Comparative genomics of the mimicry switch in Papilio dardanus

Article


Timmermans, M., Baxter, S., Clark, R., Heckel, D., Vogel, H., Collins, S., Papanicolaou, A., Fukova, I., Joron, M., Thompson, M., Jiggins, C., ffrench-Constant, R. and Vogler, A. 2014. Comparative genomics of the mimicry switch in Papilio dardanus. Proceedings of the Royal Society B: Biological Sciences. 281 (1787), pp. 1-8. https://doi.org/10.1098/rspb.2014.0465
TypeArticle
TitleComparative genomics of the mimicry switch in Papilio dardanus
AuthorsTimmermans, M., Baxter, S., Clark, R., Heckel, D., Vogel, H., Collins, S., Papanicolaou, A., Fukova, I., Joron, M., Thompson, M., Jiggins, C., ffrench-Constant, R. and Vogler, A.
Abstract

The African Mocker Swallowtail, Papilio dardanus, is a textbook example in evolutionary genetics. Classical breeding experiments have shown that wing pattern variation in this polymorphic Batesian mimic is determined by the polyallelic H locus that controls a set of distinct mimetic phenotypes. Using bacterial artificial chromosome (BAC) sequencing, recombination analyses and comparative genomics, we show that H co-segregates with an interval of less than 500 kb that is collinear with two other Lepidoptera genomes and contains 24 genes, including the transcription factor genes engrailed (en) and invected (inv). H is located in a region of conserved gene order, which argues against any role for genomic translocations in the evolution of a hypothesized multi-gene mimicry locus. Natural populations of P. dardanus show significant associations of specific morphs with single nucleotide polymorphisms (SNPs), centred on en. In addition, SNP variation in the H region reveals evidence of non-neutral molecular evolution in the en gene alone. We find evidence for a duplication potentially driving physical constraints on recombination in the lamborni morph. Absence of perfect linkage disequilibrium between different genes in the other morphs suggests that H is limited to nucleotide positions in the regulatory and coding regions of en. Our results therefore support the hypothesis that a single gene underlies wing pattern variation in P. dardanus.

PublisherThe Royal Society
JournalProceedings of the Royal Society B: Biological Sciences
ISSN0962-8452
Electronic1471-2954
Publication dates
Online22 Jul 2014
Print22 Jul 2014
Publication process dates
Deposited01 May 2015
Submitted25 Feb 2014
Accepted14 May 2014
Output statusPublished
Publisher's version
Copyright Statement

© 2014 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/3.0/, which permits unrestricted use, provided the original author and source are credited.

Digital Object Identifier (DOI)https://doi.org/10.1098/rspb.2014.0465
LanguageEnglish
Permalink -

https://repository.mdx.ac.uk/item/85316

Download files


Publisher's version
  • 43
    total views
  • 11
    total downloads
  • 3
    views this month
  • 1
    downloads this month

