Speciation with gene flow in equids despite extensive chromosomal plasticity

• Published in: Proceedings of the National Academy of Sciences - PNAS 2014-12, Vol.111 (52), p.18655-18660
• Main Authors: Jónsson, Hákon, Schubert, Mikkel, Seguin-Orlando, Andaine, Ginolhac, Aurélien, Petersen, Lillian, Fumagalli, Matteo, Albrechtsen, Anders, Petersen, Bent, Korneliussen, Thorfinn S., Vilstrup, Julia T., Lear, Teri, Myka, Jennifer Leigh, Lundquist, Judith, Miller, Donald C., Alfarhan, Ahmed H., Alquraishi, Saleh A., Al-Rasheid, Khaled A. S., Stagegaard, Julia, Strauss, Günter, Bertelsen, Mads Frost, Sicheritz-Ponten, Thomas, Antczak, Douglas F., Bailey, Ernest, Nielsen, Rasmus, Willerslev, Eske, Orlando, Ludovic
• Format: Article
• Language: English
• Subjects: Admixtures; Africa; Animal behavior; Animals; Biological Sciences; Chromosomes; Chromosomes, Mammalian - genetics; Demographics; Equidae - genetics; Equus; Evolution; Evolution, Molecular; Extinct species; Extinction; Extinction, Biological; Gene Flow; Genomes; Horses; North America; Speciation; Species extinction; Zebras
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1412627111

Significance Thirty years after the first DNA fragment from the extinct quagga zebra was sequenced, we set another milestone in equine genomics by sequencing its entire genome, along with the genomes of the surviving equine species. This extensive dataset allows us to decipher the genetic makeup underlying lineage-specific adaptations and reveal the complex history of equine speciation. We find that Equus first diverged in the New World, spread across the Old World 2.1–3.4 Mya, and finally experienced major demographic expansions and collapses coinciding with past climate changes. Strikingly, we find multiple instances of hybridization throughout the equine tree, despite extremely divergent chromosomal structures. This contrasts with theories promoting chromosomal incompatibilities as drivers for the origin of equine species. 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.