Abstract
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.
Highlights
Sex chromosomes have originated independently many times from ordinary autosomes in both plants and animals [1]
DNA is packaged with proteins into two general types of chromatin: the transcriptionally active euchromatin and repressive heterochromatin
We investigate a pair of unusual young sex chromosomes in D. busckii, which formed through fusions of a largely heterochromatic autosome to the ancestral sex chromosomes
Summary
Sex chromosomes have originated independently many times from ordinary autosomes in both plants and animals [1]. The older neo-Y chromosome of D. miranda (1.5 million years old) has acquired stop codons and frame-shift mutations in almost half of its genes, shows a dramatic accumulation of transposable elements (between 30–50% of its DNA is composed of TEs) [12,13], and most neo-Y genes are expressed at a lower level than their neo-X homologs [11] These changes at the DNA sequence level are accompanied by a global change in chromatin structure, and the D. miranda neo-Y is adopting a heterochromatic appearance marked by histone H3 lysine 9 di-methylation (H3K9me2) [3]. The neo-sex chromosome shared by members of the D. pseudoobscura species group was formed about 15 million years ago, and has evolved the typical properties of old sex chromosomes: the neo-Y is completely degenerate and heterochromatic, while the neo-X is fully dosage compensated by the MSL machinery [3,16]
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