Evolutionary Ecology

, Volume 13, Issue 7–8, pp 777–806 | Cite as

Causes and Consequences of a Lack of Coevolution in Müllerian mimicry

  • James Mallet


Müllerian mimicry, in which both partners are unpalatable to predators, is often used as an example of a coevolved mutualism. However, it is theoretically possible that some Müllerian mimics are parasitic if a weakly defended mimic benefits at the expense of a more highly defended model, a phenomenon known as ‘quasi-Batesian mimicry’. The theory expounded by Müller and extended here for unequal unpalatability, on the other hand, suggests that quasi-Batesian mimicry should be rare in comparison with classical, or mutualistic Müllerian mimicry. Evolutionarily, quasi-Batesian mimicry has consequences similar to classical Batesian mimicry, including unilateral ‘advergence’ of the mimic to the model, and diversifying frequency-dependent selection on the mimic which may lead to mimetic polymorphism. In this paper, theory and empirical evidence for mutual benefit and coevolution in Müllerian mimicry are reviewed. I use examples from well-known insect Müllerian mimicry complexes: the Limenitis–Danaus (Nymphalidae) system in North America, the Bombus–Psithyrus (Apidae) system in the north temperate zone, and the Heliconius–Laparus (Nymphalidae) system in tropical America. These give abundant evidence for unilateral advergence, and no convincing evidence, to my knowledge, for coevolved mutual convergence. Furthermore, mimetic polymorphisms are not uncommon. Yet classical mutualistic Müllerian mimicry, coupled with spatial (and possibly temporal) variation in model abundances convincingly explain these apparent anomalies without recourse to a quasi-Batesian explanation. Nevertheless, the case against classical Müllerian mimicry is not totally disproved, and should be investigated further. I hope that this tentative analysis of actual mimicry rings may encourage others to look for evidence of coevolution and quasi-Batesian effects in a variety of other Müllerian mimicry systems.

advertising coloration aposematism Batesian mimicry mimicry mutualism signalling warning colour 


