Adaptive introgression and incompatibility shape interspecific hybrid genomes in ornamental and feral Xiphophorus...

Adaptive introgression can propel the rapid evolution of species but it is resisted by hybrid incompatibility. Ornamental swordtails are the result of century-old hybridization among multiple ancestries, which is a precious system for understanding interspecific gene flow under artificial selection. We combine HMM-based local ancestry inference and simulations to infer the hybridization parameters. We develop new pseudolikelihood statistics for identifying candidate regions under strong adaptive introgression. Candidate regions involved in high-frequency introgressions are enriched for functions such as immunity, reproduction, survival, and life history traits. Compared to short genomic regions harboring high frequency of the minor ancestry (>90%), which contained lower protein-coding density and lower relative genetic load in the minor parental, strong adaptive introgression occurs more often in regions of higher functional density, suggesting that highly adaptive alleles can potentially overcome the resistance by incompatibility. We further identified incompatibility loci involved in mito-nuclear interactions. These findings highlight the interplay between adaptive introgression and hybrid incompatibility in shaping hybrid genomes.