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Proc Natl Acad Sci U S A. 2014 Dec 30;111(52):18655-60. doi: 10.1073/pnas.1412627111. Epub 2014 Dec 1.

Speciation with gene flow in equids despite extensive chromosomal plasticity.

Author information

1
Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, DK-1350 Copenhagen K, Denmark;
2
Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, DK-1350 Copenhagen K, Denmark; National High-Throughput DNA Sequencing Center, DK-1353 Copenhagen K, Denmark;
3
National High-Throughput DNA Sequencing Center, DK-1353 Copenhagen K, Denmark;
4
Department of Integrative Biology, University of California, Berkeley, CA 94720; UCL Genetics Institute, Department of Genetics, Evolution, and Environment, University College London, London WC1E 6BT, United Kingdom;
5
The Bioinformatics Centre, Department of Biology, University of Copenhagen, DK-2200 Copenhagen N, Denmark;
6
Centre for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark, DK-2800 Lyngby, Denmark;
7
Maxwell H. Gluck Equine Research Center, Veterinary Science Department, University of Kentucky, Lexington, KY 40546;
8
Baker Institute for Animal Health, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853;
9
Zoology Department, College of Science, King Saud University, Riyadh 11451, Saudi Arabia;
10
Ree Park, Ebeltoft Safari, DK-8400 Ebeltoft, Denmark;
11
Tierpark Berlin-Friedrichsfelde, 10319 Berlin, Germany; and.
12
Centre for Zoo and Wild Animal Health, Copenhagen Zoo, DK-2000 Frederiksberg, Denmark.
13
Department of Integrative Biology, University of California, Berkeley, CA 94720;
14
Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, DK-1350 Copenhagen K, Denmark; Lorlando@snm.ku.dk.

Abstract

Horses, asses, and zebras belong to a single genus, Equus, which emerged 4.0-4.5 Mya. Although the equine fossil record represents a textbook example of evolution, the succession of events that gave rise to the diversity of species existing today remains unclear. Here we present six genomes from each living species of asses and zebras. This completes the set of genomes available for all extant species in the genus, which was hitherto represented only by the horse and the domestic donkey. In addition, we used a museum specimen to characterize the genome of the quagga zebra, which was driven to extinction in the early 1900s. We scan the genomes for lineage-specific adaptations and identify 48 genes that have evolved under positive selection and are involved in olfaction, immune response, development, locomotion, and behavior. Our extensive genome dataset reveals a highly dynamic demographic history with synchronous expansions and collapses on different continents during the last 400 ky after major climatic events. We show that the earliest speciation occurred with gene flow in Northern America, and that the ancestor of present-day asses and zebras dispersed into the Old World 2.1-3.4 Mya. Strikingly, we also find evidence for gene flow involving three contemporary equine species despite chromosomal numbers varying from 16 pairs to 31 pairs. These findings challenge the claim that the accumulation of chromosomal rearrangements drive complete reproductive isolation, and promote equids as a fundamental model for understanding the interplay between chromosomal structure, gene flow, and, ultimately, speciation.

KEYWORDS:

admixture; chromosomal rearrangements; equids; evolutionary genomics; speciation

PMID:
25453089
PMCID:
PMC4284605
DOI:
10.1073/pnas.1412627111
[Indexed for MEDLINE]
Free PMC Article

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