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Unique structure and positive selection promote the rapid divergence of Drosophila Y chromosomes


Authors:
Ching-Ho Chang 1,2; Lauren Gregory 1; Kathleen Gordon 3; Colin Meiklejohn 3; Amanda Larracuente 1

Affiliations:
1) Department of Biology, University of Rochester, Rochester, NY 14627; 2) Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA 98109; 3) School of Biological Sciences, University of Nebraska-Lincoln, NE 68502

Keywords:
Comparative genomics & genome evolution

Y chromosomes across diverse species convergently evolve a gene-poor, heterochromatic organization enriched for duplicated genes, LTR retrotransposons, and satellite DNA. Sexual antagonism and a loss of recombination play major roles in the degeneration of young Y chromosomes. However, the processes shaping the evolution of mature, already degenerated Y chromosomes are less well-understood. Because Y chromosomes evolve rapidly, comparisons between closely related species are particularly useful. We generated de novo long read assemblies complemented with cytological validation to reveal Y chromosome organization in three closely related species of the Drosophila simulans complex, which diverged only 250,000 years ago and share >98% sequence identity. We find these Y chromosomes are divergent in their organization and repetitive DNA composition and discover new Y-linked gene families whose evolution is driven by both positive selection and gene conversion. These Y chromosomes are also enriched for large deletions, suggesting that the repair of double-strand breaks on Y chromosomes may be biased toward microhomology-mediated end joining over canonical non-homologous end-joining. We propose that this repair mechanism contributes to the convergent evolution of Y chromosome organization across organisms.