Home LiteratureArticle Details
PMID: 25189940 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

The Glanville fritillary genome retains an ancient karyotype and reveals selective chromosomal fusions in Lepidoptera.

Nature communications ·Vol. 5 ·2014-09-05 ·Pages 4737

Ahola V, Lehtonen R, Somervuo P, Salmela L, Koskinen P, Rastas P, Välimäki N, Paulin L, Kvist J, Wahlberg N, Tanskanen J, Hornett EA, Ferguson LC, Luo S, Cao Z, de Jong MA, Duplouy A, Smolander OP, Vogel H, McCoy RC, Qian K, Chong WS, Zhang Q, Ahmad F, Haukka JK, Joshi A, Salojärvi J, Wheat CW, Grosse-Wilde E, Hughes D, Katainen R, Pitkänen E, Ylinen J, Waterhouse RM, Turunen M, Vähärautio A, Ojanen SP, Schulman AH, Taipale M, Lawson D, Ukkonen E, Mäkinen V, Goldsmith MR, Holm L, Auvinen P, Frilander MJ, Hanski I

Abstract

Previous studies have reported that chromosome synteny in Lepidoptera has been well conserved, yet the number of haploid chromosomes varies widely from 5 to 223. Here we report the genome (393 Mb) of the Glanville fritillary butterfly (Melitaea cinxia; Nymphalidae), a widely recognized model species in metapopulation biology and eco-evolutionary research, which has the putative ancestral karyotype of n=31. Using a phylogenetic analyses of Nymphalidae and of other Lepidoptera, combined with orthologue-level comparisons of chromosomes, we conclude that the ancestral lepidopteran karyotype has been n=31 for at least 140 My. We show that fusion chromosomes have retained the ancestral chromosome segments and very few rearrangements have occurred across the fusion sites. The same, shortest ancestral chromosomes have independently participated in fusion events in species with smaller karyotypes. The short chromosomes have higher rearrangement rate than long ones. These characteristics highlight distinctive features of the evolutionary dynamics of butterflies and moths.

MeSH Terms
Animals Base Sequence Butterflies/genetics Chromosome Aberrations Chromosome Mapping Evolution, Molecular Genome/genetics Karyotype Likelihood Functions Models, Genetic Molecular Sequence Data Phylogeny Sequence Analysis, DNA Synteny
Authors & Affiliations
47 authors, click to expand affiliations / ORCID
Ahola Virpi
1] Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland [2].
Lehtonen Rainer
1] Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland [2] Genome-Scale Biology Research Program, University of Helsinki, FI-00014 Helsinki, Finland [3] Institute of Biomedicine, University of Helsinki, FI-00014 Helsinki, Finland [4] Center of Excellence in Cancer Genetics, University of Helsinki, FI-00014 Helsinki, Finland [5] [6].
Somervuo Panu
1] Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland [2] Institute of Biotechnology, University of Helsinki, FI-00014 Helsinki, Finland [3].
Salmela Leena
Department of Computer Science &Helsinki Institute for Information Technology HIIT, University of Helsinki, FI-00014 Helsinki, Finland.
Koskinen Patrik
1] Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland [2] Institute of Biotechnology, University of Helsinki, FI-00014 Helsinki, Finland.
Rastas Pasi
Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland.
Välimäki Niko
1] Genome-Scale Biology Research Program, University of Helsinki, FI-00014 Helsinki, Finland [2] Institute of Biomedicine, University of Helsinki, FI-00014 Helsinki, Finland.
Paulin Lars
Institute of Biotechnology, University of Helsinki, FI-00014 Helsinki, Finland.
Kvist Jouni
Institute of Biotechnology, University of Helsinki, FI-00014 Helsinki, Finland.
Wahlberg Niklas
Department of Biology, University of Turku, FI-20014 Turku, Finland.
Tanskanen Jaakko
1] Institute of Biotechnology, University of Helsinki, FI-00014 Helsinki, Finland [2] Biotechnology and Food Research, MTT Agrifood Research Finland, FI-31600 Jokioinen, Finland.
