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Dimorphic Female-Limited Batesian Mimicry in Two Papilio Butterflies

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Spectrum of Sex

Abstract

To deceive predators, palatable species often resemble colour patterns and morphology of unpalatable species, which is called Batesian mimicry. In two closely related swallowtail butterflies, Papilio polytes and P. memnon, only females mimic model poisonous butterflies, and females have mimetic and non-mimetic types. Responsible loci (H for P. polytes and A for P. memnon) for mimicry were identified in the homologous chromosomal region as supergene containing doublesex (dsx) and a few genes. The supergene sequences between H and h (A and a) alleles are highly diversified due to recombination suppression, which is caused by chromosomal inversion in P. polytes, but no inversion in P. memnon. In both species, higher expression of mimetic dsx (dsx-H and dsx-A) in female pupal wings induced mimetic colouration, and the expression of genes inside the supergene was similar to that of mimetic dsx. In contrast, colouration patterns and supergene structure were considerably different between the two species. Furthermore, the chemical features of pale-yellow in hindwings, which are important both for sexual and mimicry strategies in P. polytes, seemed different in P. memnon. Here, we summarise the similarities and differences in mimetic traits between two butterflies and discuss how two mimicry supergenes have evolved.

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References

  • Ando T, Fujiwara H (2013) Electroporation-mediated somatic transgenesis for rapid functional analysis in insects. Development 140:454–458

    Article  CAS  PubMed  Google Scholar 

  • Bates HW (1862) Contributions to an insect fauna of the Amazon Valley (lepidoptera: Heliconidae). Trans Linn Soc Lond 23:495–556

    Article  Google Scholar 

  • Charlesworth D, Charlesworth B (1975) Theoretical genetics of Batesian mimicry II. Evolution of supergenes. J Theoretic Biol 55:305–324

    Article  CAS  Google Scholar 

  • Clark R, Brown SM, Collins SC, Jiggins CD, Heckel DG, Vogler AP (2008) Colour pattern specification in the mocker swallowtail Papilio dardanus: the transcription factor invected is a candidate for the mimicry locus H. Proc R Soc B 275:1181–1188

    Article  PubMed  PubMed Central  Google Scholar 

  • Clarke CA, Sheppard PM (1960) The genetics of Papilio dardanus Brown. II. Races dardanus, polytrophus, meseres, and tibullus. Genetics 45:439–456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke CA, Sheppard PM (1972) The genetics of the mimetic butterfly Papilio polytes L. Philos Trans R Soc Lond Ser B Biol Sci 26:431–458

    Google Scholar 

  • Clarke CA, Sheppard PM, Thornton IWB (1968) The genetics of the mimetic butterfly Papilio memnon L. Philos Trans R Soc Lond Ser B Biol Sci 254:37–89

    Google Scholar 

  • Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, Oxford

    Book  Google Scholar 

  • Gutiérrez-Valencia J, Hughes PW, Berdan EL, Slotte T (2021) The genomic architecture and evolutionary fates of supergenes. Genom Biol Evol 13:evab057

    Article  Google Scholar 

  • Huheey JE (1988) Mathematical models of mimicry. Am Nat 131:S22–S41

    Article  Google Scholar 

  • Iijima T, Kajitani R, Komata S, Lin CP, Sota T, Itoh T, Fujiwara H (2018) Parallel evolution of Batesian mimicry supergene in two Papilio butterflies, P. polytes and P. memnon. Sci Adv 4:eaao5416

    Article  PubMed  PubMed Central  Google Scholar 

  • Iijima T, Yoda S, Fujiwara H (2019) The mimetic wing pattern of Papilio polytes butterflies is regulated by a doublesexorchestrated gene network. Commun Biol 2:1–10

    Article  CAS  Google Scholar 

  • Joron M et al (2011) Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477:203–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitamura T, Imafuku M (2015) Behavioural mimicry in flight path of Batesian intraspecific polymorphic butterfly Papilio polytes. Proc Biol Sci 282:20150483

