Sex bias and dosage compensation in the zebra finch versus chicken genomes: General and specialized patterns among birds

Abstract

We compared global patterns of gene expression between two bird species, the chicken and zebra finch, with regard to sex bias of autosomal versus Z chromosome genes, dosage compensation, and evolution of sex bias. Both species appear to lack a Z chromosome–wide mechanism of dosage compensation, because both have a similar pattern of significantly higher expression of Z genes in males relative to females. Unlike the chicken Z chromosome, which has female-specific expression of the noncoding RNA MHM (male hypermethylated) and acetylation of histone 4 lysine 16 (H4K16) near MHM, the zebra finch Z chromosome appears to lack the MHM sequence and acetylation of H4K16. The zebra finch also does not show the reduced male-to-female (M:F) ratio of gene expression near MHM similar to that found in the chicken. Although the M:F ratios of Z chromosome gene expression are similar across tissues and ages within each species, they differ between the two species. Z genes showing the greatest species difference in M:F ratio were concentrated near the MHM region of the chicken Z chromosome. This study shows that the zebra finch differs from the chicken because it lacks a specialized region of greater dosage compensation along the Z chromosome, and shows other differences in sex bias. These patterns suggest that different avian taxa may have evolved specific compensatory mechanisms.

Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle

“…This result suggests a compensatory mechanism working through upregulation of female genes (Supplementary Fig. 23), as has also been noted previously in birds and silkworm 42,43 . …”

“…Our finding of the same compensation mechanisms for the relatively young sex chromosomes of tongue sole provides support for this hypothesis. However, although the dosage sensitivity of specific sets of Z-chromosome genes is evolutionarily conserved between zebrafinch and chicken, the compensated Z-chromosome genes in tongue sole are not the same as those in birds ( Supplementary Tables 32-39) 42 .…”

Impact of experience-dependent and -independent factors on gene expression in songbird brain

“…The comparatively limited effect of sex is interesting, given the chromosomal differences between the sexes and the absence of robust dosage compensation in birds (30,31). In the one experiment where sex was an explicit contrast (e04), we detected 652 significant differences after Bonferroni correction, or 1,192 using the criterion of raw P < 0.001.…”

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

“…Outside mammals, sex chromosomes have evolved independently many times, but chromosome-wide dosage compensation between sexes is not universal (8,32). For example, in birds, which have ZZ males and ZW females, expression levels of most Z-linked genes are substantially higher in males than in females (36,37). With our demonstration of a lack of chromosome-wide up-regulation of X-linked genes in mammals and the recent findings of no or incomplete between-sex dosage compensation in many nonmammalian organisms (8,32), the study of dosage compensation in sex chromosome evolution enters a new era in which new models and theories are urgently needed.…”