Hornett Emily A
1] Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK [2] Department of Biology, Pennsylvania State University, Pennsylvania 16802, USA.
Ferguson Laura C
Department of Zoology, University of Oxford, Oxford OX1 3PS, UK.
Luo Shiqi
College of Life Sciences, Peking University, Beijing 100871, P.R. China.
Cao Zijuan
College of Life Sciences, Peking University, Beijing 100871, P.R. China.
de Jong Maaike A
1] Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland [2] School of Biological Sciences, University of Bristol, Bristol BS8 1UG, UK.
Duplouy Anne
Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland.
Smolander Olli-Pekka
Institute of Biotechnology, University of Helsinki, FI-00014 Helsinki, Finland.
Vogel Heiko
Department of Entomology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.
McCoy Rajiv C
Department of Biology, Stanford University, Stanford, California 94305, USA.
Qian Kui
Institute of Biotechnology, University of Helsinki, FI-00014 Helsinki, Finland.
Chong Wong Swee
Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland.
Zhang Qin
BioMediTech, University of Tampere, FI-33520 Tampere, Finland.
Ahmad Freed
Department of Information Technology, University of Turku, FI-20014 Turku, Finland.
Haukka Jani K
BioMediTech, University of Tampere, FI-33520 Tampere, Finland.
Joshi Aruj
BioMediTech, University of Tampere, FI-33520 Tampere, Finland.
Salojärvi Jarkko
Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland.
Wheat Christopher W
Department of Zoology, Stockholm University, SE-10691 Stockholm, Sweden.
Grosse-Wilde Ewald
Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.
Hughes Daniel
1] European Bioinformatics Institute, Hinxton CB10 1SD, UK [2] Baylor College of Medicine, Human Genome Sequencing Center, Houston, Texas 77030-3411, USA.
Katainen Riku
1] Genome-Scale Biology Research Program, University of Helsinki, FI-00014 Helsinki, Finland [2] Institute of Biomedicine, University of Helsinki, FI-00014 Helsinki, Finland.
Pitkänen Esa
1] Genome-Scale Biology Research Program, University of Helsinki, FI-00014 Helsinki, Finland [2] Institute of Biomedicine, University of Helsinki, FI-00014 Helsinki, Finland.
Ylinen Johannes
Department of Computer Science &Helsinki Institute for Information Technology HIIT, University of Helsinki, FI-00014 Helsinki, Finland.
Waterhouse Robert M
1] Department of Genetic Medicine and Development, University of Geneva Medical School &Swiss Institute of Bioinformatics, 1211 Geneva, Switzerland [2] Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA [3] The Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142, USA.
Turunen Mikko
Genome-Scale Biology Research Program, University of Helsinki, FI-00014 Helsinki, Finland.
Vähärautio Anna
1] Genome-Scale Biology Research Program, University of Helsinki, FI-00014 Helsinki, Finland [2] Department of Pathology, University of Helsinki, FI-00014 Helsinki, Finland [3] Science for Life Laboratory, Department of Biosciences and Nutrition, Karolinska Institutet, SE-14183 Stockholm, Sweden.
Ojanen Sami P
Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland.
Schulman Alan H
1] Institute of Biotechnology, University of Helsinki, FI-00014 Helsinki, Finland [2] Biotechnology and Food Research, MTT Agrifood Research Finland, FI-31600 Jokioinen, Finland.
Taipale Minna
1] Genome-Scale Biology Research Program, University of Helsinki, FI-00014 Helsinki, Finland [2] Science for Life Laboratory, Department of Biosciences and Nutrition, Karolinska Institutet, SE-14183 Stockholm, Sweden.
Lawson Daniel
European Bioinformatics Institute, Hinxton CB10 1SD, UK.
Ukkonen Esko
Department of Computer Science &Helsinki Institute for Information Technology HIIT, University of Helsinki, FI-00014 Helsinki, Finland.
