Mimicry in butterflies: co-option and a bag of magnificent developmental genetic tricks
Riddhi Deshmukh
National Centre for Biological Sciences, Bengaluru, India
Search for more papers by this authorSaurav Baral
National Centre for Biological Sciences, Bengaluru, India
Search for more papers by this authorA. Gandhimathi
National Centre for Biological Sciences, Bengaluru, India
Search for more papers by this authorMuktai Kuwalekar
National Centre for Biological Sciences, Bengaluru, India
Search for more papers by this authorCorresponding Author
Krushnamegh Kunte
National Centre for Biological Sciences, Bengaluru, India
Correspondence to: [email protected]Search for more papers by this authorRiddhi Deshmukh
National Centre for Biological Sciences, Bengaluru, India
Search for more papers by this authorSaurav Baral
National Centre for Biological Sciences, Bengaluru, India
Search for more papers by this authorA. Gandhimathi
National Centre for Biological Sciences, Bengaluru, India
Search for more papers by this authorMuktai Kuwalekar
National Centre for Biological Sciences, Bengaluru, India
Search for more papers by this authorCorresponding Author
Krushnamegh Kunte
National Centre for Biological Sciences, Bengaluru, India
Correspondence to: [email protected]Search for more papers by this authorAbstract
Butterfly wing patterns are key adaptations that are controlled by remarkable developmental and genetic mechanisms that facilitate rapid evolutionary change. With swift advancements in the fields of genomics and genetic manipulations, identifying the regulators of wing development and mimetic wing patterns has become feasible even in nonmodel organisms such as butterflies. Recent mapping and gene expression studies have identified single switch loci of major effects such as transcription factors and supergenes as the main drivers of adaptive evolution of mimetic and polymorphic butterfly wing patterns. We highlight several of these examples, with emphasis on doublesex, optix, WntA and other dynamic, yet essential, master regulators that control critical color variation and sex-specific traits. Co-option emerges as a predominant theme, where typically embryonic and other early-stage developmental genes and networks have been rewired to regulate polymorphic and sex-limited mimetic wing patterns in iconic butterfly adaptations. Drawing comparisons from our knowledge of wing development in Drosophila, we illustrate the functional space of genes that have been recruited to regulate butterfly wing patterns. We also propose a developmental pathway that potentially results in dorsoventral mismatch in butterfly wing patterns. Such dorsoventrally mismatched color patterns modulate signal components of butterfly wings that are used in intra- and inter-specific communication. Recent advances—fuelled by RNAi-mediated knockdowns and CRISPR/Cas9-based genomic edits—in the developmental genetics of butterfly wing patterns, and the underlying biological diversity and complexity of wing coloration, are pushing butterflies as an emerging model system in ecological genetics and evolutionary developmental biology. WIREs Dev Biol 2018, 7:e291. doi: 10.1002/wdev.291
This article is categorized under:
- Gene Expression and Transcriptional Hierarchies > Regulatory Mechanisms
- Comparative Development and Evolution > Regulation of Organ Diversity
- Comparative Development and Evolution > Evolutionary Novelties
Graphical Abstract
REFERENCES
- 1Wickler W. Mimicry in Plants and Animals. London, United Kingdom: Weidenfeld & Nicholson Limited; 1968.
- 2Ruxton GD, Sherratt TN, Speed MP. Avoiding Attack: The Evolutionary Ecology of Crypsis, Warning Signals and Mimicry. Oxford, United Kingdom: Oxford University Press; 2004.
10.1093/acprof:oso/9780198528609.001.0001 Google Scholar
- 3Mallet J, Joron M. Evolution of diversity in warning color and mimicry: polymorphisms, shifting balance, and speciation. Annu Rev Ecol Syst 1999, 30: 201–233.
- 4Fisher RA. The Genetical Theory of Natural Selection. 2nd ed. New York: Dover Publications; 1958.
- 5Kunte K. The diversity and evolution of Batesian mimicry in Papilio swallowtail butterflies. Evolution (N Y) 2009, 63: 2707–2716. https://doi.org/10.1111/j.1558-5646.2009.00752.x.
- 6Kunte K. Female-limited mimetic polymorphism: a review of theories and a critique of sexual selection as balancing selection. Anim Behav 2009, 78: 1029–1036. https://doi.org/10.1016/j.anbehav.20 09.08.013.
- 7Ford EB. The genetics of polymorphism in the Lepidoptera. Adv Genet 1953, 5: 43–87.
- 8Sheppard PM. Natural Selection and Heredity. 4th ed. San Diego, CA: Hutchinson & Co.; 1975.
