A conserved supergene locus controls colour pattern diversity in Heliconius butterflies

PLoS Biology

Volumn 4, Issue 10, 2006, Pages 1831-1840

  Joron, Mathieu ^a,b,c   Papa, Riccardo ^d   Beltrán, Margarita ^a   Chamberlain, Nicola ^e   Mavárez, Jesús ^c,f   Baxter, Simon ^a   Abanto, Moisés ^g   Bermingham, Eldredge ^f   Humphray, Sean J ^h   Rogers, Jane ^h   Beasley, Helen ^h   Barlow, Karen ^h   Ffrench Constant, Richard H ^e   Mallet, James ^c   McMillan, W Owen ^d   Jiggins, Chris D ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b LEIDEN UNIVERSITY   (Netherlands)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^e University of Bath ^*  (United Kingdom)

^f SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^g Jirón Alegría Arias de Morey ^*  (Peru)

^h WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BUTTERFLY; CONTROLLED STUDY; DNA POLYMORPHISM; GENE CONTROL; GENE LOCUS; GENETIC LINKAGE; GENETIC VARIABILITY; NONHUMAN; SPECIES DIVERSITY; ANIMAL; BACTERIAL ARTIFICIAL CHROMOSOME; BIODIVERSITY; BIOLOGICAL MODEL; BIOLOGY; CROSS BREEDING; FEMALE; MALE; MOLECULAR GENETICS; MORPHOGENESIS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYSIOLOGY;

HELICONIUS; HELICONIUS ERATO; HELICONIUS MELPOMENE; HELICONIUS NUMATA; HEXAPODA; MELINAEA; PAPILIONOIDEA;

MICROSATELLITE DNA;

ANIMALS; BIODIVERSITY; BIOLOGY; BODY PATTERNING; BUTTERFLIES; CHROMOSOMES, ARTIFICIAL, BACTERIAL; CONSERVED SEQUENCE; CROSSES, GENETIC; FEMALE; MALE; MICROSATELLITE REPEATS; MODELS, BIOLOGICAL; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PHENOTYPE;

EID: 33748901660     PISSN: 15457885     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0040303     Document Type: Article

References (54)

