Predictability and parallelism in the contemporary evolution of hybrid genomes

Abstract

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 surprisingly 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.

Mate choice enhances post-zygotic barriers to gene flow via ancestry bundling

“…Even in cases where mating is not observed, 𝜌 can still be measured by estimating the ancestry fractions of mothers and offspring. In a hybrid population of the swordtail fish species Xiphophorus birchmanni and X. cortezi in Hidalgo, Mexico, genomic evidence suggests that the minor-parent ancestry (birchmanni) is deleterious to individuals of predominantly major-parent ancestry (cortezi) (Langdon et al 2021). Powell et al (2021) measured mother-offspring ancestry differences to infer paternal ancestry, finding evidence for strong ancestry-based assortative mating in this system [consistent with other swordtail systems (Culumber et al 2014, Schumer et al 2017].…”

Selection leads to remarkable variability in the outcomes of hybridization across replicate hybrid zones

“…This also means that we would not have found a correlation between recombination and minor ancestry as in (Langdon et al 2022), although we also did not find a correlation of minor ancestry between replicate populations. Future work could simulate such recombination landscapes and ask how this affects variation in outcomes across replicate hybrid zones.…”

“…Further, previous work has shown that selection on individual loci can lead these loci to deviate in ancestry from neutral loci elsewhere in the genome (Gompert & Buerkle 2011), though attributing deviation at exceptional loci to drift or selection is fraught (Gompert & Buerkle 2011, McFarlane et al 2021). These assumptions underlie the basic premise of replicate hybrid zone research: similarities across replicates should be indicative of shared isolating barriers, independent of the effects of genetic drift at each individual population, thereby giving insight into the nature of reproductive isolation between a pair of species (Langdon et al 2022, Matute et al 2020, Rieseberg et al 1999, Simon et al 2020, 2021, Westram et al 2021). Despite this expectation, many of our simulations highlight remarkable variation in individual-level parameters (Figs.…”

“…Some studies have used minor ancestry at haplotypes, rather than admixture proportion, to determine to what extent there are regions of the genome with depleted variation, suggesting incompatibilities (e.g. Langdon et al 2022, Schumer et al 2018). While we explored this for specific loci (Table S3), we are conscious that polarizing by minor parent assumes that backcrossing in either direction has the same consequences, regardless of the ancestry of the genetic background.…”

“…Moreover, replicate hybrid zones could be used to understand how these evolutionary processes vary across space, time, and ecological variation (Buerkle & Rieseberg 2001, Harrison & Larson 2016, Westram et al 2021). In the context of identifying loci important to determining hybridization outcomes, consistency or parallelism of loci with exceptional differentiation or introgression between populations (via F ST , and geographic or genomic clines) have been suggested as evidence for either loci associated with adaptive introgression or genomic regions associated with reproductive isolation (Langdon et al 2022, Matute et al 2020, Rieseberg et al 1999, Simon et al 2020, 2021, Westram et al 2021). But the question remains: if hybrid zones are indeed windows into evolution (Harrison 1990), do different scenes viewed through the window imply differences in process?…”