Multidirectional cross-species painting illuminates the history of karyotypic evolution in Perissodactyla

Abstract

The order Perissodactyla, the group of odd-toed ungulates, includes three extant families: Equidae, Tapiridae, and Rhinocerotidae. The extremely rapid karyotypic diversification in perissodactyls has so far prevented the establishment of genome-wide homology maps between these three families by traditional cytogenetic approaches. Here we report the first genome-wide comparative chromosome maps of African rhinoceroses, four tapir species, four equine species, and humans. These maps were established by multidirectional chromosome painting, with paint probes derived from flow-sorted chromosomes of Equus grevyi, Tapirus indicus, and Ceratotherium simum as well as painting probes from horse and human. The Malayan tapir (Tapirus indicus), Baird's tapir (T. bairdii), mountain tapir (T. pinchaque), lowland tapir (T. terrestris), and onager (E. hemionus onager), were studied by cross-species chromosome painting for the first time. Our results, when integrated with previously published comparative chromosome maps of the other perissodactyl species, have enabled the reconstruction of perissodactyl, ceratomorph, and equid ancestral karyotypes, and the identification of the defining evolutionary chromosomal rearrangements along each lineage. Our results allow a more reliable estimate of the mode and tempo of evolutionary chromosomal rearrangements, revealing a striking switch between the slowly evolving ceratomorphs and extremely rapidly evolving equids.

Tracking the complex flow of chromosome rearrangements from the Hominoidea Ancestor to extant Hylobates and Nomascus Gibbons by high-resolution synteny mapping

“…The gibbon rates are at least a magnitude higher (10-20 times higher) and up to twice those found in the mouse (1.71-2.76) and the canine (2.1) lineages (Murphy et al 2005). Higher rates of evolution are only found in some gerbils (Dobigny et al 2005) and in the karyotypic evolution of onager, donkey, and zebras (Trifonov et al 2008).…”

Centromere repositioning in mammals

“…Carbone et al (2006) compared chromosomal marker order between Burchelli's zebra (Equus burchelli) and the donkey (Equus asinus), using the horse (Equus caballus) as an outgroup. Equidae, and these three species in particular, underwent a recent, rapid evolution and accumulated a large number of chromosomal changes (Trifonov et al, 2008). Zebra and donkey diverged about 0.9 MYA, while their common ancestor diverged from the horse around 2 MYA (Oakenfull and Clegg, 1998;Oakenfull et al, 2000).…”

Phylogeny of Horse Chromosome 5q in the Genus <i>Equus</i> and Centromere Repositioning

“…The Equus species shared a common ancestor about 2-3 MYa, and the extant species emerged very recently [Oakenfull and Clegg, 1998]. Although the phylogenetic relationships within the genus Equus have been investigated using morphological [Bennet, 1980;Harris and Porter, 1980], molecular [Lowenstein and Ryder, 1985;George and Ryder, 1986;Flint et al, 1990;Oakenfull and Clegg, 1998;Oakenfull et al, 2000] and cytogenetic [Trifonov et al, 2008] data, they are still a matter of debate. Perissodactyla have widely variable chromosome numbers with 2n = 32-66 in Equidae [Ryder et al, 1978], 2n = 52-80 in Tapiridae [Houck et al, 2000], and 2n = 82-84 in Rhinocerotidae [Wurster and Benirschke, 1968;Houck et al, 1994].…”

“…The karyotype of the extant species of Ceratomorpha is characterized by mostly acrocentric elements; this arrangement is believed to correspond to the Perissodactyl ancestral karyotype [Trifonov et al, 2008]. On the other hand, equid species display variable numbers of meta-and submetacentric chromosomes that presumably arose by fusion of ancestral acrocentric elements.…”