Letter | Published:

The industrial melanism mutation in British peppered moths is a transposable element

Nature volume 534, pages 102105 (02 June 2016) | Download Citation

Abstract

Discovering the mutational events that fuel adaptation to environmental change remains an important challenge for evolutionary biology. The classroom example of a visible evolutionary response is industrial melanism in the peppered moth (Biston betularia): the replacement, during the Industrial Revolution, of the common pale typica form by a previously unknown black (carbonaria) form, driven by the interaction between bird predation and coal pollution1. The carbonaria locus has been coarsely localized to a 200-kilobase region, but the specific identity and nature of the sequence difference controlling the carbonariatypica polymorphism, and the gene it influences, are unknown2. Here we show that the mutation event giving rise to industrial melanism in Britain was the insertion of a large, tandemly repeated, transposable element into the first intron of the gene cortex. Statistical inference based on the distribution of recombined carbonaria haplotypes indicates that this transposition event occurred around 1819, consistent with the historical record. We have begun to dissect the mode of action of the carbonaria transposable element by showing that it increases the abundance of a cortex transcript, the protein product of which plays an important role in cell-cycle regulation, during early wing disc development. Our findings fill a substantial knowledge gap in the iconic example of microevolutionary change, adding a further layer of insight into the mechanism of adaptation in response to natural selection. The discovery that the mutation itself is a transposable element will stimulate further debate about the importance of ‘jumping genes’ as a source of major phenotypic novelty3.

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Accessions

Primary accessions

Data deposits

The typica 1 haplotype (b–d interval) reference sequence has been deposited in GenBank under accession number KT182637; The B. betularia whole genome sequence has been deposited in the NCBI SRA database under accession number SRX1060178; the cortex splice variants have been deposited in GenBank under accession numbers KT235895KT235906; Rps3A has been deposited in GenBank under accession number JF811439; α-spec has been deposited in GenBank under accession number KT182638.

References

  1. 1.

    The rise and fall of the carbonaria form of the peppered moth. Q. Rev. Biol. 78, 399–417 (2003)

  2. 2.

    , , , & Industrial melanism in British peppered moths has a singular and recent mutational origin. Science 332, 958–960 (2011)

  3. 3.

    Evolutionary genetics: mobile DNAs as sources of adaptive change? Curr. Biol. 14, R344–R345 (2004)

  4. 4.

    & Molecular spandrels: tests of adaptation at the genetic level. Nature Rev. Genet. 12, 767–780 (2011)

  5. 5.

    & A golden age for evolutionary genetics ? Genomic studies of adaptation in natural populations. Trends Genet. 26, 484–492 (2010)

  6. 6.

    & The loci of repeated evolution: a catalog of genetic hotspots of phenotypic variation. Evolution 67, 1235–1250 (2013)

  7. 7.

    The genetic causes of convergent evolution. Nature Rev. Genet. 14, 751–764 (2013)

  8. 8.

    , & Ecological genomics of local adaptation. Nature Rev. Genet. 14, 807–820 (2013)

  9. 9.

    & The locus of evolution: evo devo and the genetics of adaptation. Evolution 61, 995–1016 (2007)

  10. 10.

    & The peppered moth and industrial melanism: evolution of a natural selection case study. Heredity 110, 207–212 (2013)

  11. 11.

    , , & Cortex, a Drosophila gene required to complete oocyte meiosis, is a member of the Cdc20/fizzy protein family. Genesis 29, 141–152 (2001)

  12. 12.

    , , , & Selection and gene flow along a diminishing cline of melanic peppered moths. Proc. Natl Acad. Sci. USA 105, 16212–16217 (2008)

  13. 13.

    Biston betularia, obligate f. insularia indistinguishable from f. carbonaria (Geometridae). J. Lepid. Soc. 33, 60–64 (1979)

  14. 14.

    & Genetics of insularia forms of peppered moth, Biston betularia. Heredity 39, 67–73 (1977)

  15. 15.

    & Linkage disequilibrium as a signature of selective sweeps. Genetics 167, 1513–1524 (2004)

  16. 16.

    , & Melanic moth frequencies in Yorkshire, an old English industrial hot spot. J. Hered. 96, 522–528 (2005)

  17. 17.

    Transposable elements and the evolution of regulatory networks. Nature Rev. Genet. 9, 397–405 (2008)

  18. 18.

    et al. Insights into degron recognition by APC/C coactivators from the structure of an Acm1-Cdh1 complex. Mol. Cell 50, 649–660 (2013)

  19. 19.

    , , & A meiosis-specific form of the APC/C promotes the oocyte-to-embryo transition by decreasing levels of the polo kinase inhibitor matrimony. PLoS Biol. 11, e1001648 (2013)

  20. 20.

    et al. The gene cortex controls mimicry and crypsis in butterflies and moths. Nature (this issue)

  21. 21.

    et al. Mapping and recombination analysis of two moth colour mutations, Black moth and Wild wing spot, in the silkworm Bombyx mori. Heredity 116, 52–59 (2016)

  22. 22.

    , , & Genome-wide patterns of adaptation to temperate environments associated with transposable elements in Drosophila. PLoS Genet. 6, e1000905 (2010)

  23. 23.

