1. Evolutionary Biology
  2. Genetics and Genomics
Download icon

Highly contiguous assemblies of 101 drosophilid genomes

  1. Bernard Y Kim  Is a corresponding author
  2. Jeremy Wang
  3. Danny E Miller
  4. Olga Barmina
  5. Emily Kay Delaney
  6. Ammon Thompson
  7. Aaron A Comeault
  8. David Peede
  9. Emmanuel R D'Agostino
  10. Julianne Pelaez
  11. Jessica M Aguilar
  12. Diler Haji
  13. Teruyuki Matsunaga
  14. Ellie Armstrong
  15. Molly Zych
  16. Yoshitaka Ogawa
  17. Marina Stamenković-Radak
  18. Mihailo Jelić
  19. Marija Savić Veselinović
  20. Marija Tanasković
  21. Pavle Erić
  22. Jian-Jun Gao
  23. Takehiro K Katoh
  24. Masanori J Toda
  25. Hideaki Watabe
  26. Masayoshi Watada
  27. Jeremy S Davis
  28. Leonie Moyle
  29. Giulia Manoli
  30. Enrico Bertolini
  31. Vladimír Košťál
  32. R Scott Hawley
  33. Aya Takahashi
  34. Corbin D Jones
  35. Donald K Price
  36. Noah K Whiteman
  37. Artyom Kopp
  38. Daniel R Matute
  39. Dmitri A Petrov
  1. Stanford University, United States
  2. University of North Carolina, United States
  3. University of Washington and Seattle Children's Hospital, United States
  4. UC Davis, United States
  5. University of California, Davis, United States
  6. Bangor University, United Kingdom
  7. University of North Carolina, Chapel Hill, United States
  8. University of California, Berkeley, United States
  9. University of Washington, United States
  10. Tokyo Metropolitan University, Japan
  11. University of Belgrade, Serbia
  12. National Institute of Republic of Serbia, Serbia
  13. Institute for Biological Research, Serbia
  14. Yunnan University, China
  15. Hokkaido University, Japan
  16. Sapporo College, Hokkaido University of Education, Japan
  17. Ehime University, Japan
  18. University of Kentucky, United States
  19. Indiana University, United States
  20. University of Würzburg, Germany
  21. Academy of Sciences of the Czech Republic, Czech Republic
  22. Stowers Institute for Medical Research, United States
  23. The University of North Carolina at Chapel Hill, United States
  24. University of Nevada, Las Vegas, United States
Tools and Resources
  • Cited 0
  • Views 688
  • Annotations
Cite this article as: eLife 2021;10:e66405 doi: 10.7554/eLife.66405

Abstract

Over 100 years of studies in Drosophila melanogaster and related species in the genus Drosophila have facilitated key discoveries in genetics, genomics, and evolution. While high-quality genome assemblies exist for several species in this group, they only encompass a small fraction of the genus. Recent advances in long-read sequencing allow high-quality genome assemblies for tens or even hundreds of species to be efficiently generated. Here, we utilize Oxford Nanopore sequencing to build an open community resource of genome assemblies for 101 lines of 93 drosophilid species encompassing 14 species groups and 35 sub-groups. The genomes are highly contiguous and complete, with an average contig N50 of 10.5 Mb and greater than 97% BUSCO completeness in 97/101 assemblies. We show that Nanopore-based assemblies are highly accurate in coding regions, particularly with respect to coding insertions and deletions. These assemblies, along with a detailed laboratory protocol and assembly pipelines, are released as a public resource and will serve as a starting point for addressing broad questions of genetics, ecology, and evolution at the scale of hundreds of species.

Data availability

All sequencing data and assemblies generated by this study are deposited at NCBI SRA and GenBank under NCBI BioProject PRJNA675888. Accession numbers for all data used but not generated by this study are provided in the supporting files. Dockerfiles and scripts for reproducing pipelines and analyses are provided on GitHub (https://github.com/flyseq/drosophila_assembly_pipelines). A detailed wet lab protocol is provided at Protocols.io (https://dx.doi.org/10.17504/protocols.io.bdfqi3mw).