- 9Müller F. Ituna and Thyridia: a remarkable case of mimicry in butterflies. Trans Entomol Soc Lond 1879, 1879: 20–29.
- 10Turner JRG. In: MK Hecht, MC Steere, B Wallace, eds. Evolutionary Biology, vol. 10. New York: Plenum Press; 1977, 163–206.
10.1007/978-1-4615-6953-4_3 Google Scholar
- 11Bates HW. Contributions to an insect fauna of the Amazon Valley (Lepidoptera: Heliconidae). Trans Linn Soc Lond 1862, 23: 495–556.
10.1111/j.1096-3642.1860.tb00146.x Google Scholar
- 12Wallace AR. On the phenomena of variation and geographical distribution as illustrated by the Papilionidae of the Malayan region. Trans Linn Soc Lond 1865, 25: 1–71. https://doi.org/10.1111/j.1096-3642.1865.tb00178.x.
10.1111/j.1096-3642.1865.tb00178.x Google Scholar
- 13Joshi J, Prakash A, Kunte K. Evolutionary assembly of communities in butterfly mimicry rings. Am Nat 2017, 189: e58–e76. https://doi.org/10.1086/690907.
- 14Gallant JR, Imhoff VE, Martin A, Savage WK, Chamberlain NL, Pote BL, Peterson C, Smith GE, Evans B, Reed RD, et al. Ancient homology underlies adaptive mimetic diversity across butterflies. Nat Commun 2014, 5: 4817. https://doi.org/10.1038/ncomms5817.
- 15Kunte K, Zhang W, Tenger-Trolander A, Palmer DH, Martin A, Reed RD, Mullen SP, Kronforst MR. doublesex is a mimicry supergene. Nature 2014, 507: 229–232. https://doi.org/10.1038/nature13112.
- 16Nishikawa H, Iijima T, Kajitani R, Yamaguchi J, Ando T, Suzuki Y, Sugano S, Fujiyama A, Kosugi S, Hirakawa H, et al. A genetic mechanism for female-limited Batesian mimicry in Papilio butterfly. Nat Genet 2015, 47: 1–7. https://doi.org/10.1038/ng.3241.
- 17Koch PB, Behnecke B, Ffrench-Constant RH. The molecular basis of melanism and mimicry in a swallowtail butterfly. Curr Biol 2000, 10: 591–594.
- 18Koch BP, Keys DN, Rocheleau T, Aronstein K, Blackburn M, Carroll SB, Ffrench-Constant RH. Regulation of dopa decarboxylase expression during colour pattern formation in wild-type and melanic tiger swallowtail butterflies. Development 1998, 125: 2303–2313.
- 19Koch BP, Behnecke B, Weigmann-Lenz M, Ffrench-Constant RH. Insect pigmentation: activities of beta-alanyldopamine synthase in wing color patterns of wild-type and melanic mutant swallowtail butterfly Papilio glaucus. Pigment Cell Res 2000, 13(suppl 8): 54–58.
- 20Kronforst MR, Papa R. The functional basis of wing patterning in Heliconius butterflies: the molecules behind mimicry. Genetics 2015, 200: 1–19. https://doi.org/10.1534/genetics.114.172387.
- 21Marcus JM, Ramos DM, Monteiro A. Germline transformation of the butterfly Bicyclus anynana. Proc R Soc B 2004, 271: S263–S265. https://doi.org/10.1098/rsbl.2004.0175.
- 22Ramos DM, Kamal F, Wimmer EA, Cartwright AN, Monteiro A. Temporal and spatial control of transgene expression using laser induction of the hsp70 promoter. BMC Dev Biol 2006, 6: 55. https://doi.org/10.1186/1471-213X-6-55.
- 23Zhang L, Reed RD. Genome editing in butterflies reveals that spalt promotes and Distal-less represses eyespot colour patterns. Nat Commun 2016, 7: 11769. https://doi.org/10.1038/ncomms11769.
- 24Perry M, Kinoshita M, Saldi G, Huo L, Arikawa K, Desplan C. Molecular logic behind the three-way stochastic choices that expand butterfly colour vision. Nature 2016, 535: 280–284. https://doi.org/10.1038/nature18616.
- 25Zhang L, Martin A, Perry MW, van der Burg KRL, Matsuoka Y, Monteiro A, Reed RD. Genetic basis of melanin pigmentation in butterfly wings. Genetics 2017, 205: 1537–1550. https://doi.org/10.1534/genetics.116.196451.
- 26Martin A, McCulloch KJ, Patel NH, Briscoe AD, Gilbert LE, Reed RD. Multiple recent co-options of optix associated with novel traits in adaptive butterfly wing radiations. Evodevo 2014, 5: 7. https://doi.org/10.1186/2041-9139-5-7.