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  1. Ackery, P.R. and Vane-Wright, R.I. (1984) Milkweed Butterflies: Their Cladistics and Biology. British Museum, Natural History, London.Google Scholar
  2. Bates, H.W. (1862) Contributions to an insect fauna of the Amazon valley (Lepidoptera: Heliconidae). Trans. Linn. Soc. Lond. 23, 495-566.Google Scholar
  3. Bates, H.W. (1879) [Commentary on Müller's paper]. Trans. Entomol. Soc. Lond. 1879, xxviii-xxix.Google Scholar
  4. Benson, W.W. (1972) Natural selection for Müllerian mimicry in Heliconius erato in Costa Rica. Science 176, 936-939.PubMedGoogle Scholar
  5. Boyden, T.C. (1976) Butterfly palatability and mimicry: experiments with Ameiva lizards. Evolution 30, 73-81.CrossRefGoogle Scholar
  6. Brower, A.V.Z. (1996) Parallel race formation and the evolution of mimicry in Heliconius butterflies: a phylogenetic hypothesis from mitochondrial DNA sequences. Evolution 50, 195-221.CrossRefGoogle Scholar
  7. Brower, A.V.Z. and Egan, M.G. (1997) Cladistic analysis of Heliconius butterflies and relatives (Nymphalidae: Heliconiiti): a revised phylogenetic position for Eueides based on sequences from mtDNA and a nuclear gene. Proc. Roy. Soc. Lond. B 264, 969-977.CrossRefGoogle Scholar
  8. Brower, J.V.Z. (1958) Experimental studies of mimicry in some North American butterflies. Part I. The monarch, Danaus plexippus, and viceroy, Limenitis archippus archippus. Evolution 12, 32-47.CrossRefGoogle Scholar
  9. Brower, L.P. (1984) Chemical defence in butterflies. In R.I. Vane-Wright and P.R. Ackery (eds) The Biology of Butterflies. Academic Press, London (Symposia of the Royal Entomological Society of London; 11), pp. 109-134.Google Scholar
  10. Brower, L.P., Brower, J.V.Z. and Collins, C.T. (1963) Experimental studies of mimicry. 7. Relative palatability and Müllerian mimicry among Neotropical butterflies of the subfamily Heliconiinae. Zoologica, N.Y. 48, 65-84.Google Scholar
  11. Brown, K.S. (1979) Ecologia Geográfica e Evolução nas Florestas Neotropicais. Universidade Estadual de Campinas, Campinas, Brazil, Livre de Docencia.Google Scholar
  12. Brown, K.S. (1981) The biology of Heliconius and related genera. Ann. Rev. Entomol. 26, 427-456.CrossRefGoogle Scholar
  13. Brown, K.S. and Benson, W.W. (1974) Adaptive polymorphism associated with multiple Müllerian mimicry in Heliconius numata (Lepid.: Nymph.). Biotropica 69, 205-228.CrossRefGoogle Scholar
  14. Brown, K.S., Sheppard, P.M. and Turner, J.R.G. (1974) Quaternary refugia in tropical America: evidence from race formation in Heliconius butterflies. Proc. Roy. Soc. Lond. B 187, 369-378.CrossRefGoogle Scholar
  15. Chai, P. (1986) Field observations and feeding experiments on the responses of rufous-tailed jacamars (Galbula ruficauda) to free-flying butterflies in a tropical rainforest. Biol. J. Linn. Soc. 29, 166-189.Google Scholar
  16. Chai, P. (1990) Relationships between visual characteristics of rainforest butterflies and responses of a specialized insectivorous bird. In M. Wicksten (ed.) Adaptive Coloration in Invertebrates. Texas A&M University Sea Grant College Program, College Station, TX, USA (Proceedings of a Symposium Sponsored by the American Society of Zoologists), pp. 31-60.Google Scholar
  17. D'Abrera, B. (1984) Butterflies of the Neotropical Region, Vol., Part II. Danaidae, Ithomiidae, Heliconidae & Morphidae. Hill House, Ferny Creek, Victoria, Australia.Google Scholar
  18. Deinert, E.I., Longino, J.T. and Gilbert, L.E. (1994) Mate competition in butterflies. Nature 370, 23-24.CrossRefGoogle Scholar
  19. Dixey, F.A. (1907) Recent developments in the theory of mimicry. Proc. Brit. Assoc. 1907, 1-2.Google Scholar
  20. Dixey, F.A. (1909) On Müllerian mimicry and diaposematism. Trans. Entomol. Soc. Lond. 1908, 559-583.Google Scholar
  21. Edmunds, M. (1974) Defence in Animals. Longmans, Harlow, Essex.Google Scholar
  22. Eltringham, H. (1916) On specific and mimetic relationships in the genus Heliconius. Trans. Entomol. Soc. Lond. 1916, 101-148.Google Scholar
  23. Emsley, M.G. (1964) The geographical distribution of the color-pattern components of Heliconius erato and Heliconius melpomene with genetical evidence for the systematic relationship between the two species. Zoologica, N.Y. 49, 245-286.Google Scholar
  24. Emsley, M.G. (1965) Speciation in Heliconius (Lep., Nymphalidae): morphology and geographic distribution. Zoologica, N.Y. 50, 191-254.Google Scholar