    PubMed  PubMed Central  Google Scholar 

  • Komata S, Kitamura T, Fujiwara H (2020) Batesian mimicry has evolved with deleterious effects of the pleiotropic gene doublesex. Sci Rep 10:1–8

    Article  Google Scholar 

  • Komata S, Lin CP, Iijima T, Fujiwara H, Sota T (2016) Identification of doublesex alleles associated with the female-limited Batesian mimicry polymorphism in Papilio memnon. Sci Rep 6:1–7

    Article  Google Scholar 

  • Komata S, Lin CP, Sota T (2017) Temporal dynamics of the mimetic allele frequency at the doublesex locus, which controls polymorphic Batesian mimicry in Papilio memnon butterflies. Sci Rep 7:1–6

    Article  CAS  Google Scholar 

  • Komata S, Lin CP, Sota T (2018) Do juvenile developmental and adult body characteristics differ among genotypes at the doublesex locus that controls female-limited Batesian mimicry polymorphism in Papilio memnon?: a test for the “cost of mimicry” hypothesis. J Insect Physiol 107:1–6

    Article  CAS  PubMed  Google Scholar 

  • Komata S, Yoda S, KonDo Y, Shinozaki S, Tamai K, Fujiwara H (2022a) Functional involvement of multiple genes as members of the supergene unit in the female-limited Batesian mimicry of Papilio polytes. bioRxiv. https://doi.org/10.1101/2022.02.21.480812

  • Komata S, Lin CP, Fujiwara H (2022b) doublesex controls both hindwing and abdominal mimicry traits in the female-limited batesian mimicry of Papilio memnon. Front Insect Sci 2:2929518

    Article  Google Scholar 

  • Komata S, Kajitani R, Itoh T, Fujiwara H (2022c) Genomic architecture and functional unit of mimicry supergene in female limited Batesian mimic Papilio butterflies. Phil Trans Royal Soc B 377:1856

    Article  Google Scholar 

  • Kunte K (2009a) Female-limited mimetic polymorphism: a review of theories and a critique of sexual selection as balancing selection. Anim Behav 78:1029–1036

    Article  Google Scholar 

  • Kunte K (2009b) The diversity and evolution of Batesian mimicry in Papilio swallowtail butterflies. Evolution 63:2707–2716

    Article  PubMed  Google Scholar 

  • Kunte K, Zhang W, Tenger-Trolander A, Palmer DH, Martin A, Reed RD, Mullen SP, Kronforst MR (2014) doublesex is a mimicry supergene. Nature 507:229–232

    Article  CAS  PubMed  Google Scholar 

  • Kupper C et al (2016) A supergene determines highly divergent male reproductive morphs in the ruff. Nat Genet 48:79–83

    Article  CAS  PubMed  Google Scholar 

  • Lamichhaney S et al (2016) Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nat Genet 48:84–88

    Article  CAS  PubMed  Google Scholar 

  • Li J et al (2016) Genetic architecture and evolution of the S locus supergene in Primula vulgaris. Nat Plants 2:16188

    Article  CAS  PubMed  Google Scholar 

  • Müller F (1879) Ituna and Thyridia: a remarkable case of mimicry in butterflies. Trans Entomol Soc Lond 1879:20–29

    Google Scholar 

  • Nishikawa H, Iga M, Yamaguchi J, Saito K, Kataoka H, Suzuki Y, Sugano S, Fujiwara H (2013) Molecular basis of wing coloration in a Batesian mimic butterfly, Papilio polytes. Sci Rep 3:1–9

    Article  Google Scholar 

  • Nishikawa H et al (2015) A genetic mechanism for female-limited Batesian mimicry in Papilio butterfly. Nat Genet 47:405–409

    Article  CAS  PubMed  Google Scholar 

  • Ohsaki N (2005) A common mechanism explaining the evolution of female-limited and both-sex Batesian mimicry in butterflies. J Anim Ecol 74:728–734

