Evolution of the avian sex chromosomes from an ancestral pair of autosomes

Abstract

Among the mechanisms whereby sex is determined in animals, chromosomal sex determination is found in a wide variety of distant taxa. The widespread but not ubiquitous occurrence, not even within lineages, of chromosomal sex determination suggests that sex chromosomes have evolved independently several times during animal radiation, but firm evidence for this is lacking. The most favored model for this process is gradual differentiation of ancestral pairs of autosomes. As known for mammals, sex chromosomes may have a very ancient origin, and it has even been speculated that the sex chromosomes of mammals and birds would share a common chromosomal ancestry. In this study we showed that the two genes, ATP5A1 and CHD1, so far assigned to the female-specific W chromosome of birds both exist in a very closely related copy on the Z chromosome but are not pseudoautosomal. This indicates a common ancestry of the two sex chromosomes, consistent with the evolution from a pair of autosomes. Comparative mapping demonstrates, however, that ATP5A1 and CHD1 are not sex-linked among eutherian mammals; this is also not the case for the majority of other genes so far assigned to the avian Z chromosome. Our results suggest that the evolution of sex chromosomes has occurred independently in mammals and birds.

Figure 1

An HindIII RFLP in the chicken CHD1Z gene demonstrating Z chromosome linkage JF, Jungle Fowl; WL, White Leghorn.

Figure 2

Fig. 2. FISH localization of the chicken CHD1Z (a) and ATP5A1Z (b) genes. (Left) Hybridization signal. (Right) 4′,6-Diamidino-2-phenylindole-banding pattern (in black and white) of the corresponding metaphases.

Figure 3

A summary of genetic, physical, and comparative map data for the chicken Z and W chromosomes. Note that the orientation of the W chromosome is not known; the signals of CHD1W and ATP5A1W are both from one of the chromosome ends. The location of Z chromosome genes have been drawn to scale according to the recombination distances separating them in the linkage map derived from the East Lansing reference population. A large number of anonymous markers placed between the genes are not included in the figure. Also note that the OTC gene has not been genetically mapped in chickens. The curved lines next to the ALDOB–GGTB2–IREB1 linkage groups in mice and cattle indicate rearranged gene orders.

Figure 4

A tree depicting the phylogenetic relationship among chicken CHD1Z, chicken CHD1W, ostrich, human, and murine CHD1 gene. Figures indicate bootstrap support for branches (1,000 replicates). The total tree length was 242 steps, the consistency index = 0.781, the retention index = 0.701, and the homeoplasy index = 0.219.