Emergence of male-biased genes on the chicken Z-chromosome: Sex-chromosome contrasts between male and female heterogametic systems: Figure 1.

Abstract

There has been extensive traffic of male-biased genes out of the mammalian and Drosophila X-chromosomes, and there are also reports of an under-representation of male-biased genes on the X. This may reflect an adaptive process driven by natural selection where an autosomal location of male-biased genes is favored since male genes are only exposed to selection one-third of the time when X-linked. However, there are several alternative explanations to ''out-of-the-X'' gene movement, including mutational bias and a means for X-linked genes to escape meiotic sex chromosome inactivation (MSCI) during spermatogenesis. As a critical test of the hypothesis that genomic relocation of sex-biased genes is an adaptive process, I examined the emergence, and loss, of genes on the chicken Z-chromosome, i.e., a female heterogametic system (males ZZ, females ZW ). Here, the analogous prediction would be an emergence of male-biased genes onto, not a loss from, the Z-chromosome because Z is found more often in males than autosomes are. I found that genes expressed in testis but not in ovary are highly over-represented among genes that have emerged on the Z-chromosome during avian evolution. Moreover, genes with male-biased expression are similarly over-represented among new Z-chromosomal genes. Interestingly, genes with female-biased expression have more often moved from than to the Z-chromosome. These observations show that male and female heterogametic organisms display opposing directionalities in the emergence and loss of sex-biased genes on sex chromosomes. This is consistent with theoretical models on the evolution of sexually antagonistic genes in which new mutations are at least partly dominant.

Trade-off Between Selection for Dosage Compensation and Masculinization on the Avian Z Chromosome

“…The older strata have been subjected to longer periods of stronger selection for dominant male-benefit alleles, and hence show a greater degree of masculinization. This finding is consistent with theoretical predictions and a recent study showing that genes expressed in the testis are overrepresented among newly emerged Z-linked genes (Ellegren 2011). The results can also explain previous findings that the extent of sex-biased expression varies across the Z chromosome (Melamed and Arnold 2007).…”

“…However, it has not been clear from previous work in birds how much of the male bias on the Z chromosome is due to masculinization (Ellegren 2011) and how much to incomplete dosage compensation Itoh et al 2007). Previous attempts to circumvent the problems of gene dose compared embryonic and adult gene expression levels (Mank and Ellegren 2009b); however, this did not account for the fact that sex-specific selection and sex-biased gene expression shift rapidly throughout development and the adult life cycle (Mank et al 2010).…”

Expression reduction in mammalian X chromosome evolution refutes Ohno’s hypothesis of dosage compensation

“…Indeed, we found a dozen of human autosomal genes that have chicken orthologs residing in the chromosome blocks orthologous to X (Figs. S10 and S11), although gene traffic need not arise from the pressure for dosage balance (33,34). This said, expression doubling to avoid haploinsufficiency appears to have occurred in ∼5% of X-linked genes that encode members of large protein complexes and was also demonstrated previously in one X-linked gene that was relocated from an autosome (35).…”

Problems of Birds Sex Determination

“…There are two Z chromosomes in males, while females have got Z and W chromosomes, therefore heterogametic sex is female. This type of definition of sex exists in many species of fishes, reptiles, amphibians, crustaceans and birds [1]. Known case of the presence of two systems of sex determination is XX/XY and ZZ/ZW within a species in the frog Rana raposa [2].…”

“…The chicken Z chromosome is about 80 Mb and is highly conserved among avian. The Z harbors over 1000 genes [1] [4]. W chromosome has got approximately 44 Mb of repeats and about 10 Mb of unique DNA, which may contain up to 20 active genes (Figure 1).…”