Mäkinen Veli
Department of Computer Science &Helsinki Institute for Information Technology HIIT, University of Helsinki, FI-00014 Helsinki, Finland.
Goldsmith Marian R
Department of Biological Sciences, University of Rhode Island, Kingston, Rhode Island 02881-0816, USA.
Holm Liisa
1] Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland [2] Institute of Biotechnology, University of Helsinki, FI-00014 Helsinki, Finland [3].
Auvinen Petri
1] Institute of Biotechnology, University of Helsinki, FI-00014 Helsinki, Finland [2].
Frilander Mikko J
1] Institute of Biotechnology, University of Helsinki, FI-00014 Helsinki, Finland [2].
Hanski Ilkka
Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland.
References (62)
62 references, click to expand
  1. A rapid bootstrap algorithm for the RAxML Web servers.
    Syst Biol. 2008 Oct;57(5):758-71 PMID: 18853362
  2. Linkage map of the peppered moth, Biston betularia (Lepidoptera, Geometridae): a model of industrial melanism.
    Heredity (Edinb). 2013 Mar;110(3):283-95 PMID: 23211790
  3. Speciation by monobrachial centric fusions.
    Proc Natl Acad Sci U S A. 1986 Nov;83(21):8245-8 PMID: 16593777
  4. Fast and accurate long-read alignment with Burrows-Wheeler transform.
    Bioinformatics. 2010 Mar 1;26(5):589-95 PMID: 20080505
  5. The genome of Tetranychus urticae reveals herbivorous pest adaptations.
    Nature. 2011 Nov 23;479(7374):487-92 PMID: 22113690
  6. Timing and patterns in the taxonomic diversification of Lepidoptera (butterflies and moths).
    PLoS One. 2013 Nov 25;8(11):e80875 PMID: 24282557
  7. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes.
    Genome Res. 2008 Jan;18(1):188-96 PMID: 18025269
  8. Chromosomal evolution in tortricid moths: conserved karyotypes with diverged features.
    PLoS One. 2013 May 24;8(5):e64520 PMID: 23717623
  9. Chromosomal speciation revisited: rearranging theory with pieces of evidence.
    Trends Ecol Evol. 2010 Nov;25(11):660-9 PMID: 20817305
  10. Linkage mapping and comparative genomics using next-generation RAD sequencing of a non-model organism.
    PLoS One. 2011 Apr 26;6(4):e19315 PMID: 21541297
  11. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons.
    Nucleic Acids Res. 2007 Jul;35(Web Server issue):W265-8 PMID: 17485477
  12. A genomewide survey of homeobox genes and identification of novel structure of the Hox cluster in the silkworm, Bombyx mori.
    Insect Biochem Mol Biol. 2008 Dec;38(12):1111-20 PMID: 19280701
  13. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species.
    Nature. 2012 Jul 5;487(7405):94-8 PMID: 22722851
  14. A large-scale evaluation of computational protein function prediction.
    Nat Methods. 2013 Mar;10(3):221-7 PMID: 23353650
  15. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation.
    Nat Biotechnol. 2010 May;28(5):511-5 PMID: 20436464
  16. A gene-based linkage map for Bicyclus anynana butterflies allows for a comprehensive analysis of synteny with the lepidopteran reference genome.
    PLoS Genet. 2009 Feb;5(2):e1000366 PMID: 19197358
  17. Genome-wide evidence for speciation with gene flow in Heliconius butterflies.
    Genome Res. 2013 Nov;23(11):1817-28 PMID: 24045163
  18. Chromosome evolution in Neotropical butterflies.
    Hereditas. 2013 Jun;150(2-3):26-37 PMID: 23865963
  19. Moth sex chromatin probed by comparative genomic hybridization (CGH).
    Genome. 2003 Apr;46(2):339-42 PMID: 12723050
  20. Transcriptome analysis reveals signature of adaptation to landscape fragmentation.
    PLoS One. 2014 Jul 02;9(7):e101467 PMID: 24988207
  21. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement.