    & Strong selective sweep associated with a transposon insertion in Drosophila simulans. Proc. Natl Acad. Sci. USA 101, 1626–1631 (2004)

  24. 24.

    et al. Transposable element islands facilitate adaptation to novel environments in an invasive species. Nature Commun. 5, 5495 (2014)

  25. 25.

    & The impact of transposable elements in environmental adaptation. Mol. Ecol. 22, 1503–1517 (2013)

  26. 26.

    , , , & Vertebrate DNA transposon as a natural mutator: the medaka fish Tol2 element contributes to genetic variation without recognizable traces. Mol. Biol. Evol. 23, 1414–1419 (2006)

  27. 27.

    et al. Linkage map of the peppered moth, Biston betularia (Lepidoptera, Geometridae): a model of industrial melanism. Heredity 110, 283–295 (2013)

  28. 28.

    & AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res. 33, W465–W467 (2005)

  29. 29.

    et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnol. 29, 644–652 (2011)

  30. 30.

    , & A linear complexity phasing method for thousands of genomes. Nature Methods 9, 179–181 (2011)

  31. 31.

    & Indices of multilocus linkage disequilibrium. Mol. Ecol. Notes 1, 101–102 (2001)

  32. 32.

    , , & Inference of population structure using dense haplotype data. PLoS Genet. 8, e1002453 (2012)

  33. 33.

    et al. Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade. PLoS Genet. 6, e1000794 (2010)

  34. 34.

    , & Gene expression underlying adaptive variation in Heliconius wing patterns: non-modular regulation of overlapping cinnabar and vermilion prepatterns. Proc. R. Soc. Lond. B 275, 37–45 (2008)

  35. 35.

    & MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013)

  36. 36.

    , , , & MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729 (2013)

  37. 37.

    & Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779–815 (1993)

  38. 38.

    , , , & ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res. 38, W529–W533 (2010)

  39. 39.

    & DNA transposons: nature and applications in genomics. Curr. Genomics 11, 115–128 (2010)

  40. 40.

    , , , & Atomic structure of the APC/C and its mechanism of protein ubiquitination. Nature 522, 450–454 (2015)

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Acknowledgements

The University of Liverpool Centre for Genomic Research (M. Hughes, C. Bourne, R. Eccles, C. Hertz-Fowler and J. Kenny) performed next-generation sequencing and Fragment Analyzer measurements. L. Cook directed us to historical data sources. C. Bergman advised on transposon detection. Population genetics simulations were performed on the University of Liverpool Advanced Research Computing Condor service. This work was supported by Natural Environment Research Council grants NE/H024352/1 and NE/J022993/1.

Author information

Author notes

    • Arjen E. van’t Hof
    •  & Pascal Campagne

    These authors contributed equally to this work.

Affiliations

  1. Institute of Integrative Biology, University of Liverpool, Biosciences Building, Crown Street, Liverpool L69 7ZB, UK

    • Arjen E. van’t Hof
    • , Pascal Campagne
    • , Daniel J. Rigden
    • , Carl J. Yung
    • , Jessica Lingley
    • , Neil Hall
    • , Alistair C. Darby
    •  & Ilik J. Saccheri
  2. Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK

    • Michael A. Quail

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Contributions

I.J.S., A.E.v.H. and P.C. designed the study and wrote the paper; P.C., A.E.v.H. and D.J.R. produced the figures; A.E.v.H. directed molecular biology experiments; A.E.v.H., C.J.Y. and J.L. conducted molecular biology experiments; A.E.v.H. constructed the BAC and fosmid tilepaths; A.E.v.H. and A.C.D. assembled, finished and annotated sequences; P.C. analysed population genetic and gene expression data; I.J.S. collected the wild sample; I.J.S. and C.J.Y. reared the samples and performed dissections; D.J.R. and A.E.v.H. built the cortex tree; D.J.R. modelled the cortex structure; M.A.Q. constructed the fosmid library; and A.C.D. and N.H. advised on the design of sequencing strategies.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Ilik J. Saccheri.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Methods, Supplementary Figures 1-2 and Supplementary References.

Text files

  1. 1.

    Supplementary Data

    This file contains the sequence alignment of the carbonaria and three typica haplotypes spanning the ‘b-d’ region (illustrated in Extended Data Figure 1).

  2. 2.

    Supplementary Data

    This file contains full-length sequence alignment in aligned FASTA format of cortex proteins and selected homologues. Incompleteness of some sequences at the N-terminus and some uncertainty regarding translation start sites have no impact on the phylogenetic tree since it was calculated using only the propeller domain (see Extended Data Figure 9a).

Excel files

  1. 1.

    Supplementary Table 1

    This table shows polymorphisms in the carbonaria candidate region.

  2. 2.

    Supplementary Table 2

    This table contains polymorphisms in the locus b-d region.

  3. 3.

    Supplementary Table 3

    This table contains Carbonaria morph frequencies in the Manchester area.

  4. 4.

    Supplementary Table 4

    This table contains PCR primers for cortex, control genes and candidate genes.

  5. 5.

    Supplementary Table 5

    This table contains sources, including accession numbers, for cortex and Fizzy family sequences.

About this article

Publication history

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DOI

https://doi.org/10.1038/nature17951

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