Replicate geographic transects across a hybrid zone reveal parallelism and differences in the genetic architecture of reproductive isolation

Abstract

Determining the genetic architecture of traits involved in adaptation and speciation is one of the key components of understanding the evolutionary mechanisms behind biological diversification. Hybrid zones provide a unique opportunity to use genetic admixture to identify traits and loci contributing to partial reproductive barriers between taxa. Many studies have focused on the temporal dynamics of hybrid zones, but geographical variation in hybrid zones that span distinct ecological contexts has received less attention. We address this knowledge gap by analyzing hybridization and introgression between black-capped and Carolina chickadees in two geographically remote transects across their extensive hybrid zone, one located in eastern and one in central North America. Previous studies demonstrated that this hybrid zone is moving northward as a result of climate change but is staying consistently narrow due to selection against hybrids. In addition, the hybrid zone is moving ~5× slower in central North America compared to more eastern regions, reflecting continent-wide variation in the rate of climate change. We use whole genome sequencing of 259 individuals to assess whether variation in the rate of hybrid zone movement is reflected in patterns of hybridization and introgression, and which genes and genomic regions show consistently restricted introgression in distinct ecological contexts. Our results highlight substantial similarities between geographically remote transects and reveal large Z-linked chromosomal rearrangements that generate measurable differences in the degree of gene flow between transects. We further use simulations and analyses of climatic data to examine potential factors contributing to continental-scale nuances in selection pressures. We discuss our findings in the context of speciation mechanisms and the importance of sex chromosome inversions in chickadees and other species.