- 27Clarke CA, Sheppard PM. The genetics of the mimetic butterfly Hypolimnas bolina L. Philos Trans R Soc B 1975, 272: 229–265.
- 28Clarke CA, Sheppard PM. Super-genes and mimicry. Heredity (Edinb) 1960, 14: 175–185. https://doi.org/10.1038/hdy.1960.15.
10.1038/hdy.1960.15 Google Scholar
- 29Mather K. The genetical architecture of heterostyle in Primula sinensis. Evolution (N Y) 1950, 4: 340. https://doi.org/10.2307/2405601.
- 30Thompson MJ, Jiggins CD. Supergenes and their role in evolution. Heredity (Edinb) 2014, 113: 1–8. https://doi.org/10.1038/hdy.2014.20.
- 31Charlesworth D. The status of supergenes in the 21st century: recombination suppression in Batesian mimicry and sex chromosomes and other complex adaptations. Evol Appl 2016, 9: 74–90. https://doi.org/10.1111/eva.12291.
- 32Charlesworth D, Charlesworth B. Theoretical genetics of Batesian mimicry II. Evolution of supergenes. J Theor Biol 1975, 55: 305–324.
- 33Küpper C, Stocks M, Risse JE, Remedios ND, Farrell LL, McRae SB, Morgan TC, Karlionova N, Pinchuk P, Verkuil YI, et al. A supergene determines highly divergent male reproductive morphs in the ruff. Nat Genet 2016, 48: 79–83. https://doi.org/10.1038/ng.3443.
- 34Lamichhaney S, Fan G, Widemo F, Gunnarsson U, Thalmann DS, Hoeppner MP, Kerje S, Gustafson U, Shi C, Zhang H, et al. Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nat Genet 2016, 48: 84–88. https://doi.org/10.1038/ng.3430.
- 35Kurian V, Richards AJ. A new recombinant in the heteromorphy ‘S’ supergene in Primula. Heredity (Edinb) 1997, 78: 383–390.
- 36Clarke CA, Sheppard PM. The genetics of the mimetic butterfly Papilio polytes L. Philos Trans R Soc B 1972, 263: 431–458. https://doi.org/10.1098/rstb.1972.0006.
- 37Clarke CA, Sheppard PM. The genetics of some mimetic forms of Papilio dardanus and Papilio glaucus. J Genet 1959, 56: 236–260.
10.1007/BF02984747 Google Scholar
- 38Clarke CA, Sheppard PM, Thornton IWB. Further studies on the genetics of the mimetic butterfly Papilio memnon L. Philos Trans R Soc B 1971, 263: 35–70.
- 39Joron M, Papa R, Beltran M, Chamberlain NL, Mavarez J, Baxter S, Abanto M, Bermingham E, Humphray SJ, Rogers J, et al. A conserved supergene locus controls colour pattern diversity in Heliconius butterflies. PLoS Biol 2006, 4: e303.
- 40Joron M, Frezal L, Jones RT, Chamberlain NL, Lee SF, Haag CR, Whibley A, Becuwe M, Baxter SW, Ferguson L, et al. Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 2011, 477: 203–206. https://doi.org/10.1038/nature10341.
- 41Chouteau M, Ariasb M, Joron M. Warning signals are under positive frequency-dependent selection in nature. Proc Natl Acad Sci USA 2016, 113: 2164–2169. https://doi.org/10.1073/pnas.1519216113.
- 42Baker BS. Sex in flies: the splice of life. Nature 1989, 340: 521–524. https://doi.org/10.1038/340521a0.
- 43Jursnich VA, Burtis KC. A positive role in differentiation for the male doublesex protein of Drosophila. Dev Biol 1993, 155: 235–249. https://doi.org/10.1006/dbio.1993.1021.
- 44Taylor BJ, Villella A, Ryner LC, Baker BS, Hall JC. Behavioral and neurobiological implications of sex-determining factors in Drosophila. Dev Genet 1994, 15: 275–296. https://doi.org/10.1002/dvg.1020150309.
- 45Li J, Cocker JM, Wright J, Webster MA, McMullan M, Dyer S, Swarbreck D, Caccamo M, van Oosterhout C, Gilmartin PM. Genetic architecture and evolution of the S locus supergene in Primula vulgaris. Nat Plants 2016, 2: 16188. https://doi.org/10.1038/nplants.2016.188.
- 46Kitamura T, Imafuku M. Behavioral Batesian mimicry involving intraspecific polymorphism in the butterfly Papilio polytes. Zoolog Sci 2010, 27: 217–221. https://doi.org/10.2108/zsj.27.217.
