Evolutionary Genomics of Equine Species: A History of Adaptation, Gene Flow, and Expansion out of the Americas

The evolutionary history of the horse family is well known thanks to an extremely rich fossil record and represents a textbook example of evolution. However, little is known about the radiation which resulted in the present diversity of horses, asses and zebras, and the emergence of the genus Equus within the last 4-4.5 million years. Here, we complete the whole-genome characterization of all extant equine species by sequencing the genomes of each living species of asses and zebras.  We also sequenced the genome of a recently extinct variant of the plains zebra, the Quagga. Our extensive dataset, allowed us to scan for lineage specific adaptations, resulting in list of 48 positively selected genes involved in in olfaction, development, locomotion and behavior. Furthermore, the whole-genome sequences illuminated a complex population history across species, revealing an extremely dynamic demography in the last 400 thousand years, with synchronous population sizes changes in different continents in line with major climate events. Surprisingly, we discover that equine speciation is generally characterized by gene-flow, starting with the divergence of asses and zebras from the horses in the New World 4.0-4.5 mya, which lasted for 2 million years until the former dispersed into the Old World 2.1-3.4 mya. Strikingly, we find evidence for ancestral gene-flow involving three contemporary equine species with extremely divergent karyotypes. This challenges the role of karyotype plasticity as the driver behind complete reproductive isolation, promoting equids as an exciting scientific avenue to investigate the complex relationship of chromosomal rearrangements, gene-flow and, ultimately, speciation.