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Bernard Y Kim

    Department of Biology, Stanford University, Stanford, United States
    For correspondence
    bernardkim@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5025-1292
  2. Jeremy Wang

    Genetics, University of North Carolina, Chapel Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0673-9418
  3. Danny E Miller

    Department of Pediatrics, Division of Genetic Medicine, University of Washington and Seattle Children's Hospital, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Olga Barmina

    Department of Evolution and Ecology, UC Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Emily Kay Delaney

    Ecology and Evolution, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3609-5702
  6. Ammon Thompson

    Department of Evolution and Ecology, UC Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Aaron A Comeault

    School of Natural Sciences, Bangor University, Bangor, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3954-2416
  8. David Peede

    Biology Deparment, University of North Carolina, Chapel Hill, Chapel Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4826-0464
  9. Emmanuel R D'Agostino

    Biology Deparment, University of North Carolina, Chapel Hill, Chapel Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Julianne Pelaez

    Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Jessica M Aguilar

    Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Diler Haji

    Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Teruyuki Matsunaga

    Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6433-622X
  14. Ellie Armstrong

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  15. Molly Zych

    Molecular and Cellular Biology Program, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  16. Yoshitaka Ogawa

    Department of Biological Sciences, Tokyo Metropolitan University, Hachioji, Japan
    Competing interests
    The authors declare that no competing interests exist.
  17. Marina Stamenković-Radak

    Faculty of Biology, University of Belgrade, Belgrade, Serbia
    Competing interests
    The authors declare that no competing interests exist.
  18. Mihailo Jelić

    Faculty of Biology, University of Belgrade, Belgrade, Serbia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1637-0933
  19. Marija Savić Veselinović

    Faculty of Biology, University of Belgrade, Belgrade, Serbia
    Competing interests
    The authors declare that no competing interests exist.
  20. Marija Tanasković

    Institute for Biological Research Siniša Stanković"", National Institute of Republic of Serbia, Belgrade, Serbia
    Competing interests
    The authors declare that no competing interests exist.
  21. Pavle Erić

    Population Genetics and Ecogenotoxicology, Institute for Biological Research, Belgrade, Serbia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0053-1982
  22. Jian-Jun Gao

    School of Ecology and Environmental Science, Yunnan University, Kunming, China
    Competing interests
    The authors declare that no competing interests exist.
  23. Takehiro K Katoh

    School of Ecology and Environmental Science, Yunnan University, Kunming, China
    Competing interests
    The authors declare that no competing interests exist.
  24. Masanori J Toda

    Hokkaido University Museum, Hokkaido University, Sapporo, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0158-1858
  25. Hideaki Watabe

    Biological Laboratory, Sapporo College, Hokkaido University of Education, Sapporo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  26. Masayoshi Watada

    Graduate School of Science and Engineering, Ehime University, Matsuyama, Japan
    Competing interests
    The authors declare that no competing interests exist.
  27. Jeremy S Davis

    Department of Biology, University of Kentucky, Lexington, United States
    Competing interests
    The authors declare that no competing interests exist.
  28. Leonie Moyle

    Indiana University, Bloomington, United States
    Competing interests
    The authors declare that no competing interests exist.
  29. Giulia Manoli

    Neurobiology and Genetics, Theodor Boveri Institute, Biocentre, University of Würzburg, Würzburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  30. Enrico Bertolini

    Neurobiology and Genetics, Theodor Boveri Institute, Biocentre, University of Würzburg, Würzburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  31. Vladimír Košťál

    Institute of Entomology, Biology Centre, Academy of Sciences of the Czech Republic, Prague, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  32. R Scott Hawley

    Stowers Institute for Medical Research, Kansas City, United States
    Competing interests
    The authors declare that no competing interests exist.
  33. Aya Takahashi

    Department of Biological Sciences, Tokyo Metropolitan University, Hachioji, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8391-7417
  34. Corbin D Jones

    Biology Department, The University of North Carolina at Chapel Hill, Chapel Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  35. Donald K Price

