Variation and constraints in hybrid genome formation

Abstract

Recent genomic investigations have revealed hybridization to be an important source of variation, the working material of natural selection1,2. Hybridization can spur adaptive radiations3, transfer adaptive variation across species boundaries4, and generate species with novel niches5. Yet, the limits to viable hybrid genome formation are poorly understood. Here we investigated to what extent hybrid genomes are free to evolve or whether they are restricted to a specific combination of parental alleles by sequencing the genomes of four isolated island populations of the homoploid hybrid Italian sparrow Passer italiae6,7. Based on 61 Italian sparrow genomes from Crete, Corsica, Sicily and Malta, and 10 genomes of each of the parent species P. domesticus and P. hispaniolensis, we report that a variety of novel and fully functional hybrid genomic combinations have arisen on the different islands, with differentiation in candidate genes for beak shape and plumage colour. There are limits to successful genome fusion, however, as certain genomic regions are invariably inherited from the same parent species. These regions are overrepresented on the Z-chromosome and harbour candidate incompatibility loci, including DNA-repair and mito-nuclear genes; loci that may drive the general reduction of introgression on sex chromosomes8. Our findings demonstrate that hybridization is a potent process for generating novel variation, but variation is limited by DNA-repair and mito-nuclear genes, which play an important role in reproductive isolation and thus contribute to speciation.