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

Authors

Ching-Ho Chang, University of RochesterFollow
Lauren E. Gregory, University of Rochester
Kathleen E. Gordon, University of Nebraska-Lincoln
Colin D. Meiklejohn, University of Nebraska-Lincoln
Amanda M. Larracuente, University of Rochester

Date of this Version

2021

Citation

Chang et al. eLife 2022;11:e75795. DOI: https://doi.org/10.7554/eLife.75795

Comments

OPEN Access

Abstract

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.