    Article  Google Scholar 

  • Ohsaki N (2009) Gitai no Shinka: Darwin mo Gokai shita 150 Nen no Nazo wo Toku (the evolution of mimicry: solve the 150-year-old mystery that has puzzled biologists ever since Charles Darwin) Kaiyusha, Tokyo

    Google Scholar 

  • Palmer DH, Kronforst MR (2020) A shared genetic basis of mimicry across swallowtail butterflies points to ancestral co-option of doublesex. Nat Commun 11:6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pearse DE et al (2019) Sex-dependent dominance maintains migration supergene in rainbow trout. Nat Ecol Evol 3:1731–1742

    Article  PubMed  Google Scholar 

  • Rembold H, Umebachi Y (1985) In: Schlossberger HG, Kochen W, Linzen B, Steinhart H (eds) The structure of papiliochrome II, the yellow wing pigment of the papilionid butterflies. In Progress in tryptophan and serotonin research. Walter de Gruyter, Berlin, pp 743–746

    Google Scholar 

  • Ruxton GD, Sherratt TN, Speed M (2004) Avoiding attack: the evolutionary ecology of crypsis, Warning Signals and Mimicry. Oxford University Press, Oxford

    Book  Google Scholar 

  • Shore JS et al (2019) The long and short of the S-locus in Turnera (Passifloraceae). New Phytol 224:1316–1329

    Article  CAS  PubMed  Google Scholar 

  • Stavenga DG, Matsushita A, Arikawa K (2015) Combined pigmentary and structural effects tune wing scale coloration to color vision in the swallowtail butterfly Papilio xuthus. Zool Lett 1:1–10

    Article  Google Scholar 

  • Tuttle EM et al (2016) Divergence and functional degradation of a sex chromosome-like supergene. Curr Biol 26:344–350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Umebachi Y (1978) Red pigments in the wings of papilionid butterflies. Extraction and purification. Sci Rep Kanazawa Univ 23:119–128

    CAS  Google Scholar 

  • Umebachi Y (1985) Papiliochrome, a new pigment group of butterfly. Zool Sci 2:163–174

    CAS  Google Scholar 

  • Vane-Wright RI (1980) On the definition of mimicry. Biol J Linne Soc 13:1–6

    Article  Google Scholar 

  • Wallace AR (1865) On the phenomena of variation and geographical distribution as illustrated by the Papilionidae of the Malayan region. Trans Linn Soc (Lond) 25:1–71

    Article  Google Scholar 

  • Wang J et al (2013) A Y-like social chromosome causes alternative colony organization in fire ants. Nature 493:664–668

    Article  CAS  PubMed  Google Scholar 

  • Westerman EL, Antonson N, Kreutzmann S, Peterson A, Pineda S, Kronforst MR, Olson-Manning CF (2019) Behaviour before beauty: signal weighting during mate selection in the butterfly Papilio polytes. Ethology 125:565–574

    Article  PubMed  PubMed Central  Google Scholar 

  • Yan Z et al (2020) Evolution of a supergene that regulates a trans-species social polymorphism. Nat Ecol Evol 4:240–249

    Article  PubMed  Google Scholar 

  • Yoda S et al (2021) Genetic switch in UV response of mimicry-related pale-yellow colors in Batesian mimic butterfly, Papilio polytes. Sci Adv 7:eabd6475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Chiba, Japan

    Haruhiko Fujiwara & Shinya Komata

Authors
  1. Haruhiko Fujiwara
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  2. Shinya Komata
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Correspondence to Haruhiko Fujiwara .

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Editors and Affiliations

  1. Graduate School of Science, Nagoya University, Nagoya, Aichi, Japan

    Minoru Tanaka

  2. Graduation School of Frontier Biosciences, Osaka University, Suita, Osaka, Japan

    Makoto Tachibana

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Fujiwara, H., Komata, S. (2022). Dimorphic Female-Limited Batesian Mimicry in Two Papilio Butterflies. In: Tanaka, M., Tachibana, M. (eds) Spectrum of Sex. Springer, Singapore. https://doi.org/10.1007/978-981-19-5359-0_3

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