title: Speciation with gene flow in equids despite extensive chromosomal plasticity.
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.
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, DK-1350 Copenhagen K, Denmark;
authors.forename: Hákon
authors.initials: H
authors.lastname: Jónsson
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, DK-1350 Copenhagen K, Denmark;
authors.forename: Mikkel
authors.identifier: http://orcid.org/0000-0003-2401-9921
authors.initials: M
authors.lastname: Schubert
authors.affiliation: 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;
authors.forename: Andaine
authors.initials: A
authors.lastname: Seguin-Orlando
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, DK-1350 Copenhagen K, Denmark;
authors.forename: Aurélien
authors.initials: A
authors.lastname: Ginolhac
authors.affiliation: National High-Throughput DNA Sequencing Center, DK-1353 Copenhagen K, Denmark;
authors.forename: Lillian
authors.initials: L
authors.lastname: Petersen
authors.affiliation: 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;
authors.forename: Matteo
authors.initials: M
authors.lastname: Fumagalli
authors.affiliation: The Bioinformatics Centre, Department of Biology, University of Copenhagen, DK-2200 Copenhagen N, Denmark;
authors.forename: Anders
authors.initials: A
authors.lastname: Albrechtsen
authors.affiliation: Centre for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark, DK-2800 Lyngby, Denmark;
authors.forename: Bent
authors.initials: B
authors.lastname: Petersen
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, DK-1350 Copenhagen K, Denmark;
authors.forename: Thorfinn S
authors.identifier: http://orcid.org/0000-0001-7576-5380
authors.initials: TS
authors.lastname: Korneliussen
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, DK-1350 Copenhagen K, Denmark;
authors.forename: Julia T
authors.initials: JT
authors.lastname: Vilstrup
authors.affiliation: Maxwell H. Gluck Equine Research Center, Veterinary Science Department, University of Kentucky, Lexington, KY 40546;
authors.forename: Teri
authors.initials: T
authors.lastname: Lear
authors.affiliation: Maxwell H. Gluck Equine Research Center, Veterinary Science Department, University of Kentucky, Lexington, KY 40546;
authors.forename: Jennifer Leigh
authors.initials: JL
authors.lastname: Myka
authors.affiliation: Maxwell H. Gluck Equine Research Center, Veterinary Science Department, University of Kentucky, Lexington, KY 40546;
authors.forename: Judith
authors.initials: J
authors.lastname: Lundquist
authors.affiliation: Baker Institute for Animal Health, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853;
authors.forename: Donald C
authors.initials: DC
authors.lastname: Miller
authors.affiliation: Zoology Department, College of Science, King Saud University, Riyadh 11451, Saudi Arabia;
authors.forename: Ahmed H
authors.initials: AH
authors.lastname: Alfarhan
authors.affiliation: Zoology Department, College of Science, King Saud University, Riyadh 11451, Saudi Arabia;
authors.forename: Saleh A
authors.initials: SA
authors.lastname: Alquraishi
authors.affiliation: Zoology Department, College of Science, King Saud University, Riyadh 11451, Saudi Arabia;
authors.forename: Khaled A S
authors.initials: KA
authors.lastname: Al-Rasheid
authors.affiliation: Ree Park, Ebeltoft Safari, DK-8400 Ebeltoft, Denmark;
authors.forename: Julia
authors.initials: J
authors.lastname: Stagegaard
authors.affiliation: Tierpark Berlin-Friedrichsfelde, 10319 Berlin, Germany; and.
authors.forename: Günter
authors.initials: G
authors.lastname: Strauss
authors.affiliation: Centre for Zoo and Wild Animal Health, Copenhagen Zoo, DK-2000 Frederiksberg, Denmark.
authors.forename: Mads Frost
authors.initials: MF
authors.lastname: Bertelsen
authors.affiliation: Centre for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark, DK-2800 Lyngby, Denmark;
authors.forename: Thomas
authors.identifier: http://orcid.org/0000-0001-6615-1141
authors.initials: T
authors.lastname: Sicheritz-Ponten
authors.affiliation: Baker Institute for Animal Health, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853;
authors.forename: Douglas F
authors.initials: DF
authors.lastname: Antczak
authors.affiliation: Maxwell H. Gluck Equine Research Center, Veterinary Science Department, University of Kentucky, Lexington, KY 40546;
authors.forename: Ernest
authors.initials: E
authors.lastname: Bailey
authors.affiliation: Department of Integrative Biology, University of California, Berkeley, CA 94720;
authors.forename: Rasmus
authors.initials: R
authors.lastname: Nielsen
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, DK-1350 Copenhagen K, Denmark;
authors.forename: Eske
authors.initials: E
authors.lastname: Willerslev
authors.affiliation: Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, DK-1350 Copenhagen K, Denmark; Lorlando@snm.ku.dk.
authors.forename: Ludovic
authors.initials: L
authors.lastname: Orlando
mesh_terms: D000349:Africa; D000818:Animals; D033481:Chromosomes, Mammalian / Q000235:genetics*; D018397:Equidae / Q000235:genetics*; D019143:Evolution, Molecular; D053476:Extinction, Biological; D051456:Gene Flow; D009656:North America
keywords: admixture; chromosomal rearrangements; equids; evolutionary genomics; speciation