Independent evolution of sexual dimorphism and female-limited mimicry in swallowtail butterflies (Papilio dardanus and Papilio phorcas)

Article


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
TypeArticle
TitleIndependent evolution of sexual dimorphism and female-limited mimicry in swallowtail butterflies (Papilio dardanus and Papilio phorcas)
AuthorsTimmermans, M., Thompson, M., Collins, S. and Vogler, A.
Abstract

Several species of Swallowtail butterflies (genus Papilio) are Batesian mimics that express multiple mimetic female forms, while the males are monomorphic and non-mimetic. The evolution of such sex-limited mimicry may involve sexual dimorphism arising first and mimicry subsequently. Such a stepwise scenario through a non-mimetic, sexually dimorphic stage has been proposed for two closely related sexually dimorphic species; P. phorcas, a non-mimetic species with two female forms, and P. dardanus, a female-limited polymorphic mimetic species. Their close relationship indicates that female-limited polymorphism could be a shared derived character of the two species. Here we present a phylogenomic analysis of the dardanus group using 3964 nuclear loci and whole mitochondrial genomes showing that they are not sister species, and thus that the sexually-dimorphic state has arisen independently in the two species. Non-homology of the female polymorphism in both species is supported by population genetic analysis of engrailed, the presumed mimicry switch locus in P. dardanus. McDonald-Kreitman tests performed on SNPs in engrailed showed the signature of balancing selection in a polymorphic population of P. dardanus, but not in monomorphic populations, nor in the non-mimetic P. phorcas. Hence the wing polymorphism does not balance polymorphisms in engrailed in P. phorcas. Equally, unlike in P. dardanus, none of the SNPs in P. phorcas engrailed were associated with either female morph. We conclude that sexual dimorphism due to female polymorphism evolved independently in both species from monomorphic, non-mimetic states. While sexual selection may drive male-female dimorphism in non-mimetic species, in mimetic Papilios natural selection for protection from predators in females is an alternative route to sexual dimorphism.

LanguageEnglish
PublisherWiley
JournalMolecular Ecology
ISSN0962-1083
Publication dates
Online08 Feb 2017
Publication process dates
Deposited25 Jan 2017
Accepted03 Jan 2017
Accepted author manuscript
Copyright Statement

This is the peer reviewed version of the following article: Timmermans, M. J. T. N., Thompson, M. J., Collins, S. and Vogler, A. P. (2017), Independent evolution of sexual dimorphism and female-limited mimicry in swallowtail butterflies (Papilio dardanus and Papilio phorcas). Mol Ecol. doi:10.1111/mec.14012, which has been published in final form at http://doi.org/10.1111/mec.14012. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.

Additional information

Accepted manuscript online: 18 January 2017
Version of record online: 8 February 2017

Digital Object Identifier (DOI)https://doi.org/10.1111/mec.14012
Permalink -

https://repository.mdx.ac.uk/item/86w77

Download files

  • 34
    total views
  • 11
    total downloads
  • 7
    views this month
  • 2
    downloads this month

Export as

Related outputs

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
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.
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.
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
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
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
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