- 47Kitamura T, Imafuku M. Behavioural mimicry in flight path of Batesian intraspecific polymorphic butterfly Papilio polytes. Proc R Soc B 2015, 282: 20150483. 10.1098/rspb.2015.0483.
- 48Klein A, Schultner E, Lowak H, Schrader L, Heinze J, Holman L, Oettler J. Evolution of social insect polyphenism facilitated by the sex differentiation cascade. PLoS Genet 2016, 12: e1005952. https://doi.org/10.1371/journal.pgen.1005952.
- 49Kronforst MR, Young LG, Kapan DD, McNeely C, O'Neill RJ, Gilbert LE. Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless. Proc Natl Acad Sci USA 2006, 103: 6575–6580. https://doi.org/10.1073/pnas.0509685103.
- 50Boggs CL, Watt WB, Ehrlich PR. Butterflies: Ecology and Evolution Taking Flight. Chicago, IL: University of Chicago Press; 2003.
10.7208/chicago/9780226063195.001.0001 Google Scholar
- 51Nijhout HF. The Development and Evolution of Butterfly Wing Patterns. Smithsonian Series in Comparative Evolutionary Biology. Washington DC: Smithsonian Institution Press; 1991.
- 52Turner JRG. In: RI Vane-Wright, PR Ackery, eds. The Biology of Butterflies. London: Academic Press; 1984, 141–161.
- 53Sheppard PM, Turner JRG, Brown KS, Benson WW, Singer MC. Genetics and the evolution of Mullerian mimicry in Heliconius butterflies. Philos Trans R Soc B 1985, 308: 433–610. https://doi.org/10.1098/rstb.1985.0066.
- 54Baxter SW, Johnston SE, Jiggins CD. Butterfly speciation and the distribution of gene effect sizes fixed during adaptation. Heredity (Edinb) 2009, 102: 57–65. https://doi.org/10.1038/hdy.2008.109.
- 55Jones RT, Salazar PA, Ffrench-Constant RH, Jiggins CD, Joron M. Evolution of a mimicry supergene from a multilocus architecture. Proc R Soc B 2012, 279: 316–325. https://doi.org/10.1098/rspb.2011.0882.
- 56Papa R, Kapan DD, Counterman BA, Maldonado K, Lindstrom DP, Reed RD, Nijhout HF, Hrbek T, McMillan WO. Multi-allelic major effect genes interact with minor effect QTLs to control adaptive color pattern variation in Heliconius erato. PLoS One 2013, 8: e57033. https://doi.org/10.1371/journal.pone.0057033.
- 57Reed RD, Papa R, Martin A, Hines HM, Counterman BA, Pardo-Diaz C, Jiggins CD, Chamberlain NL, Kronforst MR, Chen R, et al. optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 2011, 333: 1137–1141.
- 58Martin A, Papa R, Nadeau NJ, Hill RI, Counterman BA, Halder G, Jiggins CD, Kronforst MR, Long AD, McMillan WO, et al. Diversification of complex butterfly wing patterns by repeated regulatory evolution of a Wnt ligand. Proc Natl Acad Sci USA 2012, 109: 12632–12637. https://doi.org/10.1073/pnas.1204800109.
- 59Nadeau NJ, Pardo-Diaz C, Whibley A, Supple MA, Saenko SV, Wallbank RWR, Wu GC, Maroja L, Ferguson L, Hanly JJ, et al. The gene cortex controls mimicry and crypsis in butterflies and moths. Nature 2016, 534: 106–110. https://doi.org/10.1038/nature17961.
- 60Baxter SW, Nadeau NJ, Maroja LS, Wilkinson P, Counterman BA, Dawson A, Beltran M, Perez-Espona S, Chamberlain NL, Ferguson L, et al. Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade. PLoS Genet 2010, 6: e1000794. https://doi.org/10.1371/journal.pgen.1000794.
- 61Counterman BA, Araujo-Perez F, Hines HM, Baxter SW, Morrison CM, Lindstrom DP, Papa R, Ferguson L, Joron M, Ffrench-Constant RH, et al. Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in Heliconius erato. PLoS Genet 2010, 6: e1000796. https://doi.org/10.1371/journal.pgen.1000796.
- 62Pardo-Diaz C, Jiggins CD. Neighboring genes shaping a single adaptive mimetic trait. Evol Dev 2014, 16: 3–12. https://doi.org/10.1111/ede.12058.