  25. Engler, H., Spencer, K.C. and Gilbert, L.E. (2000) Preventing cyanide release from leaves. Nature 406, 144-145.PubMedCrossRefGoogle Scholar
  26. Futuyma, D.J. (1998) Evolutionary Biology. Sinauer, Sunderland, Mass.Google Scholar
  27. Gilbert, L.E. (1983) Coevolution and Mimicry. In D.J. Futuyma and M. Slatkin (eds) Coevolution. Sinauer Associates, Sunderland, Mass, pp. 263-281.Google Scholar
  28. Gilbert, L.E. (1984) The biology of butterfly communities. In R.I. Vane-Wright and P.R. Ackery (eds) The Biology of Butterflies. Academic Press, London (Symposia of the Royal Entomological Society of London; 11), pp. 41-54.Google Scholar
  29. Huheey, J.E. (1988) Mathematical models of mimicry. Am. Nat. 131, S22-S41.CrossRefGoogle Scholar
  30. Jiggins, C.D., McMillan, W.O., Neukirchen, W. and Mallet, J. (1996) What can hybrid zones tell us about speciation? The case of Heliconius erato and H. himera (Lepidoptera: Nymphalidae). Biol. J. Linn. Soc. 59, 221-242.CrossRefGoogle Scholar
  31. Joron, M. and Mallet, J. (1998) Diversity in mimicry: paradox or paradigm? Trends Ecol. Evol. 13, 461-466.CrossRefGoogle Scholar
  32. Kapan, D. (2000) Three-butterfly system provides a field test of Müllerian mimicry. Nature 409, 338-340.CrossRefGoogle Scholar
  33. Linares, M. (1997a) The ghost of mimicry past: laboratory reconstitution of an extinct butterfly 'race'. Heredity 78, 628-635.CrossRefGoogle Scholar
  34. Linares, M. (1997b) Origin of neotropical mimetic diversity from a three-way hybrid zone of Heliconius cydno butterflies. In H. Ulrich (ed.) Tropical Diversity and Systematics. Zoologisches Forschunginstitut und Museum Alexander Koenig, Bonn. (Proceedings of the International Symposium on Biodiversity and Systematics in Tropical Ecosystems, Bonn, 1994), pp. 93-108.Google Scholar
  35. Mallet, J. (1986a) Gregarious roosting and home range in Heliconius butterflies. Natl. Geogr. Res. 2, 198-215.Google Scholar
  36. Mallet, J. (1986b) Hybrid zones in Heliconius butterflies in Panama, and the stability and movement of warning colour clines. Heredity 56, 191-202.Google Scholar
  37. Mallet, J. (1993) Speciation, raciation, and color pattern evolution in Heliconius butterflies: evidence from hybrid zones. In R.G. Harrison (ed.) Hybrid Zones and the Evolutionary Process. Oxford University Press, New York, pp. 226-260.Google Scholar
  38. Mallet, J. and Barton, N.H. (1989) Strong natural selection in a warning color hybrid zone. Evolution 43, 421-431.CrossRefGoogle Scholar
  39. Mallet, J. and Gilbert, L.E. (1995) Why are there so many mimicry rings? Correlations between habitat, behaviour and mimicry in Heliconius butterflies. Biol. J. Linn. Soc. 55, 159-180.CrossRefGoogle Scholar
  40. Mallet, J. and Jackson, D.A. (1980) The ecology and social behaviour of the Neotropical butterfly Heliconius xanthocles Bates in Colombia. Zool. J. Linn. Soc. 70, 1-13.Google Scholar
  41. Mallet, J. and Joron, M. (1999) The evolution of diversity in warning colour and mimicry: polymorphisms, shifting balance, and speciation. Ann. Rev. Ecol. Syst. 30, 201-233.CrossRefGoogle Scholar
  42. Mallet, J., Barton, N., Lamas, G., Santisteban, J., Muedas, M. and Eeley, H. (1990) Estimates of selection and gene flow from measures of cline width and linkage disequilibrium in Heliconius hybrid zones. Genetics 124, 921-936.PubMedGoogle Scholar
  43. Mallet, J., Jiggins, C.D. and McMillan, W.O. (1996) Mimicry meets the mitochondrion. Current Biol. 6, 937-940.CrossRefGoogle Scholar
  44. Mallet, J., McMillan, W.O. and Jiggins, C.D. (1998a) Mimicry and warning color at the boundary between races and species. In D.J. Howard and S.H. Berlocher (eds) Endless Forms: Species and Speciation. Oxford University Press, New York, pp. 390-403.Google Scholar
  45. Mallet, J., McMillan, W.O. and Jiggins, C.D. (1998b) Estimating the mating behavior of a pair of hybridizing Heliconius species in the wild. Evolution 52, 503-510.CrossRefGoogle Scholar
  46. Marshall, G.A.K. (1908) On diaposematism, with reference to some of the limitations of the Müllerian hypothesis of mimicry. Trans. Entomol. Soc. Lond. 1908, 93-142.Google Scholar
  47. Müller, F. (1879) Ituna and Thyridia; a remarkable case of mimicry in butterflies. Trans. Entomol. Soc. Lond. 1879, xx-xxix.Google Scholar
  48. Nicholson, A.J. (1927) A new theory of mimicry in insects. Austral. Zool. 5, 10-104.Google Scholar
  49. Owen, R.E. and Owen, A.R.G. (1984) Mathematical paradigms for mimicry: recurrent sampling. J. Theoret. Biol. 109, 217-247.CrossRefGoogle Scholar
