Predictability and parallelism in the contemporary evolution of hybrid genomes

Hybridization between species is widespread across the tree of life. As a result, many species, including our own, harbor regions of their genome derived from hybridization. Despite the recognition that this process is widespread, we understand little about how the genome stabilizes following hybridization, and whether the mechanisms driving this stabilization tend to be shared across species. Here, we dissect the drivers of variation in local ancestry across the genome in replicated hybridization events between two species pairs of swordtail fish: Xiphophorus birchmanni × X. cortezi and X. birchmanni × X. malinche. We find unexpectedly high levels of repeatability in local ancestry across the two types of hybrid populations. This repeatability is attributable in part to the fact that the recombination landscape and locations of functionally important elements play a major role in driving variation in local ancestry in both types of hybrid populations. Beyond these broad scale patterns, we identify dozens of regions of the genome where minor parent ancestry is unusually low or high across species pairs. Analysis of these regions points to shared sites under selection across species pairs, and in some cases, shared mechanisms of selection. We show that one such region is a previously unknown hybrid incompatibility that is shared across X. birchmanni × X. cortezi and X. birchmanni × X. malinche hybrid populations.
Author summary We now know that hybridization, or the production of offspring between individuals of different species, happens frequently across many plant, animal, and fungi groups. As a result, the genomes of many contemporary species contain material derived from these hybridization events. At the same time, hybridization can have negative consequences on an organism’s ability to survive and reproduce. One major question is whether there are shared principles that determine which parts of the genome can move between species and which cannot. Here, we compare the genomes of several independently formed hybrid populations between the fish species pairs of Xiphophorus birchmanni and X. cortezi as well as X. birchmanni and X. malinche to begin to address this question. We find that across hybrid populations, regions of the genome with especially low recombination rates or especially high gene density are more likely to be derived from the parent species that contributed the majority of the genome to hybrids. Moreover, we identify regions of the genome that negatively interact in both types of hybrid population. Together our results demonstrate that genomic outcomes of hybridization between distinct species pairs are in part predictable.