1. Carroll SB, Grenier JK, Weatherbee SD (2001) From DNA to diversity: Molecular genetics and the evolution of animal design. Malden (Massachusetts): Blackwell Science. 214 p.
2. Gompel N, Prud'homme B, Wittkopp PJ, Kassner VA, Carroll SB (2005) Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433: 481-487.
3. Müller F (1879) . Müller F (1879) Ituna and Thyridia: A remarkable case of mimicry in butterflies. Trans Entomol Soc Lond 1879: xx-xxix.
4. Fisher RA (1958) The genetical theory of natural selection, 2nd revised edition. New York: Dover. 291 p.
5. Goldschmidt RB (1945) Mimetic polymorphism, a controversial chapter of Darwinism. Q Rev Biol 20: 147-164; 205-230.
6. Sucena E, Delon I, Jones I, Payre F, Stern DL (2003) Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism. Nature 424: 935-938.
7. Cresko WA, Amores A, Wilson C, Murphy J, Currey M, et al. (2004) Parallel genetic basis for repeated evolution of armor loss in Alaskan three-spine stickleback populations. Proc Natl Acad Sci U S A 101: 6050-6055.
8. Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G, Dickson M, et al. (2005) Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307: 1928-1933.
9. Losos JB, Jackman TR, Larson A, de Queiroz K, Rodríguez-Schettino L (1998) Contingency and determinism in replicated adaptive radiations of island lizards. Science 279: 2115-2118.
10. Sturmbauer C, Hainz U, Baric S, Verheyen E, Salzburger W (2003) Evolution of the tribe Tropheini from Lake Tanganyika: Synchronized explosive speciation producing multiple evolutionary parallelism. Hydrobiologia 500: 51-64.
11. Schluter D (2000) The ecology of adaptive radiation. Oxford: Oxford University Press. 296 p.
12. Wake DB (1991) Homoplasy - The result of natural selection, or evidence of design limitations. Am Nat 138: 543-567.
13. Price T, Pavelka M (1996) Evolution of a colour pattern: History, development, and selection. J Evol Biol 9: 451-470.
14. Mundy NI (2005) A window on the genetics of evolution: MC1R and plumage colouration in birds. Proc R Soc Lond B Biol Sci 272: 1633-1640.
15. Sheppard PM, Turner JRG, Brown KS, Benson WW, Singer MC (1985) Genetics and the evolution of Muellerian mimicry in Heliconius butterflies. Philos Trans R Soc Lond B Biol Sci 308: 433-610.
16. Nijhout HF (1991) The development and evolution of butterfly wing patterns. Washington (D. C.): Smithsonian Institution Press. 297 p.
17. Mallet J (1989) The genetics of warning colour in Peruvian hybrid zones of Heliconius erato and H. melpomene. Proc R Soc Lond B Biol Sci 236: 163-185.
18. Flanagan NS, Tobler A, Davison A, Pybus OG, Kapan DD, et al. (2004) Historical demography of Mullerian mimicry in the neotropical Heliconius butterflies. Proc Natl Acad Sci U S A 101: 9704-9709.
19. Brown KS, Benson WW (1974) Adaptive polymorphism associated with multiple Müllerian mimicry in Heliconius numata. Biotropica 6: 205-228.
20. Joron M, Wynne IR, Lamas G, Mallet J (1999) Variable selection and the coexistence of multiple mimetic forms of the butterfly Heliconius numata. Evol Ecol 13: 721-754.
21. Naisbit RE, Jiggins CD, Mallet J (2003) Mimicry: Developmental genes that contribute to speciation. Evol Dev 5: 269-280.
22. Jiggins CD, Mavárez J, Beltrán M, McMillan WO, Johnston JS, et al. (2005) A genetic linkage map of the mimetic butterfly, Heliconius melpomene. Genetics 171: 557-570.
23. Kronforst MR, Young LG, Kapan DD, McNeely C, O'Neill RJ, et al. (2006) Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless. Proc Natl Acad Sci U S A 103: 6575-6580.
24. Jiggins CD, McMillan WO (1997) The genetic basis of an adaptive radiation: Warning colour in two Heliconius species. Proc R Soc Lond B Biol Sci 264:1167-1175.
25. Mather K (1950) The genetical architecture of heterostyly in Primula sinensis. Evolution 4: 340-352.
26. Turner JRG (1968) Natural selection for and against a polymorphism which interacts with sex. Evolution 22: 481-495.
27. Kapan DD, Flanagan NS, Tobler A, Papa R, Reed RD, et al. (2006) Localization of Müllerian mimicry genes on a dense linkage map of Heliconius erato. Genetics 173: 735-757.
28. Tobler A, Kapan DD, Flanagan N, González C, Peterson E, et al. (2005) First-generation linkage map of the warningly colored butterfly Heliconius erato. Heredity 94: 408-417.