  50. Pinheiro, C.E.G. (1996) Palatability and escaping ability in neotropical butterflies: tests with wild kingbirds (Tyrannus melancholicus). Biol. J. Linn. Soc. 59, 351-365.CrossRefGoogle Scholar
  51. Platt, A.P. (1983) Evolution of North American admiral butterflies (Limenitis: Nymphalidae). Bull. Entomol. Soc. Amer. 29, 10-22.Google Scholar
  52. Plowright, R.C. and Owen, R.E. (1980) The evolutionary significance of bumble bee color patterns: a mimetic interpretation. Evolution 34, 622-637.CrossRefGoogle Scholar
  53. Ricklefs, R.E. and Miller, G.L. (2000) Ecology. Freeman, New York.Google Scholar
  54. Ritland, D.B. (1990) Localized interspecific hybridization between mimetic Limenitis butterflies (Nymphalidae) in Florida. J. Lepid. Soc. 44, 163-173.Google Scholar
  55. Ritland, D.B. (1991) Revising a classic butterfly mimicry scenario: demonstration of Müllerian mimicry between Florida viceroys (Limenitis archippus floridensis) and queens (Danaus gilippus berenice). Evolution 45, 918-934.CrossRefGoogle Scholar
  56. Ritland, D.B. and Brower, L.P. (1991) The viceroy butterfly is not a Batesian mimic. Nature 350, 497-498.CrossRefGoogle Scholar
  57. Sheppard, P.M., Turner, J.R.G., Brown, K.S., Benson, W.W. and Singer, M.C. (1985) Genetics and the evolution of muellerian mimicry in Heliconius butterflies. Philos. Trans. Royal Soc. Lond. B 308, 433-613.Google Scholar
  58. Speed, M.P. (1993) Muellerian mimicry and the psychology of predation. Anim. Behav. 45, 571-580.CrossRefGoogle Scholar
  59. Speed, M.P. (1999) Robot predators in virtual ecologies: the importance of memory in mimicry studies. Anim. Behav. 57, 203-213.PubMedCrossRefGoogle Scholar
  60. Speed, M.P. and Turner, J.R.G. (1999) Learning and memory in mimicry: II. Do we understand the mimicry spectrum? Biol. J. Linn. Soc. 67, 281-312.CrossRefGoogle Scholar
  61. Speed, M.P., Alderson, N.J., Hardman, C. and Ruxton, G.D. (2000) Testing Mullerian mimicry: an experiment with wild birds. Proc. Roy. Soc. Lond. B 267, 725-731.CrossRefGoogle Scholar
  62. Thompson, J.N. (1994) The Coevolutionary Process. Chicago University Press, Chicago.Google Scholar
  63. Turner, J.R.G. (1976) Muellerian mimicry: classical “beanbag” evolution and the role of ecological islands in adaptive race formation. In S. Karlin and E. Nevo (eds) Population Genetics and Ecology. Academic Press, New York, pp. 185-218.Google Scholar
  64. Turner, J.R.G. (1977) Butterfly mimicry — the genetical evolution of an adaptation. Evol. Biol. 10, 163-206.Google Scholar
  65. Turner, J.R.G. (1978) Why male butterflies are non-mimetic: natural selection, sexual selection, group selection, modification and sieving. Biol. J. Linn. Soc. 10, 385-432.Google Scholar
  66. Turner, J.R.G. (1984) Mimicry: the palatability spectrum and its consequences. In R.I. Vane-Wright and P.R. Ackery (eds) The Biology of Butterflies. Academic Press, London (Symposia of the Royal Entomological Society of London; 11), pp. 141-161.Google Scholar
  67. Turner, J.R.G. (1995) Mimicry as a model for coevolution. In R. Arai, M. Kato and Y. Doi (eds) Biodiversity and Evolution. National Science Museum Foundation, Tokyo, pp. 131-150.Google Scholar
  68. Turner, J.R.G. and Mallet, J.L.B. (1996) Did forest islands drive the diversity of warningly coloured butterflies? Biotic drift and the shifting balance. Philos. Trans. Royal Soc. Lond. B 351, 835-845.Google Scholar
  69. Waldbauer, G.P. (1988) Asynchrony between Batesian mimics and their models. Am. Nat. 131, s103-s121.CrossRefGoogle Scholar
  70. Wickler, W. (1968) Mimicry in Plants and Animals. McGraw-Hill, New York.Google Scholar
  71. Williams, P.H. (1985) A preliminary cladistic investigation of relationships among the bumble bees (Hymenoptera: Apidae). Syst. Entomol. 10, 239-255.Google Scholar
  72. Williams, P.H. (1991) The bumble bees of the Kashmir Himalaya (Hymenoptera: Apidae, Bombini). Bull. Brit. Mus. (Nat. Hist.), Entomol. 60, 1-204.Google Scholar
  73. Williams, P.H. (1994) Phylogenetic relationships among bumble bees (Bombus Latr.): a reappraisal of morphological evidence. Syst. Entomol. 19, 327-344.Google Scholar

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© Kluwer Academic Publishers 1999

Authors and Affiliations

  • James Mallet
    • 1
  1. 1.Galton Laboratory, Department of BiologyUniversity College LondonLondonEngland (

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