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.equids | evolutionary genomics | speciation | admixture | chromosomal rearrangements

Fast, Accurate and Automatic Ancient Nucleosome and Methylation Maps with epiPALEOMIX

“…Insert length, GC-content (%GC) and repeats represent well-known factors affecting read depth variation along the genome (Benjamini and Speed 2012; Jónsson et al 2014), potentially conflicting with our nucleosome calling procedure. To assess whether nucleosome calls were robust to such biases, we restricted nucleosome calls to uniquely mappable genomic regions, which were defined following the procedure described in Jonsson et al (2014), where we computed the sequence mappability within 20-kb genomic blocks using a 41-mers (Derrien et al 2012) and restricted nucleosome calls to blocks showing mappability uniqueness ≥ 0.9.…”

Impact of Karyotype Organization on Interlocus Recombination between T Cell Receptor Genes in Equidae

“…No data on the TCR gene structure in asses and zebras are available. As equids diverged quite recently [Steiner and Ryder, 2011;Jónsson et al, 2014], we presume that they share a similar structure of the TCR genes. However, the impact of gene complexity on the number of trans-rearrangements cannot be completely ruled out.…”

“…It has been estimated by Steiner and Ryder [2011] that horses diverged from other equids ∼ 3.8 Mya, prior to the split of zebras and asses ∼ 1.69-1.9 Mya [Jónsson et al, 2014]. African and Asiatic asses diverged ∼ 1.47-1.75 Mya, and Hartmann's zebra became a sister taxon of Burchell's zebra and Grevy's zebra ∼ 1.28-1.59 Mya [Jónsson et al, 2014]. Despite the close relationship among equids, we observed differences in the frequencies of illegitimate recombination between the TCR loci.…”

“…The phylogeny of this genus has been extensively studied [Steiner and Ryder, 2011;Jónsson et al, 2014], and although equids diverged quite recently, their karyotypes differ widely due to their rapid evolution [Musilova et al, 2013].…”

Maintaining genetic integrity of coexisting wild and domestic populations: Genetic differentiation between wild and domestic Rangifer with long traditions of intentional interbreeding

“…However, new models of domestication suggest that while spatial separation of wild and domestic types is often sought, various domestic species ranging from pigs to horses have also been cross‐bred for specific characteristics by allowing controlled introgression from wild herds. (Ottoni, 2013; Jónsson, 2014; Frantz, 2015). For most domestic breeds, this idea remains a hypothesis as the original free‐ranging wild forms have become largely extinct or restricted to a few isolated areas (Clutton‐Brock, 1987).…”