Abstract
The analysis of introgression of genomic regions between divergent populations provides an excellent opportunity to determine the genetic basis of reproductive isolation during the early stages of speciation. However, hybridization and subsequent gene flow must be relatively common in order to localize individual loci that resist introgression. In this study, we used next-generation sequencing to study genome-wide patterns of genetic differentiation between two hybridizing subspecies of rabbits (Oryctolagus cuniculus algirus and O. c. cuniculus) that are known to undergo high rates of gene exchange. Our primary objective was to identify specific genes or genomic regions that have resisted introgression and are likely to confer reproductive barriers in natural conditions. On the basis of 326,000 polymorphisms, we found low to moderate overall levels of differentiation between subspecies, and fewer than 200 genomic regions dispersed throughout the genome showing high differentiation consistent with a signature of reduced gene flow. Most differentiated regions were smaller than 200 Kb and contained very few genes. Remarkably, 30 regions were each found to contain a single gene, facilitating the identification of candidate genes underlying reproductive isolation. This gene-level resolution yielded several insights into the genetic basis and architecture of reproductive isolation in rabbits. Regions of high differentiation were enriched on the X-chromosome and near centromeres. Genes lying within differentiated regions were often associated with transcription and epigenetic activities, including chromatin organization, regulation of transcription, and DNA binding. Overall, our results from a naturally hybridizing system share important commonalities with hybrid incompatibility genes identified using laboratory crosses in mice and flies, highlighting general mechanisms underlying the maintenance of reproductive barriers.
Highlights
Most research into the genetic underpinnings of speciation is based on laboratory studies of specific reproductively isolating phenotypes [1,2]
Consistent with variable levels of introgression playing a substantial role in determining patterns of genomic differentiation, we found a significant increase in mean relative node depth (RND) values for fragments residing within regions of differentiation defined both using the Z-score or the proportion of fixed differences versus shared polymorphisms (P,0.05 for all comparisons; Figure 3)
Our results indicate that both FST (i.e. Z-score) and the ratio of shared polymorphisms to fixed differences are capturing signatures of reduced gene flow and that regions of high differentiation indentified in our study are likely to be enriched for regions involved in reproductive barriers
Summary
Most research into the genetic underpinnings of speciation is based on laboratory studies of specific reproductively isolating phenotypes [1,2]. A small number of these studies have identified individual genes that confer lower fitness when in a foreign or admixed genetic background [3,4,5,6] It is not clear whether these genes and corresponding phenotypes - often identified in crosses between highly divergent species pairs - were ever relevant to restricting gene flow in nature, or whether they represent an inevitable byproduct of functional divergence between species [1,7]. The direct analysis of naturally hybridizing populations provides an alternative and arguably more direct way to study the genetic basis of reproductive isolation [8] This approach assures relevance to the early stages of speciation and allows the fitness of hybrid genotypes to be evaluated under natural conditions [9,10]. It is well established that genomic regions harboring hybrid incompatibilities are expected to display low levels of introgression, whereas regions not harboring incompat-
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