Avian W and mammalian Y chromosomes convergently retained dosage-sensitive regulators

Abstract

After birds diverged from mammals, different ancestral autosomes evolved into sex chromosomes in each lineage. In birds, females are ZW and males ZZ, but in mammals females are XX and males XY. We sequenced the chicken W chromosome, compared its gene content with our reconstruction of the ancestral autosomes, and followed the evolutionary trajectory of ancestral W-linked genes across birds. Avian W chromosomes evolved in parallel with mammalian Y chromosomes, preserving ancestral genes through selection to maintain the dosage of broadly-expressed regulators of key cellular processes. We propose that, like the human Y chromosome, the chicken W chromosome is essential for embryonic viability of the heterogametic sex. Unlike other sequenced sex chromosomes, the chicken W did not acquire and amplify genes specifically expressed in reproductive tissues. We speculate that the pressures that drive the acquisition of reproduction related genes on sex chromosomes may be specific to the male germ line.

Sex-biased microRNA expression in mammals and birds reveals underlying regulatory mechanisms and a role in dosage compensation

“…This miRNA therefore joins the highly select group of dosage-sensitive genes that were retained on the W Chromosome (Bellott et al 2017). We did however detect significant female bias for miR-122-5p in the chicken heart, which could be due to sex-specific control or may indicate slight regulatory diversification of the Z-linked and W-linked copies in this tissue.…”

“…In addition, remapping confirmed W linkage of the mir-7b locus (Ayers et al 2013), which belongs to a family with both Z-linked and autosomal members. Given that the chicken W Chromosome is thought to host only 28 protein-coding genes (Bellott et al 2017), miRNAs thus make up a sizable fraction of the total W-linked gene repertoire.…”

“…The need for dosage compensation arises during sex chromosome evolution when increasingly larger regions of the originally identical sex chromosomes cease to recombine, leading to the gradual decay of one member of the pair, e.g., the female W Chromosome in birds (Graves 2016). Although some genes, such as the mir-122 locus, are retained on the W Chromosome and therefore are present in equal numbers in males and females, the number of W-linked genes in chicken is vanishingly small (Bellott et al 2017) and most Z-linked genes are therefore present in a single copy in ZW females and double copies in ZZ males. The reduced gene dosage in ZW females, from two copies prior to W decay to the present single copy, is potentially problematic, since Z-linked genes might interact with autosomal genes that remain in their ancestral double-copy state in both sexes.…”

A Genetic Map of Ostrich Z Chromosome and the Role of Inversions in Avian Sex Chromosome Evolution

“…2014; Smeds et al. 2015; Bellott et al. 2017), largely heterochromatic (Stefos and Arrighi 1971), and rich in satellite-like repeats (Saitoh et al.…”

Preparation of lampbrush chromosomes dissected from avian and reptilian growing oocytes

“…The cause of such similarity lies in the high degree of chromatin despiralization and the presence of numerous lateral loops of DNA, which are extended from chromomeres along the chromosome axis and actively transcribed by RNA polymerase II (Callan 1986). The high degree of decondensation, combined with the preservation of chromosome axial structure, have made lampbrush chromosomes a unique tool for high-resolution gene mapping and genome assembly data verification (Diaz and Gall 1985;Ogawa et al, 1997;Andreozzi et al, 2001;Galkina et al, 2006;Solinhac et al, 2010;Zlotina et al, 2010;Bellott et al, 2017). The first attempts of manual microdissection of lampbrush chromosomes from avian oocyte nuclei were made in the 1960s (Koecke and Muller 1965;Gaginskaya and Gruzova 1969;Ahmad 1970).…”