The Genomic Architecture of Population Divergence between Subspecies of the European Rabbit
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Author
Carneiro, Miguel
Albert, Frank W.
Afonso, Sandra
Pereira, Ricardo J.
Burbano, Hernán
Campos, Rita
Melo-Ferreira, José
Blanco-Aguiar, José A.
Villafuerte, Rafael
Nachman, Michael W.
Good, Jeffrey M.
Ferrand, Nuno
Publisher
Public Library of Science (PLOS)Date
2014Subject
DNA-binding proteinsRabbits
Introgression
Antiport proteins
Cytoskeletal proteins
Transcription factors
Gene flow
X chromosomes
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Show full item recordAbstract
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.