- 63Ferguson LC, Lee SF, Chamberlain NL, Nadeau N, Joron M, Baxter SW, Wilkinson P, Papanicolaou A, Kumar S, Kee T-J, et al. Characterization of a hotspot for mimicry: assembly of a butterfly wing transcriptome to genomic sequence at the HmYb/Sb locus. Mol Ecol 2010, 19: 240–254. https://doi.org/10.1111/j.1365-294X.2009.04475.x.
- 64Nadeau NJ, Ruiz M, Salazar P, Counterman B, Medina JA, Ortiz-Zuazaga H, Morrison A, McMillan OW, Jiggins CD, Papa R. Population genomics of parallel hybrid zones in the mimetic butterflies, H. melpomene and H. erato. Genome Res 2014, 24: 1316–1333. https://doi.org/10.1101/gr.169292.113.
- 65Pesin JA, Orr-Weaver TL. Developmental role and regulation of cortex, a meiosis-specific anaphase-promoting complex/cyclosome activator. PLoS Genet 2007, 3: e202. https://doi.org/10.1371/journal.pgen.0030202.
- 66Chu T, Henrion G, Haegeli V, Strickland S. Cortex, a Drosophila gene required to complete oocyte meiosis, is a member of the Cdc20/fizzy protein family. Genesis 2001, 29: 141–152.
- 67van't Hof AE, Campagne P, Rigden DJ, Yung CJ, Lingley J, Quail MA, Hall N, Darby AC, Saccheri IJ. The industrial melanism mutation in British peppered moths is a transposable element. Nature 2016, 534: 102–105. https://doi.org/10.1038/nature17951.
- 68Macdonald WP, Martin A, Reed RD. Butterfly wings shaped by a molecular cookie cutter: evolutionary radiation of lepidopteran wing shapes associated with a derived cut/wingless wing margin boundary system. Evol Dev 2010, 12: 296–304. https://doi.org/10.1111/j.1525-142X.2010.00415.x.
- 69de Celis JF, Garcia-Bellido A, Bray SJ. Activation and function of Notch at the dorsal–ventral boundary of the wing imaginal disc. Development 1996, 122: 359–369.
- 70Neumann CJ, Cohen SM. A hierarchy of cross-regulation involving Notch, wingless, vestigial and cut organizes the dorsal/ventral axis of the Drosophila wing. Development 1996, 122: 3477–3485.
- 71Micchelli CA, Rulifson EJ, Blair SS. The function and regulation of cut expression on the wing margin of Drosophila: notch, wingless and a dominant negative role for Delta and Serrate. Development 1997, 124: 1485–1495.
- 72Jia D, Bryant J, Jevitt A, Calvin G, Deng W-M. The ecdysone and notch pathways synergistically regulate cut at the dorsal–ventral boundary in Drosophila wing discs. J Genet Genomics 2016, 43: 179–186. https://doi.org/10.1016/j.jgg.2016.03.002.
- 73Williams JA, Paddock SW, Carroll SB. Pattern formation in a secondary field: a hierarchy of regulatory genes subdivides the developing Drosophila wing disc into discrete subregions. Development 1993, 117: 571–584.
- 74Ng M, Diaz-Benjumea FJ, Vincent JP, Wu J, Cohen SM. Specification of the wing by localized expression of wingless protein. Nature 1996, 381: 316–318. https://doi.org/10.1038/381316a0.
- 75Goulev Y, Fauny JD, Gonzalez-Marti B, Flagiello D, Silber J, Zider A. SCALLOPED interacts with YORKIE, the nuclear effector of the hippo tumor-suppressor pathway in Drosophila. Curr Biol 2008, 18: 435–441. https://doi.org/10.1016/j.cub.2008.02.034.
- 76Galant R, Skeath JB, Paddock S, Lewis DL, Carroll SB. Expression pattern of a butterfly achaete-scute homolog reveals the homology of butterfly wing scales and insect sensory bristles. Curr Biol 1998, 8: 807–813.
- 77Furman DP, Bukharina TA. How Drosophila melanogaster forms its mechanoreceptors. Curr Genomics 2008, 9: 312–323. https://doi.org/10.2174/138920208785133271.
- 78Culí J, Martín-Blanco E, Modolell J. The EGF receptor and N signalling pathways act antagonistically in Drosophila mesothorax bristle patterning. Development 2001, 128: 299–308.
- 79Weatherbee SD, Nijhout FH, Grunert LW, Halder G, Galant R, Selegue J, Carroll SB. Ultrabithorax function in butterfly wings and the evolution of insect wing patterns. Curr Biol 1999, 9: 109–115.
