Evolution of a mimicry supergene from a multilocus architecture

The origin and evolution of supergenes have long fascinated evolutionary biologists. In the polymorphic butterfly Heliconius numata, a supergene controls the switch between multiple different forms, and results in near-perfect mimicry of model species. Here, we use a morphometric analysis to quantify the variation in wing pattern observed in two broods of H. numata with different alleles at the supergene locus, ‘P’. Further, we genotype the broods to associate the variation we capture with genetic differences. This allows us to begin mapping the quantitative trait loci that have minor effects on wing pattern. In addition to finding loci on novel chromosomes, our data, to our knowledge, suggest for the first time that ancestral colour-pattern loci, known to have major effects in closely related species, may contribute to the wing patterns displayed by H. numata, despite the large transfer of effects to the supergene.

[1]  Camilo Salazar,et al.  Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry , 2011, Nature.

[2]  Simon W. Baxter,et al.  Genomic Hotspots for Adaptation: The Population Genetics of Müllerian Mimicry in Heliconius erato , 2010, PLoS genetics.

[3]  James Mallet,et al.  Genomic Hotspots for Adaptation: The Population Genetics of Müllerian Mimicry in the Heliconius melpomene Clade , 2010, PLoS genetics.

[4]  L. Cook,et al.  Achiasmatic oogenesis in the Heliconiine butterflies , 2009 .

[5]  C. Jiggins,et al.  Butterfly speciation and the distribution of gene effect sizes fixed during adaptation , 2009, Heredity.

[6]  J. Oliver,et al.  Accommodating natural and sexual selection in butterfly wing pattern evolution , 2009, Proceedings of the Royal Society B: Biological Sciences.

[7]  S. Humphray,et al.  Convergent Evolution in the Genetic Basis of Müllerian Mimicry in Heliconius Butterflies , 2008, Genetics.

[8]  P. Brakefield,et al.  The Male Sex Pheromone of the Butterfly Bicyclus anynana: Towards an Evolutionary Analysis , 2008, PloS one.

[9]  James Mallet,et al.  A Conserved Supergene Locus Controls Colour Pattern Diversity in Heliconius Butterflies , 2006, PLoS biology.

[10]  Durrell D. Kapan,et al.  Parallel Genetic Architecture of Parallel Adaptive Radiations in Mimetic Heliconius Butterflies , 2006, Genetics.

[11]  E. Coen,et al.  Evolutionary Paths Underlying Flower Color Variation in Antirrhinum , 2006, Science.

[12]  A. Papanicolaou,et al.  Heliconius wing patterns: an evo-devo model for understanding phenotypic diversity , 2006, Heredity.

[13]  Durrell D. Kapan,et al.  Localization of Müllerian Mimicry Genes on a Dense Linkage Map of Heliconius erato , 2006, Genetics.

[14]  Durrell D. Kapan,et al.  Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Y. Iwasa,et al.  The evolution of a Müllerian mimic in a spatially distributed community. , 2005, Journal of theoretical biology.

[16]  M. Joron Polymorphic mimicry, microhabitat use, and sex‐specific behaviour , 2005, Journal of evolutionary biology.

[17]  J. Mallet,et al.  Variable Selection and the Coexistence of Multiple mimetic forms of the Butterfly Heliconius numata , 1999, Evolutionary Ecology.

[18]  J. Mallet,et al.  Mimicry: developmental genes that contribute to speciation , 2003, Evolution & development.

[19]  P. Brakefield,et al.  The genetics and evo–devo of butterfly wing patterns , 2002, Nature Reviews Genetics.

[20]  James Mallet,et al.  Reproductive isolation caused by colour pattern mimicry , 2001, Nature.

[21]  P. Brakefield,et al.  The genetic basis of eyespot size in the butterfly Bicyclus anynana: an analysis of line crosses , 2000, Heredity.

[22]  Róbert,et al.  Plant domestication: a model for studying the selection of linkage , 1999 .

