High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species.

Molly Schumer,Daniel L Powell,Gil G Rosenthal,Peter Andolfatto,Rebecca Dresner,Rongfeng Cui

doi:10.7554/elife.02535

Abstract

Hybridization is increasingly being recognized as a common process in both animal and plant species. Negative epistatic interactions between genes from different parental genomes decrease the fitness of hybrids and can limit gene flow between species. However, little is known about the number and genome-wide distribution of genetic incompatibilities separating species. To detect interacting genes, we perform a high-resolution genome scan for linkage disequilibrium between unlinked genomic regions in naturally occurring hybrid populations of swordtail fish. We estimate that hundreds of pairs of genomic regions contribute to reproductive isolation between these species, despite them being recently diverged. Many of these incompatibilities are likely the result of natural or sexual selection on hybrids, since intrinsic isolation is known to be weak. Patterns of genomic divergence at these regions imply that genetic incompatibilities play a significant role in limiting gene flow even in young species.

Highlights

Hybridization between closely related species is remarkably common (Mallet, 2005)
We focus all subsequent analyses on the subset of significant linkage disequilibrium (LD) pairs (FDR = 0.05) with conspecific associations in both populations (207 locus pairs) because these sites will be enriched for hybrid incompatibilities, but similar results are observed for the whole data set (Supplementary file 1C)
Given that post-zygotic isolation between X. birchmanni and X. malinche is weak (Rosenthal et al, 2003), we propose that extrinsic selection is more likely the cause of the majority of hybrid incompatibilities detected in this study

Summary

Introduction

Many hybridizing populations and species remain genetically and ecologically distinct despite bouts of past admixture (e.g., Scascitelli et al, 2010; Vonholdt et al, 2010). This has led to a surge of interest in identifying which and how many loci are important in maintaining species barriers. Recent work has focused on identifying so-called ‘genomic islands’ of high divergence between closely related species (e.g., Turner et al, 2005; Nadeau et al, 2012) This approach assumes that the most diverged regions between species are most likely to be under divergent selection between species or important in reproductive isolation. Divergence-based measures need to be interpreted with caution because they are susceptible to artifacts as a result of linked selection events (including background selection and hitchhiking) such that outlier regions might reflect low within-population polymorphism rather than unusually high divergence (discussed in Charlesworth, 1998; Noor and Bennett, 2009; Renaut et al, 2013), and there are many possible causes of elevated divergence that are not linked to isolation between species

Methods

Results

Discussion

Conclusion