Evolution of genome structure in the Drosophila simulans species complex

Authors

Mahul Chakraborty, University of California, Irvine
Ching-Ho Chang, University of Rochester
Danielle E. Khost, University of Rochester
Jeffrey Vedanayagam, Memorial Sloan-Kettering Cancer Center
Jeffrey R. Adrion, University of Oregon
Yi Liao, University of California
Kristi L. Montooth, University of Nebraska - LincolnFollow
Colin D. Meiklejohn, University of Nebraska-LincolnFollow
Amanda M. Larracuente, University of Rochester
J J. Emerson, University of California, Irvine

Date of this Version

3-22-2021

Comments

OPEN ACCESS

Abstract

The rapid evolution of repetitive DNA sequences, including satellite DNA, tandem duplications, and transposable elements, underlies phenotypic evolution and contributes to hybrid incompatibilities between species. However, repetitive genomic regions are fragmented and misassembled in most contemporary genome assemblies. We generated highly contiguous de novo reference genomes for the Drosophila simulans species complex (D. simulans, D. mauritiana, and D. sechellia), which speciated ∼250,000 yr ago. Our assemblies are comparable in contiguity and accuracy to the current D. melanogaster genome, allowing us to directly compare repetitive sequences between these four species. We find that at least 15% of the D. simulans complex species genomes fail to align uniquely to D. melanogaster owing to structural divergence—twice the number of single-nucleotide substitutions. We also find rapid turnover of satellite DNA and extensive structural divergence in heterochromatic regions, whereas the euchromatic gene content is mostly conserved. Despite the overall preservation of gene synteny, euchromatin in each species has been shaped by clade- and species-specific inversions, transposable elements, expansions and contractions of satellite and tRNA tandem arrays, and gene duplications. We also find rapid divergence among Y-linked genes, including copy number variation and recent gene duplications from autosomes. Our assemblies provide a valuable resource for studying genome evolution and its consequences for phenotypic evolution in these genetic model species.