Replicated hybrid zones reveal genomic patterns of local adaptation and introgression in spruce

Abstract

Hybridization between species can occur along repeated zones of contact, providing a natural laboratory for studying the interplay between migration and selection, and identifying loci involved in adaptation and reproductive isolation. However, interpreting how evolutionary processes shape genomic patterns can be challenging: repeatability of genotype-environment association alone is not strong evidence for selection, as hybrid zones derived from the same parental species are not evolutionarily independent. Conversely, processes that operate within the middle of each hybrid zone, such as selection driving directional introgression, may be more evolutionarily independent, and therefore provide stronger evidence of selection. Here we compared hybridization and local adaptation patterns between two replicated regions within the western Canada interior spruce hybrid zone: a broad latitudinal transect with gradual environmental variation and a narrow elevational transect with substantial topographical and environmental variation. We discovered a complex pattern of introgression, with strong differences in ancestry maintained even across small spatial scales at several locations along the elevational transect. Despite differences in their spatial scales, the elevational and latitudinal transects revealed strikingly similar genome-wide patterns of differentiation and adaptation, and consistent patterns of directional introgression. We explore the extent to which the evolutionary non-independence of these hybrid zones allows inferences about the role of natural selection and drift in shaping these patterns. Consistent with theory, we found longer genomic tracts in the elevational transect, likely because the steeper environmental gradients over shorter distances limit the rate of mixing by migration and recombination relative to drift and selection.