X Chromosome Evolution in Cetartiodactyla

Abstract

The phenomenon of a remarkable conservation of the X chromosome in eutherian mammals has been first described by Susumu Ohno in 1964. A notable exception is the cetartiodactyl X chromosome, which varies widely in morphology and G-banding pattern between species. It is hypothesized that this sex chromosome has undergone multiple rearrangements that changed the centromere position and the order of syntenic segments over the last 80 million years of Cetartiodactyla speciation. To investigate its evolution we have selected 26 evolutionarily conserved bacterial artificial chromosome (BAC) clones from the cattle CHORI-240 library evenly distributed along the cattle X chromosome. High-resolution BAC maps of the X chromosome on a representative range of cetartiodactyl species from different branches: pig (Suidae), alpaca (Camelidae), gray whale (Cetacea), hippopotamus (Hippopotamidae), Java mouse-deer (Tragulidae), pronghorn (Antilocapridae), Siberian musk deer (Moschidae), and giraffe (Giraffidae) were obtained by fluorescent in situ hybridization. To trace the X chromosome evolution during fast radiation in specious families, we performed mapping in several cervids (moose, Siberian roe deer, fallow deer, and Pere David’s deer) and bovid (muskox, goat, sheep, sable antelope, and cattle) species. We have identified three major conserved synteny blocks and rearrangements in different cetartiodactyl lineages and found that the recently described phenomenon of the evolutionary new centromere emergence has taken place in the X chromosome evolution of Cetartiodactyla at least five times. We propose the structure of the putative ancestral cetartiodactyl X chromosome by reconstructing the order of syntenic segments and centromere position for key groups.

Karyotype relationships among selected deer species and cattle revealed by bovine FISH probes

“…nippon and Odocoileus virginianus ), which are carriers of both X chromosome variants [ 27 , 33 ]. Recently, the structure of the X chromosome was described in four Cervidae species ( Capreolus pygargus , AAL, DDA and EDA) by high resolution BAC mapping [ 31 ]. Our hybridization data are mostly in agreement with the above mentioned papers and substantially extend knowledge concerning the structure of cervid X chromosomes.…”

“…Our hybridization data are mostly in agreement with the above mentioned papers and substantially extend knowledge concerning the structure of cervid X chromosomes. In addition, our selection of X BAC clones enabled us to detected not only four, but five synteny blocks on the X chromosome of DDA that were not previously revealed by other BAC mapping [ 31 ]. We observed the same structure of X chromosome with five synteny blocks in all six studied Cervinae species (DDA, CEL, EDA, CTR, REL and MRE).…”

“…Studies that describe the detailed structure and rearrangements of the X chromosome outside the family Bovidae were scarce and limited only to a few species from the Giraffidae, Cervidae, Antilocapridae and Hippopotamidae [ 19 , 20 , 27 ]. Recently, new investigation of the X chromosome structure in eighteen different Cetartiodactyla species using comparative BAC mapping appeared [ 31 ]. Taking into account all known structures of X chromosomes in different species, the acrocentric (Cervinae) variant is unique, whereas the submetacentric (Capreolinae) type is similar to the X chromosome of the giraffe and hippo (without regard to the centromere position).…”

“…Interspecies variation of X chromosome provides a rich source of phylogenetic information but detailed structure of chromosome X has not been studied in more detail in most Ruminantia species for some considerable time. Just recently, a new investigation of the X chromosome evolution in different representatives of Cetartiodactyla employing high resolution BAC mapping was published [ 31 ]. In Cervidae, comparative FISH with whole X chromosome painting probes was employed in several studies [ 10 , 12 , 32 ].…”

“…Comparative mapping of three X chromosome-specific bovine cosmids was employed in Rangifer tarandus gonosomes [ 33 ]. The results of another detailed study concerning conserved syntenies of the X chromosome in four Cervidae species are currently available [ 31 ].…”