional candidate regions for adaptive introgression genomewide. Populus trichocarpa is a large, fast-growing tree of mild coastal regions of the Pacific Northwest, whereas P. balsamifera is a smaller stature tree of continental and boreal regions with intense winter cold. The species hybridize where they are parapatric. We detected asymmetric patterns of introgression across the whole genome of these two poplar species adapted to contrasting environments, with stronger introgression from P. balsamifera to P. trichocarpa than vice versa. Admixed P. trichocarpa individuals contained more genomic regions with unusually high levels of introgression (19 regions) and also the largest introgressed genome fragment (1.02 Mb) compared with admixed P. balsamifera (nine regions). Our analysis also revealed numerous candidate regions for adaptive introgression with strong signals of selection, notably related to disease resistance, and enriched for genes that may play crucial roles in survival and adaptation. Furthermore, we detected a potential overrepresentation of subtelomeric regions in P. balsamifera introgressed into P. trichocarpa and possible protection of sex-determining regions from interspecific gene flow.

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

“…It is interesting that 54 of our 1,764 introgression outliers are located in the 20 genomic regions found to be introgressing from P. balsamifera into admixed P. trichocarpa (13 regions) or the opposite (seven regions) as reported by Suarez‐Gonzalez, Hefer et al. (). This raises an intriguing possibility that genomic regions that are targets of adaptive introgression might be shared in geographically distant hybrid zones, even when a different hybridizing partner is involved.…”

“…While hybridization is well documented in the genus Populus in North America (Eckenwalder (); Talbot, Schroeder, Bousquet, and Isabel (); Geraldes et al. ()), and recent reports have highlighted the importance of adaptive introgression between P. balsamifera and P. trichocarpa (Suarez‐Gonzalez et al., ; Suarez‐Gonzalez, Hefer et al., ), our study provides the first genomewide assessment of adaptive introgression between Populus species specifically where they overlap at their range limits.…”

“…The prevalence of backcross hybrids with predominantly P. balsamifera ancestry likely reflects our sampling of individuals with more balsamifera ‐like traits, but we cannot rule out a bias in the direction of hybrid compatibility between parental genomes. Such asymmetric introgression is known in the P. angustifolia and P. fremontii hybrid zone in Utah where the backcrosses have been observed only with the narrowleaf cottonwood (Keim, Paige, Whitham, & Lark, ; Whitham et al., ), and is also reported between P. trichocarpa and P. balsamifera hybrid zones, in which introgression is biased towards P. balsamifera (Suarez‐Gonzalez, Hefer et al., ). Future sampling should target a broader range of individuals within this hybrid zone to determine whether hybrid viability varies asymmetrically between the genomes of the parental species.…”

“…In the same way, loci under local adaptation (in P. balsamifera and P. trichocarpa ) did not exhibit genomic islands of differentiation that inhibited introgression. Significant overlap between local adaptation outliers in pure species and introgression selection candidates has been reported in the P. trichocarpa and P. balsamifera hybridization zone in British Columbia, Alberta and Manitoba (Suarez‐Gonzalez, Hefer et al., ). Lack of such association in our study in P. balsamifera could reflect different selection regimes in allopatric vs. sympatric regions or the presence of conditional neutrality (e.g., loci involved in local adaptation elsewhere in the species range do not experience selection in the hybrid zone).…”

“…Two of our study species, P. trichocarpa and P. balsamifera , are recently speciated sister taxa with a shallow divergence time of ∼ 76,000 years (Levsen, Tiffin, & Olson, ), and share a more distant common ancestor with P. angustifolia (Cervera et al., ; Hamzeh & Dayanandan, ). Given the close phylogenetic relationships and proximate current geographic range limits of all three species (Levsen et al., ), the potential for admixture events arising from secondary contact during glacial advance and retreat may have existed for millennia (Suarez‐Gonzalez et al., ; Suarez‐Gonzalez, Hefer et al., ). To better understand the joint history of these populations and the most likely migration events between them that generated admixture, we used treemix (Pickrell & Pritchard, ) to analyse a Gaussian model of genetic drift with admixture to estimate a population phylogeny.…”