Introgression across narrow contact zones shapes the genomic landscape of phylogenetic variation in an African bird clade

Abstract

Genomic analyses of hybrid zones provide excellent opportunities to investigate the consequences of introgression in nature. In combination with phylogenomics analyses, hybrid zone studies may illuminate the role of ancient and contemporary gene flow in shaping variation of phylogenetic signals across the genome, but this avenue has not been explored yet. We combined phylogenomic and geographic cline analyses in a Pogoniulus tinkerbird clade to determine whether contemporary introgression through hybrid zones contributes to gene-tree heterogeneity across the species ranges. We found diverse phylogenetic signals across the genome with the most common topologies supporting monophyly among taxa connected by secondary contact zones. Remarkably, these systematic conflicts were also recovered when selecting only individuals from each taxons core range. Using analyses of derived allele sharing and "recombination aware" phylogenomics, we found that introgression shapes gene-tree heterogeneity, and the species tree most likely supports monophyletic red-fronted tinkerbirds, as recovered in previous reconstructions based on mitochondrial DNA. Furthermore, by fitting geographic clines across two secondary contact zones, we found that introgression rates were lower in genomic regions supporting the putative species tree compared to those supporting the two taxa in contact as monophyletic. This demonstrates that introgression through narrow contact zones shapes gene-tree heterogeneity even in allopatric populations. Finally, we did not find evidence that mitochondria-interacting nuclear genes acted as barrier loci. Our results show that species can withstand important amounts of introgression while maintaining their phenotypic integrity and ecological separation, raising questions regarding the genomic architecture of adaptation and barriers to gene flow.