Ancestral Chromatin Configuration Constrains Chromatin Evolution on Differentiating Sex Chromosomes in Drosophila

Sex chromosomes evolve distinctive types of chromatin from a pair of ancestral autosomes that are usually euchromatic. in drosophila,the dosage-compensated x becomes enriched for hyperactive chromatin in males (mediated by h4k16ac),while the y chromosome acquires silencing heterochromatin (enriched for h3k9me2/3). drosophila autosomes are typically mostly euchromatic but the small dot chromosome has evolved a heterochromatin-like milieu (enriched for h3k9me2/3) that permits the normal expression of dot-linked genes,but which is different from typical pericentric heterochromatin. in drosophila busckii,the dot chromosomes have fused to the ancestral sex chromosomes,creating a pair of ‘neo-sex’ chromosomes. here we collect genomic,transcriptomic and epigenomic data from d. busckii,to investigate the evolutionary trajectory of sex chromosomes from a largely heterochromatic ancestor. we show that the neo-sex chromosomes formed <1 million years ago,but nearly 60% of neo-y linked genes have already become non-functional. expression levels are generally lower for the neo-y alleles relative to their neo-x homologs,and the silencing heterochromatin mark h3k9me2,but not h3k9me3,is significantly enriched on silenced neo-y genes. despite rampant neo-y degeneration,we find that the neo-x is deficient for the canonical histone modification mark of dosage compensation (h4k16ac),relative to autosomes or the compensated ancestral x chromosome,possibly reflecting constraints imposed on evolving hyperactive chromatin in an originally heterochromatic environment. yet,neo-x genes are transcriptionally more active in males,relative to females,suggesting the evolution of incipient dosage compensation on the neo-x. our data show that y degeneration proceeds quickly after sex chromosomes become established through genomic and epigenetic changes,and are consistent with the idea that the evolution of sex-linked chromatin is influenced by its ancestral configuration. © 2015 zhou,bachtrog.