- 80Warren R, Nagy L, Selegue J, Gates J, Carroll SB. Evolution of homeotic gene regulation and function in flies and butterflies. Nature 1994, 372: 458–461.
- 81Carroll SB, Weatherbee SD, Langeland JA. Homeotic genes and the regulation and evolution of insect wing number. Nature 1995, 375: 58–61. https://doi.org/10.1038/375058a0.
- 82Casares F, Calleja M, Sánchez-Herrero E. Functional similarity in appendage specification by the Ultrabithorax and abdominal-A Drosophila HOX genes. EMBO J 1996, 15: 3934–3942.
- 83Struhl G. Genes controlling segmental specification in the Drosophila thorax. Proc Natl Acad Sci USA 1982, 79: 7380–7384.
- 84Weatherbee SD, Halder G, Kim J, Hudson A, Carroll S. Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. Genes Dev 1998, 12: 1474–1482.
- 85Koch PB. Colour pattern specific melanin synthesis is controlled by ecdysteroids via dopa decarboxylase in wings of Precis coenia (Lepidoptera: Nymphalidae). Eur J Entomol 1995, 92: 161–167.
- 86Wright TRF, Bewley GC, Sherald AF. The genetics of dopa decarboxylase in Drosophila melanogaster. II. Isolation and characterization of dopa-decarboxylase-deficient mutants and their relationship to the α-methyl-dopa-hypersensitive mutants. Genetics 1976, 84: 287–310.
- 87Wright TRF, Hodgetts RB, Sherald AF. The genetics of dopa decarboxylase in Drosophila melanogaster I. Isolation and characterization of deficiencies that delete the dopa-decarboxylase-dosage-sensitive region and the α-methyl-dopa-hypersensitive locus. Genetics 1976, 84: 267–285.
- 88De Luca M, Roshina NV, Geiger-Thornsberry GL, Lyman RF, Pasyukova EG, Mackay TFC. Dopa decarboxylase (Ddc) affects variation in Drosophila longevity. Nat Genet 2003, 34: 429–433. https://doi.org/10.1038/ng1218.
- 89Sideri M, Tsakas S, Markoutsa E, Lampropoulou M, Marmaras VJ. Innate immunity in insects: surface-associated dopa decarboxylase-dependent pathways regulate phagocytosis, nodulation and melanization in medfly haemocytes. Immunology 2008, 123: 528–537. https://doi.org/10.1111/j.1365-2567.2007.02722.x.
- 90Brakefield PM, Gates J, Keys D, Kesbeke F, Wijngaarden PJ, Montelro A, French V, Carroll SB. Development, plasticity and evolution of butterfly eyespot patterns. Nature 1996, 384: 236–242. https://doi.org/10.1038/384236a0.
- 91Reed RD, Serfas MS. Butterfly wing pattern evolution is associated with changes in a Notch/Distal-less temporal pattern formation process. Curr Biol 2004, 14: 1159–1166. https://doi.org/10.1016/j.cub.2004.06.046.
- 92Reed RD, Gilbert LE. Wing venation and distal-less expression in Heliconius butterfly wing pattern development. Dev Genes Evol 2004, 214: 628–634. https://doi.org/10.1007/s00427-004-0439-8.
- 93Monteiro A, Chen B, Ramos DM, Oliver JC, Tong X, Guo M, Wang W-K, Fazzino L, Kamal F. Distal-less regulates eyespot patterns and melanization in Bicyclus butterflies. J Exp Zool 2013, 320: 321–331. https://doi.org/10.1002/jez.b.22503.
- 94Gorfinkiel N, Morata G, Guerrero I. The homeobox gene Distal-less induces ventral appendage development in Drosophila. Genes Dev 1997, 11: 2259–2271.
- 95Martin A, Reed RD. wingless and aristaless2 define a developmental ground plan for moth and butterfly wing pattern evolution. Mol Biol Evol 2010, 27: 2864–2878. https://doi.org/10.1093/molbev/msq173.
- 96Campbell G, Weaver T, Tomlinson A. Axis specification in the developing Drosophila appendage: the role of wingless, decapentaplegic, and the homeobox gene aristaless. Cell 1993, 74: 1113–1123.
- 97Oliver JC, Tong X-L, Gall LF, Piel WH, Monteiro A. A single origin for Nymphalid butterfly eyespots followed by widespread loss of associated gene expression. PLoS Genet 2012, 8: e1002893. https://doi.org/10.1371/journal.pgen.1002893.
- 98Lecuit T, Cohen SM. Dpp receptor levels contribute to shaping the Dpp morphogen gradient in the Drosophila wing imaginal disc. Development 1998, 125: 4901–4907.