    PLoS One. 2010 Jun 25;5(6):e11147 PMID: 20593022
  22. Repbase Update, a database of eukaryotic repetitive elements.
    Cytogenet Genome Res. 2005;110(1-4):462-7 PMID: 16093699
  23. Karyotypic diversity and speciation in Agrodiaetus butterflies.
    Evolution. 2007 Mar;61(3):546-59 PMID: 17348919
  24. Correction of sequencing errors in a mixed set of reads.
    Bioinformatics. 2010 May 15;26(10):1284-90 PMID: 20378555
  25. Nymphalid butterflies diversify following near demise at the Cretaceous/Tertiary boundary.
    Proc Biol Sci. 2009 Dec 22;276(1677):4295-302 PMID: 19793750
  26. The genome of a lepidopteran model insect, the silkworm Bombyx mori.
    Insect Biochem Mol Biol. 2008 Dec;38(12):1036-45 PMID: 19121390
  27. "Holo"er than thou: chromosome segregation and kinetochore function in C. elegans.
    Chromosome Res. 2004;12(6):641-53 PMID: 15289669
  28. Chromosome evolution in Neotropical Danainae and Ithomiinae (Lepidoptera).
    Hereditas. 2004;141(3):216-36 PMID: 15703038
  29. Lep-MAP: fast and accurate linkage map construction for large SNP datasets.
    Bioinformatics. 2013 Dec 15;29(24):3128-34 PMID: 24078685
  30. Synteny and chromosome evolution in the lepidoptera: evidence from mapping in Heliconius melpomene.
    Genetics. 2007 Sep;177(1):417-26 PMID: 17603110
  31. KAAS: an automatic genome annotation and pathway reconstruction server.
    Nucleic Acids Res. 2007 Jul;35(Web Server issue):W182-5 PMID: 17526522
  32. Fast scaffolding with small independent mixed integer programs.
    Bioinformatics. 2011 Dec 1;27(23):3259-65 PMID: 21998153
  33. Chromosomes tell half of the story: the correlation between karyotype rearrangements and genetic diversity in sedges, a group with holocentric chromosomes.
    Mol Ecol. 2010 Aug;19(15):3124-38 PMID: 20618902
  34. Circos: an information aesthetic for comparative genomics.
    Genome Res. 2009 Sep;19(9):1639-45 PMID: 19541911
  35. Telomere fusions in early human breast carcinoma.
    Proc Natl Acad Sci U S A. 2012 Aug 28;109(35):14098-103 PMID: 22891313
  36. A framework for variation discovery and genotyping using next-generation DNA sequencing data.
    Nat Genet. 2011 May;43(5):491-8 PMID: 21478889
  37. Dfam: a database of repetitive DNA based on profile hidden Markov models.
    Nucleic Acids Res. 2013 Jan;41(Database issue):D70-82 PMID: 23203985
  38. Extensive conserved synteny of genes between the karyotypes of Manduca sexta and Bombyx mori revealed by BAC-FISH mapping.
    PLoS One. 2009 Oct 15;4(10):e7465 PMID: 19829706
  39. The mosaic genome of warm-blooded vertebrates.
    Science. 1985 May 24;228(4702):953-8 PMID: 4001930
  40. De novo assembly of human genomes with massively parallel short read sequencing.
    Genome Res. 2010 Feb;20(2):265-72 PMID: 20019144
  41. TopHat: discovering splice junctions with RNA-Seq.
    Bioinformatics. 2009 May 1;25(9):1105-11 PMID: 19289445
  42. Unlocking holocentric chromosomes: new perspectives from comparative and functional genomics?
    Curr Genomics. 2012 Aug;13(5):343-9 PMID: 23372420
  43. Large scale full-length cDNA sequencing reveals a unique genomic landscape in a lepidopteran model insect, Bombyx mori.