Export as

Related outputs

Turning the tide: rhythmic aggregation behaviour in Anurida maritima (Collembola) is entrained by inundation
Timmermans, M., King, M., Purchase, D., Dickins, J.A., Dickins, T. and Kett, S. 2024. Turning the tide: rhythmic aggregation behaviour in Anurida maritima (Collembola) is entrained by inundation. Journal of Experimental Marine Biology and Ecology. 581. https://doi.org/10.1016/j.jembe.2024.152062
A study of bacteria producing carbonic anhydrase enzyme for CaCO3 precipitation and soil biocementation
Meandira, W., Mavroulidou, M., Timmermans, M., Gunn, M., Gray, C., Pantoja Munoz, L. and Purchase, D. 2024. A study of bacteria producing carbonic anhydrase enzyme for CaCO3 precipitation and soil biocementation. Environmental Science and Pollution Research. 31 (33), pp. 45818-45833. https://doi.org/10.1007/s11356-024-34077-0
Molding the future: optimization of bioleaching of rare earth elements from electronic waste by Penicillium expansum and insights into its mechanism
Gonzalez Baez, A., Pantoja Munoz, L., Timmermans, M., Garelick, H. and Purchase, D. 2024. Molding the future: optimization of bioleaching of rare earth elements from electronic waste by Penicillium expansum and insights into its mechanism. Bioresource Technology. 402. https://doi.org/10.1016/j.biortech.2024.130750
Wolbachia and Spiroplasma endosymbionts in the Anurida maritima (Collembola) species group
Timmermans, M., Prabha, H. and Kett, S. 2023. Wolbachia and Spiroplasma endosymbionts in the Anurida maritima (Collembola) species group. Evolutionary Journal of the Linnean Society. 2 (1). https://doi.org/10.1093/evolinnean/kzad001
Mitochondrial genome divergence supports an ancient origin of circatidal behaviour in the Anurida maritima (Collembola: Neanuridae) species group
Timmermans, M., Arbea, J., Campbell, G., King, M., Prins, A. and Kett, S. 2022. Mitochondrial genome divergence supports an ancient origin of circatidal behaviour in the Anurida maritima (Collembola: Neanuridae) species group. Organisms Diversity & Evolution. 22 (1), pp. 131-140. https://doi.org/10.1007/s13127-021-00503-1
Mimicry diversification in Papilio dardanus via a genomic inversion in the regulatory region of engrailed – invected
Timmermans, M., Srivathsan, A., Collins, S., Meier, R. and Vogler, A. 2020. Mimicry diversification in Papilio dardanus via a genomic inversion in the regulatory region of engrailed – invected. Proceedings of the Royal Society B: Biological Sciences. 287 (1926). https://doi.org/10.1098/rspb.2020.0443
Phylogeny of the Hawkmoth tribe Ambulycini: mitogenomes from museum specimens resolve major relationships
Timmermans, M., Daghmoumi, S., Glass, D., Hamilton, C., Kawahara, A. and Kitching, I. 2019. Phylogeny of the Hawkmoth tribe Ambulycini: mitogenomes from museum specimens resolve major relationships. Insect Systematics and Diversity. 3 (6). https://doi.org/10.1093/isd/ixz025
Phylogenomics resolves major relationships and reveals significant diversification rate shifts in the evolution of silk moths and relatives
Hamilton, C., St Laurent, R., Dexter, K., Kitching, I., Breinholt, J., Zwick, A., Timmermans, M., Barber, J. and Kawahara, A. 2019. Phylogenomics resolves major relationships and reveals significant diversification rate shifts in the evolution of silk moths and relatives. BMC Evolutionary Biology. 19 (1), pp. 1-13. https://doi.org/10.1186/s12862-019-1505-1
The contribution of mitochondrial metagenomics to large-scale data mining and phylogenetic analysis of Coleoptera
Linard, B., Crampton-Platt, A., Moriniere, J., Timmermans, M., Andújar, C., Arribas, P., Miller, K., Lipecki, J., Favreau, E., Hunter, A., Gómez-Rodríguez, C., Barton, C., Nie, R., Gillett, C., Breeschoten, T., Bocak, L. and Vogler, A. 2018. The contribution of mitochondrial metagenomics to large-scale data mining and phylogenetic analysis of Coleoptera. Molecular Phylogenetics and Evolution. 128, pp. 1-11. https://doi.org/10.1016/j.ympev.2018.07.008
