The evolutionary genetics of highly divergent alleles of the mimicry locus in Papilio dardanus

Article


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
TypeArticle
TitleThe evolutionary genetics of highly divergent alleles of the mimicry locus in Papilio dardanus
AuthorsThompson, M., Timmermans, M., Jiggins, C. and Vogler, A.
Abstract

Background: The phylogenetic history of genes underlying phenotypic diversity can offer insight into the evolutionary origin of adaptive traits. This is especially true where single genes have large phenotypic effects, for example in determining polymorphic mimicry in butterflies. Here, we characterise the evolutionary history of two candidate genes for the mimicry switch in the polymorphic Batesian mimic Papilio dardanus coding for the transcription factors engrailed and invected.
Results: We show that phased haplotypes associated with the dominant morphs f. poultoni and f. planemoides are phylogenetically highly divergent, in particular at non-synonymous sites. Some non-synonymous changes are shared between the divergent alleles suggesting either convergence or a shared ancestry. Gene trees for invected
do not show this pattern. Despite their great divergence, all engrailed alleles of P. dardanus were monophyletic with respect to alleles of closely related species. Phylogenetic analyses therefore reveal no evidence for introgression from other species. A McDonald-Kreitman test conducted on a population sample from South Africa confirms a significant excess of intraspecific non-synonymous diversity in P. dardanus engrailed, suggesting long-term balanced polymorphism at this locus.
Conclusions: The divergence between engrailed haplotypes suggests an evolutionary history distorted by selection with multiple changes reflecting recurrent selective sweeps. The high level of intraspecific polymorphism observed is characteristic of balancing selection on this locus, as expected if the gene engrailed is under phenotypic selection for the maintenance of multiple mimetic morphs. Non-synonymous changes in key functional portions of a major transcription factor are likely to be deleterious but if maintained in a dominant allele at low frequency, heterozygosity would reduce the associated genetic load.

KeywordsMimicry, balanced polymorphism, supergene, engrailed, phylogenetics, molecular evolution
PublisherBioMed Central
JournalBMC Evolutionary Biology
ISSN1471-2148
Publication dates
Print31 Aug 2014
Publication process dates
Deposited29 Apr 2015
Accepted19 Jun 2014
Output statusPublished
Publisher's version
File Access Level
Open
Copyright Statement

© 2014 Thompson et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Digital Object Identifier (DOI)https://doi.org/10.1186/1471-2148-14-140
LanguageEnglish
Permalink -

https://repository.mdx.ac.uk/item/8531y

Download files


Publisher's version
1471-2148-14-140.pdf
File access level: Open

  • 40
    total views
  • 8
    total downloads
  • 1
    views this month
  • 0
    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
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
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
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
Comparative genomics of the mimicry switch in Papilio dardanus
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
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