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.

Keywords: Pecora; Ruminantia; cattle bacterial artificial chromosome (BAC) clones; centromere reposition; fluorescent in situ hybridization (FISH); intrachromosomal rearrangements; inversion.

Figure 1

Centromere location (cen, white line) and positions of specific BAC clones (pink and green) on X chromosome of several cetartiodactyl species. Species three-letter codes are listed in Table 1.

Figure 2

The scheme of evolutionary transformations of X chromosome in Cetartiodactyla. Chromosome rearrangements were identified by changes in BAC order. Three major conservative segments are designated by different colors: pink—X syntenic block 1; yellow—X syntenic block 2, and; blue—X syntenic block 3. Individual BAC clones are shown with a different color in small colored circles on corresponding conservative segment. Centromere position is indicated by a black circle. The orientation of the conservative segments is indicated by the white arrowhead. Ancestral associations are shown in black rectangle (Cetartiodactyla ancestral X (CAX), Ruminantia ancestral X (RAX), Pecora ancestral X (PAX), Antilopinae ancestral X (AAX), Cervinae ancestral X (CEAX)). CR: centromere reposition. Inv: inversion.

Figure 3

The structure of the Cetartiodactyla X chromosome depicted on the phylogenetic tree of the order (the tree topology from [47]) Major conservative segments are shown by yellow, blue, and pink. Centromere positions are designated by a black circle. White arrowheads show the orientation of the conservative segments. Ancestral associations are shown under X chromosomes (Cetartiodactyla ancestral X (CAX), Ruminantia ancestral X (RAX), Pecora ancestral X (PAX), Antilopinae ancestral X (AAX). MMO X chromosome is inverted here relatively to its cytogenetic orientation for presentation purposes [8].