Two European Cornus L. feeding leafmining moths, Antispila petryi Martini, 1899, sp. rev. and A. treitschkiella (Fischer von Röslerstamm, 1843) (Lepidoptera, Heliozelidae): an unjustified synonymy and overlooked range expansion
van Nieukerken, E., Lees, D., Doorenweerd, C., Koster, S., Bryner, R., Schreurs, A., Timmermans, M. and Sattler, K. 2018. Two European Cornus L. feeding leafmining moths, Antispila petryi Martini, 1899, sp. rev. and A. treitschkiella (Fischer von Röslerstamm, 1843) (Lepidoptera, Heliozelidae): an unjustified synonymy and overlooked range expansion. Nota Lepidopterologica. 41 (1), pp. 39-86. https://doi.org/10.3897/nl.41.22264
Nature read in tooth and fur: non-invasive sampling of the Pygmy Shrew (Sorex minutus Linnaeus, 1766) on Lundy for population genetics
Legall, N., Kett, S. and Timmermans, M. 2016. Nature read in tooth and fur: non-invasive sampling of the Pygmy Shrew (Sorex minutus Linnaeus, 1766) on Lundy for population genetics. Journal of the Lundy Field Society. 5, pp. 101-108.
Black rabbits on Lundy: Tudor treasures or post-war phonies?
Timmermans, M., Elmi, H. and Kett, S. 2018. Black rabbits on Lundy: Tudor treasures or post-war phonies? Journal of the Lundy Field Society. 6, pp. 105-113.
What's on the menu: Drosera rotundifolia diet determination using DNA data
Lekesyte, B., Kett, S. and Timmermans, M. 2018. What's on the menu: Drosera rotundifolia diet determination using DNA data. Journal of the Lundy Field Society. 6, pp. 55-64.
The phylogeny of Galerucinae (Coleoptera: Chrysomelidae) and the performance of mitochondrial genomes in phylogenetic inference compared to nuclear rRNA genes
Nie, R., Breeschoten, T., Timmermans, M., Nadein, K., Xue, H., Bai, M., Huang, Y., Yang, X. and Vogler, A. 2018. The phylogeny of Galerucinae (Coleoptera: Chrysomelidae) and the performance of mitochondrial genomes in phylogenetic inference compared to nuclear rRNA genes. Cladistics. 34 (2), pp. 113-130. https://doi.org/10.1111/cla.12196
Independent evolution of sexual dimorphism and female-limited mimicry in swallowtail butterflies (Papilio dardanus and Papilio phorcas)
Timmermans, M., Thompson, M., Collins, S. and Vogler, A. 2017. Independent evolution of sexual dimorphism and female-limited mimicry in swallowtail butterflies (Papilio dardanus and Papilio phorcas). Molecular Ecology. 26 (5), pp. 1273-1284. https://doi.org/10.1111/mec.14012
Intraspecific genetic variation in complex assemblages from mitochondrial metagenomics: comparison with DNA barcodes
Gómez-Rodríguez, C., Timmermans, M., Crampton-Platt, A. and Vogler, A. 2017. Intraspecific genetic variation in complex assemblages from mitochondrial metagenomics: comparison with DNA barcodes. Methods in Ecology and Evolution. 8 (2), pp. 248-256. https://doi.org/10.1111/2041-210X.12667
Uncovering trophic interactions in arthropod predators through DNA shotgun-sequencing of gut contents
Paula, D., Linard, B., Crampton-Platt, A., Srivathsan, A., Timmermans, M., Sujii, E., Pires, C., Souza, L., Andow, D. and Vogler, A. 2016. Uncovering trophic interactions in arthropod predators through DNA shotgun-sequencing of gut contents. PLoS ONE. 11 (9), pp. 1-14. https://doi.org/10.1371/journal.pone.0161841
Family-level sampling of mitochondrial genomes in coleoptera: compositional heterogeneity and phylogenetics
Timmermans, M., Barton, C., Haran, J., Ahrens, D., Culverwell, C., Ollikainen, A., Dodsworth, S., Foster, P., Bocak, L. and Vogler, A. 2016. Family-level sampling of mitochondrial genomes in coleoptera: compositional heterogeneity and phylogenetics. Genome Biology and Evolution. 8 (1), pp. 161-175. https://doi.org/10.1093/gbe/evv241
Mitogenomics of ‘old world Acraea’ butterflies reveals a highly divergent ‘Bematistes’
