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.

Sex determination: the amphibian models

“…Moreover there is no information about sex chromosomes, especially heteromorphism, in Caecilians, one of the three amphibian orders [3]. In fact, there is currently no evidence that following the example of birds [22], the various amphibian sex chromosomes are derived from one or more ancestral autosome pairs.…”

Disruption of FEM1C-W gene in zebra finch: evolutionary insights on avian ZW genes

“…The ancestral chromosomes of avian sex chromosomes are different from those of eutherian mammals and snakes (Fridolfsson et al 1998;Nanda et al 1999;Matsubara et al 2006), although recent evidence indicates surprising shared gene content of the avian Z and monotreme X chromosomes (Rens et al 2007). The gene content of the Z chromosome appears to have changed little during avian evolution, as shown by comparative painting analysis (Itoh and Arnold 2005;Nishida-Umehara et al 2007;Tsuda et al 2007), even in Ratites (Struthioniformes) which are considered to be an ancestral avian species whose sex chromosomes are morphologically relatively undifferentiated (Ogawa et al 1998;Shetty et al 1999).…”

W chromosome expression responds to female-specific selection

“…In birds, both the Z and the W chromosomes descend from a shared autosomal precursor that was present in the common ancestor of all modern birds (12)(13)(14); however, as recombination between the sex chromosomes was curtailed over the course of >120 million years, the W chromosome has degenerated both in size and gene number compared with the Z chromosome (15)(16)(17). Theoretically, the genes that have remained on or that have transferred to the W chromosome should play a disproportionately large role in determining female phenotypes, and varying female-specific selection should strongly affect the evolution of the W chromosome.…”