A molecular cytogenetic analysis of X chromosome repatterning in the Bovidae: transpositions, inversions, and phylogenetic inference

Abstract

Chromosomal homologies among the X chromosomes of species representative of eight bovid subfamilies and most of the recognized tribes were established using a combination of FISH and conventional G- and C-banding. Our analyses allowed for the delimitation of three X chromosome types represented, respectively, by cattle (Bovinae, tribe Bovini), the tragelaphines (Bovinae, tribe Tragelaphini), and a large assemblage comprising all the remaining subfamilies and their tribes (the Cephalophinae, Hippotraginae, Alcelaphinae, Antilopinae, Aepycerotinae, Peleinae, and Caprinae). The use of the bacterial artificial chromosome probe BAC 101 (which maps to Xp12 in cattle) and an Xp painting probe comprising sequences specific for the short arm of cattle Xp (Xp24→p12) allowed us to orient this region, which has moved as a conserved euchromatic block during the evolution of the bovid X chromosome. We show that the differences between the three chromosomal types are attributable to a transposition, two inversions, and heterochromatic additions/deletions. A paucity of comparative mapping data precludes the assignment of the sequences contained in cattle Xp to either the presumed conserved (XCR) or the recently added (XAR) region of the eutherian X chromosome, and the reasons for the retention of these sequences as an evolutionarily conserved unit in the intrachromosomal restructuring of the bovid X across lineages remain enigmatic.

Comparative Analysis (Hippotragini versus Caprini, Bovidae) of X-Chromosome's Constitutive Heterochromatin by in situ Restriction Endonuclease Digestion: X-Chromosome Constitutive Heterochromatin Evolution

“…These results are in accordance with previous ones, which described CH addition or elimination, during the Bovidae X-chromosome rearrangements (e.g. centromeric transpositions) (Piumi et al, 1998;Robinson et al, 1998;Gallagher et al, 1999;Iannuzzi et al, 2000). However, the data cited before was obtained with the comparison between diff erent morphological X-chromosomes (metacentric, submetacentric and acrocentric) where X-chromosome rearrangements are obvious, and some of that rearrangements were consistently confirmed with microdissected paints or BAC probes.…”

“…The X-chromosome variation is mostly a consequence of CH variation; in what respect to its amount and position (Robinson et al, 1998;Gallagher et al,1999). This is especially common among the non-Bovinae subfamilies and tribes (Robinson et al,1998;Gallagher et al, 1999).…”

“…The X-chromosome variation is mostly a consequence of CH variation; in what respect to its amount and position (Robinson et al, 1998;Gallagher et al,1999). This is especially common among the non-Bovinae subfamilies and tribes (Robinson et al,1998;Gallagher et al, 1999). In order to characterize the X-chromosome CH in non-Bovinae species (Hippotragini and Caprini tribes) we applied the technique discussed above: in situ RE digestion (with a panel of seven different REs) on fixed chromosomes and sequential C-banding (Figure 2 and Table 1).…”

“…In contrast to the preservative autosomal conservatism evident in the Bovidae, the X-chromosome is reported to show considerable variation between subfamilies, and often between tribes within subfamilies (Buckland & Evans, 1978b;Gallagher & Womack, 1992). The Xchromosome variation in the bovids is due to disruption of euchromatic regions, centromere placement, heterochromatic variation, and autosomal translocation (Robinson et al, 1998;Gallagher et al, 1999;Iannuzzi et al, 2000). Several studies have been done to delineate the structural rearrangements that characterized the evolution of bovid X-chromosome and to determine the primitive and ancestral condition of Bovidae X-chromosome.…”

“…Chromosomal change in the Bovidae has occurred primarily through centric fusion (Wurster & Benirschke, 1968;Effron et al, 1976;Buckland & Evans, 1978a;Gallagher & Womack, 1992;Gallagher, Derr & Womack, 1994). Although there is good evidence of tandem rearrangements in some species (Gallagher & Womack, 1992) and paracentric inversions in others (Hayes, Petit & Dutrillaux,1991;Robinson et al, 1998), these seem to be the exception rather than the rule. In contrast to the preservative autosomal conservatism evident in the Bovidae, the X-chromosome is reported to show considerable variation between subfamilies, and often between tribes within subfamilies (Buckland & Evans, 1978b;Gallagher & Womack, 1992).…”