Timmermans, M., Lees, D., Thompson, M., Sáfián, S. and Brattström, O. 2016. Mitogenomics of ‘old world Acraea’ butterflies reveals a highly divergent ‘Bematistes’. Molecular Phylogenetics and Evolution. 97, pp. 233-241. https://doi.org/10.1016/j.ympev.2015.12.009
Rapid assembly of taxonomically validated mitochondrial genomes from historical insect collections
Timmermans, M., Viberg, C., Martin, G., Hopkins, K. and Vogler, A. 2016. Rapid assembly of taxonomically validated mitochondrial genomes from historical insect collections. Biological Journal of the Linnean Society. 117 (1), pp. 83-95. https://doi.org/10.1111/bij.12552
Metagenome skimming of insect specimen pools: potential for comparative genomics
Linard, B., Crampton-Platt, A., Gillett, C., Timmermans, M. and Vogler, A. 2015. Metagenome skimming of insect specimen pools: potential for comparative genomics. Genome Biology and Evolution. https://doi.org/10.1093/gbe/evv086
Soup to tree: the phylogeny of beetles inferred by mitochondrial metagenomics of a Bornean rainforest sample
Crampton-Platt, A., Timmermans, M., Gimmel, M., Kutty, S., Cockerill, T., Khen, C. and Vogler, A. 2015. Soup to tree: the phylogeny of beetles inferred by mitochondrial metagenomics of a Bornean rainforest sample. Molecular Biology and Evolution. 32 (9), pp. 2302-2316. https://doi.org/10.1093/molbev/msv111
Bulk de novo mitogenome assembly from pooled total DNA elucidates the phylogeny of weevils (Coleoptera: Curculionoidea)
Gillett, C., Crampton-Platt, A., Timmermans, M., Jordal, B., Emerson, B. and Vogler, A. 2014. Bulk de novo mitogenome assembly from pooled total DNA elucidates the phylogeny of weevils (Coleoptera: Curculionoidea). Molecular Biology and Evolution. 31 (8), pp. 2223-2237. https://doi.org/10.1093/molbev/msu154
Towards a mitogenomic phylogeny of Lepidoptera
Timmermans, M., Lees, D. and Simonsen, T. 2014. Towards a mitogenomic phylogeny of Lepidoptera. Molecular Phylogenetics and Evolution. 79, pp. 169-178. https://doi.org/10.1016/j.ympev.2014.05.031
Validating the power of mitochondrial metagenomics for community ecology and phylogenetics of complex assemblages
Gómez-Rodríguez, C., Crampton-Platt, A., Timmermans, M., Baselga, A. and Vogler, A. 2015. Validating the power of mitochondrial metagenomics for community ecology and phylogenetics of complex assemblages. Methods in Ecology and Evolution. 6 (8), pp. 883-894. https://doi.org/10.1111/2041-210X.12376
Interplay of robustness and plasticity of life-history traits drives ecotypic differentiation in thermally distinct habitats
Liefting, M., van Grunsven, R., Morrissey, M., Timmermans, M. and Ellers, J. 2015. Interplay of robustness and plasticity of life-history traits drives ecotypic differentiation in thermally distinct habitats. Journal of Evolutionary Biology. 28 (5), pp. 1057-1066. https://doi.org/10.1111/jeb.12629
Phylogenetic community ecology of soil biodiversity using mitochondrial metagenomics
Andújar, C., Arribas, P., Ruzicka, F., Crampton-Platt, A., Timmermans, M. and Vogler, A. 2015. Phylogenetic community ecology of soil biodiversity using mitochondrial metagenomics. Molecular Ecology. 24 (14), pp. 3603-3617. https://doi.org/10.1111/mec.13195
Characterising the phenotypic diversity of Papilio dardanus wing patterns using an extensive museum collection
Thompson, M. and Timmermans, M. 2014. Characterising the phenotypic diversity of Papilio dardanus wing patterns using an extensive museum collection. PLoS ONE. 9 (5), pp. 1-9. https://doi.org/10.1371/journal.pone.0096815
The evolutionary genetics of highly divergent alleles of the mimicry locus in Papilio dardanus
Thompson, M., Timmermans, M., Jiggins, C. and Vogler, A. 2014. The evolutionary genetics of highly divergent alleles of the mimicry locus in Papilio dardanus. BMC Evolutionary Biology. 14. https://doi.org/10.1186/1471-2148-14-140