- 99de Celis JF, Barrio R. Function of the spalt/spalt-related gene complex in positioning the veins in the Drosophila wing. Mech Dev 2000, 91: 31–41.
- 100Abbott MK, Kaufman TC. The relationship between the functional complexity and the molecular organization of the Antennapedia locus of Drosophila melanogaster. Genetics 1986, 114: 919–942.
- 101Plaza S. Molecular basis for the inhibition of Drosophila eye development by Antennapedia. EMBO J 2001, 20: 802–811. https://doi.org/10.1093/emboj/20.4.802.
- 102Reed RD. Evidence for notch-mediated lateral inhibition in organizing butterfly wing scales. Dev Genes Evol 2004, 214: 43–46. https://doi.org/10.1007/s00427-003-0366-0.
- 103Diaz-Benjumea FJ, Cohen SM. Serrate signals through Notch to establish a Wingless-dependent organizer at the dorsal/ventral compartment boundary of the Drosophila wing. Development 1995, 121: 4215–4225.
- 104Keys DN, Lewis DL, Selegue JE, Pearson BJ, Goodrich LV, Johnson RL, Gates J, Scott MP, Carroll SB. Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 1999, 283: 532–534.
- 105Rudolf K, Umetsu D, Aliee M, Sui L, Jülicher F, Dahmann C. A local difference in Hedgehog signal transduction increases mechanical cell bond tension and biases cell intercalations along the Drosophila anteroposterior compartment boundary. Development 2015, 142: 3845–3858. https://doi.org/10.1242/dev.125542.
- 106Chen Y, Struhl G. Dual roles for patched in sequestering and transducing Hedgehog. Cell 1996, 87: 553–563.
- 107Dahmann C, Basler K. Opposing transcriptional outputs of hedgehog signaling and engrailed control compartmental cell sorting at the Drosophila A/P boundary. Cell 2000, 100: 411–422.
- 108Phillips AM, Smart R, Strauss R, Brembs B, Kelly LE. The Drosophila black enigma: the molecular and behavioural characterization of the black1 mutant allele. Gene 2005, 351: 131–142. https://doi.org/10.1016/j.gene.2005.03.013.
- 109Wittkopp PJ, Carroll SB, Kopp A. Evolution in black and white: genetic control of pigment patterns in Drosophila. Trends Genet 2003, 19: 495–504. https://doi.org/10.1016/S0168-9525(03)00194-X.
- 110Seimiya M, Gehring WJ. The Drosophila homeobox gene optix is capable of inducing ectopic eyes by an eyeless-independent mechanism. Development 2000, 127: 1879–1886.
- 111Croce JC, McClay DR. Evolution of the Wnt pathways. Methods Mol Biol 2008, 469: 3–18.
- 112Janssen R, Le Gouar M, Pechmann M, Poulin F, Bolognesi R, Schwager EE, Hopfen C, Colbourne JK, Budd GE, Brown SJ, et al. Conservation, loss, and redeployment of Wnt ligands in protostomes: implications for understanding the evolution of segment formation. BMC Evol Biol 2010, 10: 374. https://doi.org/10.1186/1471-2148-10-374.
- 113Gieseler K, Wilder E, Mariol M-C, Buratovitch M, Bérenger H, Graba Y, Pradel J. DWnt4 and wingless elicit similar cellular responses during imaginal development. Dev Biol 2001, 232: 339–350. https://doi.org/10.1006/dbio.2001.0184.
- 114Reed RD, McMillan WO, Nagy LM. Gene expression underlying adaptive variation in Heliconius wing patterns: non-modular regulation of overlapping cinnabar and vermilion prepatterns. Proc R Soc B 2007, 275: 37–45. https://doi.org/10.1098/rspb.2007.1115.
- 115Reed RD, Nagy LM. Evolutionary redeployment of a biosynthetic module: expression of eye pigment genes vermilion, cinnabar, and white in butterfly wing development. Evol Dev 2005, 7: 301–311. https://doi.org/10.1111/j.1525-142X.2005.05036.x.
- 116Ferguson LC, Jiggins CD. Shared and divergent expression domains on mimetic Heliconius wings. Evol Dev 2009, 11: 498–512. https://doi.org/10.1111/j.1525-142X.2009.00358.x.
- 117Warren WD, Palmer S, Howells AJ. Molecular characterization of the cinnabar region of Drosophila melanogaster: identification of the cinnabar transcription unit. Genetica 1996, 98: 249–262.
- 118Searles LL, Voelker RA. Molecular characterization of the Drosophila vermilion locus and its suppressible alleles. Proc Natl Acad Sci USA 1986, 83: 404–408.
