Two new hybrid populations expand the swordtail hybridization model system

Abstract

Natural hybridization events provide unique windows into the barriers that keep species apart as well as the consequences of their breakdown. Here, we characterize hybrid populations formed between the northern swordtail fish Xiphophorus cortezi and Xiphophorus birchmanni from collection sites on two rivers. We use simulations and new genetic reference panels to develop sensitive and accurate local ancestry calling in this novel system. Strikingly, we find that hybrid populations on both rivers consist of two genetically distinct subpopulations: a cluster of pure X. birchmanni individuals and one of phenotypically intermediate hybrids that derive ∼85–90% of their genome from X. cortezi. Simulations suggest that initial hybridization occurred ∼150 generations ago at both sites, with little evidence for contemporary gene flow between subpopulations. This population structure is consistent with strong assortative mating between individuals of similar ancestry. The patterns of population structure uncovered here mirror those seen in hybridization between X. birchmanni and its sister species, Xiphophorus malinche, indicating an important role for assortative mating in the evolution of hybrid populations. Future comparisons will provide a window into the shared mechanisms driving the outcomes of hybridization not only among independent hybridization events between the same species but also across distinct species pairs.

Predictability and parallelism in the contemporary evolution of hybrid genomes

“…Research on this sister species pair has shown that variation in local ancestry along the genome is best explained by the presence of prevalent hybrid incompatibilities (as opposed to historical effective populations size differences in the parental species or ecological drivers of ancestry variation; [35]), and has documented strong DMIs between them [23]. Here, we expand on our recent description of replicate hybrid populations of the species pair X. birchmanni ´ X. cortezi [46] to explore repeatability in local ancestry between these two types of hybrid populations.…”

“…birchmanni ´ X. cortezi are more deeply diverged than X. birchmanni ´ X. malinche (~450k generations diverged and ~250k generations diverged respectively) and unlike X. birchmanni and X. malinche, they do not differ in their time-averaged historical effective population sizes (Fig. S1) [46]. Hybrid populations between both species pairs formed recently (~100-150 generations ago [20,46]), likely due to human disturbance [47].…”

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

“…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]. Using the mother-offspring data of Powell et al (2021), we calculate an ancestry correlation among mating pairs of 𝜌 = 0.928 (Methods; Fig. S8B).…”

“…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]. Using the mother-offspring data of Powell et al (2021), we calculate an ancestry correlation among mating pairs of 𝜌 = 0.928 (Methods; Fig.…”

“…Since some mothers have multiple embryos in the data of Powell et al (2021), we calculated 𝛽 IK using the average ancestry fraction of each mother's offspring, yielding an estimate of 𝛽 IK = 0.964 (note that the same value would be obtained asymptotically if we averaged over iterations in which we randomly choose one embryo per mother and calculate 𝛽 IK for the reduced dataset). From Eq.…”