[23]  S. Carroll,et al.  Pattern formation and eyespot determination in butterfly wings. , 1994, Science.

[24]  F. Sperling SEX-LINKED GENES AND SPECIES DIFFERENCES IN LEPIDOPTERA , 1994, The Canadian Entomologist.

[25]  P. Brakefield,et al.  The inheritance of a wingless character in the 2spot ladybird (Adalia bipunctata) , 1993 .

[26]  A. Simcox,et al.  Allocation of the thoracic imaginal primordia in the Drosophila embryo. , 1993, Development.

[27]  J. Mallet The genetics of warning colour in Peruvian hybrid zones of Heliconius erato and H. melpomene , 1989, Proceedings of the Royal Society of London. B. Biological Sciences.

[28]  L. Gilbert,et al.  Correlations of ultrastructure and pigmentation suggest how genes control development of wing scales of Heliconius butterflies , 1988, The Journal of Research on the Lepidoptera.

[29]  K. S. Brown,et al.  Genetics and the Evolution of Muellerian Mimicry in Heliconius Butterflies , 1985 .

[30]  I. Mackay,et al.  Evolution of dominance , 1979, Nature.

[31]  Turner J.R.G. Butterfly mimicry: the genetical evolution of an adaptation. , 1977 .

[32]  B. Clarke,et al.  Supergenes in polymorphic land snails , 1976, Heredity.

[33]  B. Clarke,et al.  Supergenes in polymorphic land snails , 1976, Heredity.

[34]  B. Charlesworth,et al.  Theoretical genetics of Batesian mimicry II. Evolution of supergenes. , 1975, Journal of theoretical biology.

[35]  B. Charlesworth,et al.  Theoretical genetics of Batesian mimicry III. Evolution of dominance. , 1975, Journal of theoretical biology.

[36]  W. W. Benson,et al.  Adaptive Polymorphism Associated with Multiple Mullerian Mimicry in Heliconius numata (Lepid. Nymph.) , 1974 .

[37]  C. Clarke,et al.  Further Studies on the Genetics of the Mimetic Butterfly Papilio memnon L. , 1971 .

[38]  T. Dobzhansky Genetics of the Evolutionary Process , 1970 .

[39]  C. Clarke,et al.  The Genetics of the Mimetic Butterfly Papilio Memnon L. , 1968 .

[40]  A. Dickson On Evolution , 1884, Science.

[41]  C. Clarke,et al.  INTERACTIONS BETWEEN MAJOR GENES AND POLYGENES IN THE DETERMINATION OF THE MIMETIC PATTERNS OF PAPILIO DARDANUS , 1963 .

[42]  K. D. Sharma,et al.  MODIFIED INCOMPATIBILITY OF BUCKWHEAT FOLLOWING IRRADIATION , 1961 .

[43]  C. Clarke,et al.  Super-genes and mimicry , 1960, Heredity.

[44]  C. Clarke,et al.  The evolution of mimicry in the butterfly Papilio dardanus , 1960, Heredity.

[45]  M. Kimura A MODEL OF A GENETIC SYSTEM WHICH LEADS TO CLOSER LINKAGE BY NATURAL SELECTION , 1956 .

[46]  J. Huxley Morphism and evolution , 1955, Heredity.

[47]  K. Mather POLYMORPHISM AS AN OUTCOME OF DISRUPTIVE SELECTION , 1955 .

[48]  P. Sheppard,et al.  Natural Selection in Cepaea. , 1954, Genetics.

[49]  P. Sheppard Polymorphism, Linkage and the Blood Groups , 1953, The American Naturalist.

[50]  E. Ford The genetics of polymorphism in the Lepidoptera. , 1953, Advances in genetics.

[51]  G. Carpenter,et al.  Natural Selection , 1936, Nature.

[52]  R. Punnett,et al.  The Genetical Theory of Natural Selection , 1930, Nature.