    G3 (Bethesda). 2013 Sep 04;3(9):1481-92 PMID: 23821615
  44. Correcting errors in short reads by multiple alignments.
    Bioinformatics. 2011 Jun 1;27(11):1455-61 PMID: 21471014
  45. Extensive synteny conservation of holocentric chromosomes in Lepidoptera despite high rates of local genome rearrangements.
    Proc Natl Acad Sci U S A. 2010 Apr 27;107(17):7680-5 PMID: 20388903
  46. Characterization of bacteriophage P1 library containing inserts of Drosophila DNA of 75-100 kilobase pairs.
    Chromosoma. 1991 Sep;100(8):487-94 PMID: 1764967
  47. Telomere-specific non-LTR retrotransposons and telomere maintenance in the silkworm, Bombyx mori.
    Chromosome Res. 2005;13(5):455-67 PMID: 16132811
  48. Retrotransposable elements on the W chromosome of the silkworm, Bombyx mori.
    Cytogenet Genome Res. 2005;110(1-4):144-51 PMID: 16093666
  49. A large-scale, higher-level, molecular phylogenetic study of the insect order Lepidoptera (moths and butterflies).
    PLoS One. 2013;8(3):e58568 PMID: 23554903
  50. The common colorectal cancer predisposition SNP rs6983267 at chromosome 8q24 confers potential to enhanced Wnt signaling.
    Nat Genet. 2009 Aug;41(8):885-90 PMID: 19561604
  51. Cytological evidence for holocentric chromosomes of the silkworms, Bombyx mori and B. mandarina, (Bombycidae, Lepidoptera).
    Chromosoma. 1974;47(2):167-78 PMID: 4141955
  52. Telomere-associated endonuclease-deficient Penelope-like retroelements in diverse eukaryotes.
    Proc Natl Acad Sci U S A. 2007 May 29;104(22):9352-7 PMID: 17483479
  53. Genome sequence of the nematode C. elegans: a platform for investigating biology.
    Science. 1998 Dec 11;282(5396):2012-8 PMID: 9851916
  54. InterProScan--an integration platform for the signature-recognition methods in InterPro.
    Bioinformatics. 2001 Sep;17(9):847-8 PMID: 11590104
  55. FISH identification of Helicoverpa armigera and Mamestra brassicae chromosomes by BAC and fosmid probes.
    Insect Biochem Mol Biol. 2013 Aug;43(8):644-53 PMID: 23628856
  56. The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics.
    PLoS Biol. 2003 Nov;1(2):E45 PMID: 14624247
  57. A second-generation integrated map of the silkworm reveals synteny and conserved gene order between lepidopteran insects.
    Genetics. 2006 Jul;173(3):1319-28 PMID: 16547103
  58. A heterozygous moth genome provides insights into herbivory and detoxification.
    Nat Genet. 2013 Feb;45(2):220-5 PMID: 23313953
  59. SANS: high-throughput retrieval of protein sequences allowing 50% mismatches.
    Bioinformatics. 2012 Sep 15;28(18):i438-i443 PMID: 22962464
  60. Gene finding in novel genomes.
    BMC Bioinformatics. 2004 May 14;5:59 PMID: 15144565
  61. A novel method for assigning functional linkages to proteins using enhanced phylogenetic trees.
    Bioinformatics. 2011 Mar 1;27(5):700-6 PMID: 21169380
  62. Initial sequencing and comparative analysis of the mouse genome.
    Nature. 2002 Dec 5;420(6915):520-62 PMID: 12466850
Article Info
Journal
Nature communications
Abbr.
Nat Commun
ISSN
2041-1723
DOI
10.1038/ncomms5737
Published
2014-09-05
Epub
2014-00-05
Pages
4737
Language
English
Region
England
NLM ID
101528555
PMCID
PMC4164777
Subset
IM
Grants
European Research Council · 232826 · International
Databases
GENBANK
APLT00000000
External Links
PubMed source DOI: 10.1038/ncomms5737 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2