29. Carroll SB, Gates J, Keys DN, Paddock SW, Panganiban GEF, et al. (1994) Pattern formation and eyespot determination in butterfly wings. Science 265: 109-114.
30. Brakefield PM, Gates J, Keys DN, Kesbeke F, Wijngaarden PJ, et al. (1996) Development, plasticity and evolution of butterfly eyespot patterns. Nature 384: 236-242.
31. Beldade P, Brakefield PM, Long AD (2002) Contribution of Distal-less to quantitative variation in butterfly eyespots. Nature 415: 315-318.
32. Schluter D, Clifford EA, Nemethy M, McKinnon JS (2004) Parallel evolution and inheritance of quantitative traits. Am Nat 163: 809-822.
33. Shubin N, Wake DB, Crawford AJ (1995) Morphological variation in the limbs of Taricha granulosa (Caudata, Salamandridae) - Evolutionary and phylogenetic implications. Evolution 49: 874-884.
34. Richardson MK, Brakefield PM (2003) Hotspots for evolution. Nature 424: 894-895.
35. Carroll SB, Gompel N, Prud'homme B, Wittkopp T, Kassner V (2005) Chance caught on the wing: cis-regulatory evolution and the origins of novelty. Dev Biol 283: 584-584.
36. Ranson H, Claudianos C, Ortelli F, Abgrall C, Hemingway J, et al. (2002) Evolution of supergene families associated with insecticide resistance. Science 298: 179-181.
37. Petkov PM, Graber JH, Churchill GA, DiPetrillo K, King BL, et al. (2005) Evidence of a large-scale functional organization of mammalian chromosomes. PLoS Genet 1: e33. DOI: 10.1371/journal.pgen.0010033
38. Gilbert LE (2003) Adaptive novelty through introgression in Heliconius wing patterns: Evidence for a shared genetic "tool box" from synthetic hybrid zones and a theory of diversification. In: Boggs CL, Watt WB, Ehrlich PR, editors. Ecology and evolution taking flight: Butterflies as model systems. Chicago: University of Chicago Press. pp. 281-318.
39. Keys DN, Lewis DL, Selegue JE, Pearson BJ, Goodrich LV, et al. (1999) Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 283: 532-534.
40. Beldade P, Brakefield PM (2002) The genetics and evo-devo of butterfly wing patterns. Nat Rev Genet 3: 442-452.
41. Charlesworth D, Charlesworth B (1975) Theoretical genetics of Batesian mimicry II. Evolution of supergenes. J Theor Biol 55: 305-324.
42. Clarke CA, Sheppard PM (1963) Interactions between major genes and polygenes in the determination of the mimetic patterns of Papilio dardanus. Evolution 17: 404-413.
43. Turner JRG (1984) Mimicry: The palatability spectrum and its consequences. In: Vane-Wright RI, Ackery PR, editors. The biology of butterflies. London: Academic Press. pp. 141-161.
44. Nijhout HF (2003) Polymorphic mimicry in Papilio dardanus: Mosaic dominance, big effects, and origins. Evol Dev 5: 579-592.
45. Sheppard PM (1959) The evolution of mimicry: A problem in ecology and genetics. Cold Spring Harb Symp Quant Biol 24: 131-140.
46. Turner JRG (1977) Butterfly mimicry: The genetical evolution of an adaptation. Evol Biol 10: 163-206.
47. Le Thierry d'Ennequin M, Toupance B, Robert T, Godelle B, Gouyon PH (1999) Plant domestication: A model for studying the evolution of linkage. J Evol Biol 12: 1138-1147.
48. Joron M, Jiggins CD, Papanicolaou A, McMillan WO (2006) Heliconius wing patterns: An evo-devo model for understanding phenotypic diversity. Heredity. E-pub ahead of print.
49. Kronforst MR (2005) Primers for the amplification of nuclear introns in Heliconius butterflies. Mol Ecol Notes 5: 158-162.
50. Mavárez J, González M (2006) A set of microsatellite markers for Heliconius melpomene and closely related species. Mol Ecol Notes 6: 20-23.
51. Papanicolaou A, Joron M, McMillan WO, Blaxter ML, Jiggins CD (2005) Genomic tools and cDNA derived markers for butterflies. Mol Ecol 14: 2883-2897.
52. Suomalainen E, Cook LM, Turner JRG (1973) Achiasmatic oogenesis in the heliconiine butterflies. Hereditas 74: 302-304.
53. Lander E, Abrahamson J, Barlow A, Daly M, Lincoln S, et al. (1987) Mapmaker: A computer package for constructing genetic-linkage maps. Cytogenet Cell Genet 46: 642-642.
54. Stam P (1993) Construction of integrated genetic-linkage maps by means of a new computer package - JoinMap. Plant J 3: 739-744.