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

Elife. 2022 Jan 6:11:e75795. doi: 10.7554/eLife.75795.

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.

Keywords: D. melanogaster; Drosophila y chromosome; ampliconic gene familiy; convergent evolution; dna repair bias; evolutionary biology; genetics; genomics; pacbio genome assembly; sexual conflict.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Chromosomes, Insect / genetics*
  • Drosophila / genetics*
  • Drosophila melanogaster / genetics
  • Drosophila simulans / genetics
  • Evolution, Molecular*
  • Selection, Genetic*
  • Species Specificity
  • Y Chromosome / genetics*

Associated data

  • Dryad/10.5061/dryad.280gb5mr6