Speciation, Adaptation and Domestication: An Evolutionary Genomics History of the Equine Lineage

Equids are richly represented in the fossil record throughout the last 55 myr and have provided one of the most famous textbook examples of macroevolution. Although this group once flourished into several dozen of genera, it also experienced dramatic extinction events as contemporary equids only consist of a handful of species, all belonging to a single genus, Equus. The first undisputed Equus member appeared in the fossil record ca. 2 myr ago. By sequencing the genome of a ca. 700 kyr horse genome, which represents the oldest genome characterized so far, we recently showed that the history of Equus was as much as twice as long, with a most recent common ancestor of donkeys and horses living 4.0-4.5 myr ago. Using comparative genomics, we further identified over 20 millions high-quality SNPs segregating within living members of Equus. This information provides a large series of Ancestry Informative Markers for conservation genomic approaches, which is of critical importance for a group that contains no less than 5 endangered species: the Somali wild donkeys, Przewalski’s horses, Asiatic wild asses, and Mountain and Grevy’s zebras. Our genomic dataset revealed a highly dynamic demographic history, punctuated by severe expansions and declines in phase with major climatic changes. It also illuminated the genetic make-up of each species, revealing specific genetic adaptations along the different branches of the equine tree. Using phylogenomics, we timed the series of speciations that radiated into caballine horses and non-caballine zebras, donkeys and asses. Our analyses support a complex speciation history in equids first associated with gene flow during the divergence of caballine and non-caballine lineages and then followed by allopatric divergence in other lineages. At a more recent time scale, the domestication of equids has also played a critical role in human history, with domestic horses facilitating the exploration of novel territories and the expansion of continental-scale nomad empires. Using ancient DNA approaches, we have reconstructed the genomes of ancient horses predating the beginning of the domestication process. Comparisons to modern genomes from a variety of domestic breeds have revealed which genetic pathways have been under selective pressure in the process of horse domestication.