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.
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Ackery, P.R. and Vane-Wright, R.I. (1984) Milkweed Butterflies: Their Cladistics and Biology. British Museum, Natural History, London.
Bates, H.W. (1862) Contributions to an insect fauna of the Amazon valley (Lepidoptera: Heliconidae). Trans. Linn. Soc. Lond. 23, 495-566.
Bates, H.W. (1879) [Commentary on Müller's paper]. Trans. Entomol. Soc. Lond. 1879, xxviii-xxix.
Benson, W.W. (1972) Natural selection for Müllerian mimicry in Heliconius erato in Costa Rica. Science 176, 936-939.
Boyden, T.C. (1976) Butterfly palatability and mimicry: experiments with Ameiva lizards. Evolution 30, 73-81.
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.
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.
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.
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.
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.
Brown, K.S. (1979) Ecologia Geográfica e Evolução nas Florestas Neotropicais. Universidade Estadual de Campinas, Campinas, Brazil, Livre de Docencia.
Brown, K.S. (1981) The biology of Heliconius and related genera. Ann. Rev. Entomol. 26, 427-456.
Brown, K.S. and Benson, W.W. (1974) Adaptive polymorphism associated with multiple Müllerian mimicry in Heliconius numata (Lepid.: Nymph.). Biotropica 69, 205-228.
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.
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.
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.
D'Abrera, B. (1984) Butterflies of the Neotropical Region, Vol., Part II. Danaidae, Ithomiidae, Heliconidae & Morphidae. Hill House, Ferny Creek, Victoria, Australia.
Deinert, E.I., Longino, J.T. and Gilbert, L.E. (1994) Mate competition in butterflies. Nature 370, 23-24.
Dixey, F.A. (1907) Recent developments in the theory of mimicry. Proc. Brit. Assoc. 1907, 1-2.
Dixey, F.A. (1909) On Müllerian mimicry and diaposematism. Trans. Entomol. Soc. Lond. 1908, 559-583.
Edmunds, M. (1974) Defence in Animals. Longmans, Harlow, Essex.
Eltringham, H. (1916) On specific and mimetic relationships in the genus Heliconius. Trans. Entomol. Soc. Lond. 1916, 101-148.
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.
Emsley, M.G. (1965) Speciation in Heliconius (Lep., Nymphalidae): morphology and geographic distribution. Zoologica, N.Y. 50, 191-254.
Engler, H., Spencer, K.C. and Gilbert, L.E. (2000) Preventing cyanide release from leaves. Nature 406, 144-145.
Futuyma, D.J. (1998) Evolutionary Biology. Sinauer, Sunderland, Mass.
Gilbert, L.E. (1983) Coevolution and Mimicry. In D.J. Futuyma and M. Slatkin (eds) Coevolution. Sinauer Associates, Sunderland, Mass, pp. 263-281.
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.
Huheey, J.E. (1988) Mathematical models of mimicry. Am. Nat. 131, S22-S41.
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.
Joron, M. and Mallet, J. (1998) Diversity in mimicry: paradox or paradigm? Trends Ecol. Evol. 13, 461-466.
Kapan, D. (2000) Three-butterfly system provides a field test of Müllerian mimicry. Nature 409, 338-340.
Linares, M. (1997a) The ghost of mimicry past: laboratory reconstitution of an extinct butterfly 'race'. Heredity 78, 628-635.
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.
Mallet, J. (1986a) Gregarious roosting and home range in Heliconius butterflies. Natl. Geogr. Res. 2, 198-215.
Mallet, J. (1986b) Hybrid zones in Heliconius butterflies in Panama, and the stability and movement of warning colour clines. Heredity 56, 191-202.
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.
Mallet, J. and Barton, N.H. (1989) Strong natural selection in a warning color hybrid zone. Evolution 43, 421-431.
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.
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.
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.
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.
Mallet, J., Jiggins, C.D. and McMillan, W.O. (1996) Mimicry meets the mitochondrion. Current Biol. 6, 937-940.
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.
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.
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.
Müller, F. (1879) Ituna and Thyridia; a remarkable case of mimicry in butterflies. Trans. Entomol. Soc. Lond. 1879, xx-xxix.
Nicholson, A.J. (1927) A new theory of mimicry in insects. Austral. Zool. 5, 10-104.
Owen, R.E. and Owen, A.R.G. (1984) Mathematical paradigms for mimicry: recurrent sampling. J. Theoret. Biol. 109, 217-247.
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.
Platt, A.P. (1983) Evolution of North American admiral butterflies (Limenitis: Nymphalidae). Bull. Entomol. Soc. Amer. 29, 10-22.
Plowright, R.C. and Owen, R.E. (1980) The evolutionary significance of bumble bee color patterns: a mimetic interpretation. Evolution 34, 622-637.
Ricklefs, R.E. and Miller, G.L. (2000) Ecology. Freeman, New York.
Ritland, D.B. (1990) Localized interspecific hybridization between mimetic Limenitis butterflies (Nymphalidae) in Florida. J. Lepid. Soc. 44, 163-173.
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.
Ritland, D.B. and Brower, L.P. (1991) The viceroy butterfly is not a Batesian mimic. Nature 350, 497-498.
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.
Speed, M.P. (1993) Muellerian mimicry and the psychology of predation. Anim. Behav. 45, 571-580.
Speed, M.P. (1999) Robot predators in virtual ecologies: the importance of memory in mimicry studies. Anim. Behav. 57, 203-213.
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.
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.
Thompson, J.N. (1994) The Coevolutionary Process. Chicago University Press, Chicago.
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.
Turner, J.R.G. (1977) Butterfly mimicry — the genetical evolution of an adaptation. Evol. Biol. 10, 163-206.
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.
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.
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.
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.
Waldbauer, G.P. (1988) Asynchrony between Batesian mimics and their models. Am. Nat. 131, s103-s121.
Wickler, W. (1968) Mimicry in Plants and Animals. McGraw-Hill, New York.
Williams, P.H. (1985) A preliminary cladistic investigation of relationships among the bumble bees (Hymenoptera: Apidae). Syst. Entomol. 10, 239-255.
Williams, P.H. (1991) The bumble bees of the Kashmir Himalaya (Hymenoptera: Apidae, Bombini). Bull. Brit. Mus. (Nat. Hist.), Entomol. 60, 1-204.
Williams, P.H. (1994) Phylogenetic relationships among bumble bees (Bombus Latr.): a reappraisal of morphological evidence. Syst. Entomol. 19, 327-344.
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Mallet, J. Causes and Consequences of a Lack of Coevolution in Müllerian mimicry. Evolutionary Ecology 13, 777–806 (1999). https://doi.org/10.1023/A:1011060330515
- advertising coloration
- Batesian mimicry
- warning colour