    School of Life Sciences, University of Nevada, Las Vegas, Las Vegas, United States
    Competing interests
    The authors declare that no competing interests exist.
  36. Noah K Whiteman

    Department of Integrative Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1448-4678
  37. Artyom Kopp

    Department of Evolution and Ecology, UC Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5224-0741
  38. Daniel R Matute

    Biology Deparment, University of North Carolina, Chapel Hill, Chapel Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  39. Dmitri A Petrov

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3664-9130

Funding

National Institute of General Medical Sciences (F32GM135998)

  • Bernard Y Kim

National Institute of General Medical Sciences (R35GM119816)

  • Noah K Whiteman

Uehara Memorial Foundation (201931028)

  • Teruyuki Matsunaga

Ministry of Education, Science and Technological Development of the Republic of Serbia (451-03-68/2020-14/200178)

  • Marina Stamenković-Radak
  • Mihailo Jelić
  • Marija Savić Veselinović

Ministry of Education, Science and Technological Development of the Republic of Serbia (451-03-68/2020-14/200007)

  • Marija Tanasković
  • Pavle Erić

National Natural Science Foundation of China (32060112)

  • Jian-Jun Gao

Japan Society for the Promotion of Science (JP18K06383)

  • Masayoshi Watada

European Union Horizon 2020 Research and Innovation Program (765937-CINCHRON)

  • Giulia Manoli
  • Enrico Bertolini

Czech Science Foundation (19-13381S)

  • Vladimír Košťál

Japan Society for the Promotion of Science (JP19H03276)

  • Aya Takahashi

National Science Foundation (1345247)

  • Donald K Price

National Institute of General Medical Sciences (R35GM118165)

  • Dmitri A Petrov

National Institute of Diabetes and Digestive and Kidney Diseases (K01DK119582)

  • Jeremy Wang

National Science Foundation (DEB-1457707)

  • Corbin D Jones

National Institute of General Medical Sciences (R01GM121750)

  • Daniel R Matute

National Institute of General Medical Sciences (R01GM125715)

  • Daniel R Matute

Google Cloud Platform Research Credits

  • Bernard Y Kim

Google Cloud Platform Research Credits

  • Jeremy Wang

National Institute of General Medical Sciences (R35GM122592)

  • Artyom Kopp

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Graham Coop, University of California, Davis, United States

Publication history

  1. Received: January 11, 2021
  2. Accepted: July 16, 2021
  3. Accepted Manuscript published: July 19, 2021 (version 1)

Copyright

© 2021, Kim et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 688
    Page views
  • 126
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Evolutionary Biology
    2. Microbiology and Infectious Disease
    George H Perry
    Editorial

    In recognition that evolutionary theory is critical for understanding modern human health, eLife is publishing a special issue on evolutionary medicine to showcase recent research in this growing and increasingly interdisciplinary field.

    1. Evolutionary Biology
    2. Physics of Living Systems
    Erida Gjini, Kevin B Wood
    Research Article

    Bacterial adaptation to antibiotic combinations depends on the joint inhibitory effects of the two drugs (drug interaction, DI) and how resistance to one drug impacts resistance to the other (collateral effects, CE). Here we model these evolutionary dynamics on two-dimensional phenotype spaces that leverage scaling relations between the drug-response surfaces of drug sensitive (ancestral) and drug resistant (mutant) populations. We show that evolved resistance to the component drugs-and in turn, the adaptation of growth rate-is governed by a Price equation whose covariance terms encode geometric features of both the two-drug response surface (DI) in ancestral cells and the correlations between resistance levels to those drugs (CE). Within this framework, mean evolutionary trajectories reduce to a type of weighted gradient dynamics, with the drug interaction dictating the shape of the underlying landscape and the collateral effects constraining the motion on those landscapes. We also demonstrate how constraints on available mutational pathways can be incorporated into the framework, adding a third key driver of evolution. Our results clarify the complex relationship between drug interactions and collateral effects in multi-drug environments and illustrate how specific dosage combinations can shift the weighting of these two effects, leading to different and temporally-explicit selective outcomes.