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Evolution of genome structure in the Drosophila simulans species complex

View ORCID ProfileMahul Chakraborty, View ORCID ProfileChing-Ho Chang, Danielle E. Khost, View ORCID ProfileJeffrey Vedanayagam, View ORCID ProfileJeffrey R. Adrion, View ORCID ProfileYi Liao, View ORCID ProfileKristi L. Montooth, Colin D. Meiklejohn, Amanda M. Larracuente, J.J. Emerson
doi: https://doi.org/10.1101/2020.02.27.968743
Mahul Chakraborty
1Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA 92697
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  • ORCID record for Mahul Chakraborty
Ching-Ho Chang
2Department of Biology, University of Rochester, Rochester, NY 14627
3Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA 98109
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Danielle E. Khost
2Department of Biology, University of Rochester, Rochester, NY 14627
4FAS Informatics and Scientific Applications, Harvard University, Cambridge, MA 02138
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Jeffrey Vedanayagam
5Department of Developmental Biology, Memorial Sloan-Kettering Cancer Center, New York, NY, 10065
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Jeffrey R. Adrion
6Institute of Ecology and Evolution, University of Oregon, Eugene, Oregon 97403
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Yi Liao
1Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA 92697
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Kristi L. Montooth
7School of Biological Sciences, University of Nebraska-Lincoln, Nebraska 68502
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Colin D. Meiklejohn
7School of Biological Sciences, University of Nebraska-Lincoln, Nebraska 68502
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Amanda M. Larracuente
2Department of Biology, University of Rochester, Rochester, NY 14627
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  • For correspondence: alarracu@ur.rochester.edu jje@uci.edu
J.J. Emerson
1Department of Ecology and Evolutionary Biology, University of California Irvine, Irvine, CA 92697
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  • For correspondence: alarracu@ur.rochester.edu jje@uci.edu
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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 years 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 due 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, while 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.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • The new version has extensive revisions of the text and contains revised figures.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Evolution of genome structure in the Drosophila simulans species complex
Mahul Chakraborty, Ching-Ho Chang, Danielle E. Khost, Jeffrey Vedanayagam, Jeffrey R. Adrion, Yi Liao, Kristi L. Montooth, Colin D. Meiklejohn, Amanda M. Larracuente, J.J. Emerson
bioRxiv 2020.02.27.968743; doi: https://doi.org/10.1101/2020.02.27.968743
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Evolution of genome structure in the Drosophila simulans species complex
Mahul Chakraborty, Ching-Ho Chang, Danielle E. Khost, Jeffrey Vedanayagam, Jeffrey R. Adrion, Yi Liao, Kristi L. Montooth, Colin D. Meiklejohn, Amanda M. Larracuente, J.J. Emerson
bioRxiv 2020.02.27.968743; doi: https://doi.org/10.1101/2020.02.27.968743

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