The Genomic Architecture of Population Divergence between Subspecies of the European Rabbit

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.

Targeted capture in evolutionary and ecological genomics

“…Although targeted capture has primarily been applied to protein-coding exons (Hodges et al 2007), regulatory regions such as UTR, miRNA, promoter regions, and other non-coding elements can also be targeted in a highly parallel fashion (Bainbridge et al 2011; Hebert et al 2013; Linnen et al 2013; Carneiro et al 2014a; Carneiro et al 2014b; Schiessl et al 2014). In addition, non-coding regions flanking exons and other baited regions are often indirectly targeted (Samuels et al 2013).…”

“…Across different capture studies, loci with intermediate GC-content are often most highly represented (45%, Tewhey et al 2009a; 53%, Saintenac et al 2011; 55%, Ávila-Arcos et al 2011) because these loci amplify well and hybridize most efficiently to probes (Sims et al 2014). Introns and intergenic regions often contain a higher frequency of repetitive elements (Tewhey et al 2009a), however non-coding capture probes can avoid annotated repetitive DNA (Carneiro et al 2014a). An increasing number of studies are including non-coding regions in their capture designs, however the potential costs associated with capturing these regions should be considered when designing a capture.…”

“…Finally, targeted capture is easily scalable from hundreds (Smadja et al 2012) to hundreds of thousands of genomic regions (Hodges et al 2007; Yi et al 2010) and can include both coding and linked non-coding regions (Bainbridge et al 2011; Hebert et al 2013; Carneiro et al 2014a; Carneiro et al 2014b; Schiessl et al 2014). Non-coding capture data sets (e.g., introns, intergenic regions) can serve as appropriate null models of genomic variation for inferring selective sweeps within the genome (e.g., Carneiro et al 2014b) or regions of elevated differentiation between species (e.g., Carneiro et al 2014a).…”

Genomic insights into adaptive divergence and speciation among malaria vectors of theAnopheles niligroup

“…Understanding the genomic architecture of reproductive isolation may reveal crucial information on the sequence of events that occur from the initial stages of divergence among populations to the onset of strong reproductive barriers between species (e.g., Turner et al, 2005;Harr, 2006;Nadeau et al, 2012;Ellegren et al, 2012;Carneiro et al, 2014;Burri et al, 2015). One influential concept of speciation coined the "genic view of species" proposes that boundaries between species are properties of individual genes or genome regions and not of whole organisms or lineages (Barton & Hewitt, 1985;Harrison, 1990;Key, 1968;Nosil & Feder, 2012;Rieseberg, Whitton, & Gardner, 1999;Wu, 2001).…”

mtDNA diversity in a rabbit population from Sicily (Italy)

“…At the end of the last glaciation the geographical distribution of this species was limited to the Iberian Peninsula (IP) and probably the south of France (SF) (Kaetzke et al, 2003;Lopez-Martinez, 2008), where there were likely two glacial refugia; thus, as a consequence, two divergent genetic lineages evolved. The signatures of this are evident throughout the genome and can be observed in the analysis of allozyme variation, mtDNA variation, the Y-chromosome, the X-chromosome, and autosomes (Branco et al, 2000;Geraldes et al, 2006Geraldes et al, , 2008Ferrand and Branco, 2007;Carneiro et al, 2010Carneiro et al, , 2014aCarneiro et al, , 2014b. The European rabbit is recognized formally in two subspecies, O. c. cuniculus (L., 1758) andO.…”