- 119Mackenzie SM, Brooker MR, Gill TR, Cox GB, Howells AJ, Ewart GD. Mutations in the white gene of Drosophila melanogaster affecting ABC transporters that determine eye colouration. Biochim Biophys Acta 1999, 1419: 173–185.
- 120Gordon IJ, Smith DAS. Genetics of the mimetic African butterfly Hypolimnas misippus: hindwing polymorphism. Heredity (Edinb) 1989, 63: 409–425.
- 121Gordon IJ, Smith DAS. Body size and colour-pattern genetics in the polymorphic mimetic butterfly Hypolimnas misippus (L.). Heredity (Edinb) 1998, 80: 62–69. https://doi.org/10.1046/j.1365-2540.1998.00259.x.
- 122Gordon IJ. Polymorphism of the tropical butterfly Danaus chrysippus L. in Africa. Heredity (Edinb) 1984, 53: 583–593.
- 123Clark R, Brown SM, Collins SC, Jiggins CD, Heckel DG, Vogler AP. 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 2008, 275: 1181–1188. https://doi.org/10.1098/rspb.2007.1762.
- 124Timmermans MJ, Baxter SW, Clark R, Heckel DG, Vogel H, Collins S, Papanicolaou A, Fukova I, Joron M, Thompson MJ, et al. Comparative genomics of the mimicry switch in Papilio dardanus. Proc R Soc B 2014, 281 pii:20140465. https://doi.org/10.1098/rspb.2014.0465.
- 125Simmonds AJ, Brook WJ, Cohen SM, Bell JB. Distinguishable functions for engrailed and invected in anterior–posterior patterning in the Drosophila wing. Nature 1995, 376: 424–427. https://doi.org/10.1038/376424a0.
- 126Zecca M, Basler K, Struhl G. Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development 1995, 121: 2265–2278.
- 127Clarke CA, Clarke FMM, Collins SC, Gill ACL, Turner JRG. Male-like females, mimicry and transvestism in butterflies (Lepidoptera: Papilionidae). Syst Entomol 1985, 10: 257–283. https://doi.org/10.1111/j.1365-3113.1985.tb00137.x.
- 128Clarke CA, Sheppard PM. The genetics of four new forms of the mimetic butterfly Papilio memnon L. Proc R Soc B 1973, 184: 1–14. https://doi.org/10.1098/rspb.1973.0027.
- 129Komata S, Lin C-P, Iijima T, Fujiwara H, Sota T. Identification of doublesex alleles associated with the female-limited Batesian mimicry polymorphism in Papilio memnon. Sci Rep 2016, 6: 34782. https://doi.org/10.1038/srep34782.
- 130Scriber JM, Hagen RH, Lederhouse RC. Genetics of mimicry in the tiger swallowtail butterflies, Papilio glaucus and P. canadensis (Lepidoptera: Papilionidae). Evolution (N Y) 1996, 50: 222–236.
- 131Andolfatto P, Scriber JM, Charlesworth B. No association between mitochondrial DNA haplotypes and a female-limited mimicry phenotype in Papilio glaucus. Evolution (N Y) 2003, 57: 305–316.
- 132Ffrench-Constant RH. Butterfly wing colours are driven by the evolution of developmental heterochrony. Butterfly wing colours and patterning by numbers. Heredity (Edinb) 2012, 108: 592–593. https://doi.org/10.1038/hdy.2012.6.
- 133True JR, Carroll SB. Gene co-option in physiological and morphological evolution. Annu Rev Cell Dev Biol 2002, 18: 53–80. https://doi.org/10.1146/annurev.cellbio.18.020402.140619.
- 134Wallbank RWR, Baxter SW, Pardo-Diaz C, Hanly JJ, Martin SH, Mallet J, Dasmahapatra KK, Salazar C, Joron M, Nadeau N, et al. Evolutionary novelty in a butterfly wing pattern through enhancer shuffling. PLoS Biol 2016, 14: e1002353. https://doi.org/10.1371/journal.pbio.1002353.
- 135Cvekl A, Piatigorsky J. Lens development and crystallin gene expression: many roles for Pax-6. Bioessays 1996, 18: 621–630. https://doi.org/10.1002/bies.950180805.
- 136Arnoult L, Su KFY, Manoel D, Minervino C, Magriña J, Gompel N, Prud'homme B. Emergence and diversification of fly pigmentation through evolution of a gene regulatory module. Science 2013, 339: 1423–1426. https://doi.org/10.1126/science.1233749.
- 137Carroll SB, Gates J, Keys D, Paddock SW, Panganiban GF, Selegue J, Williams JA. Pattern formation and eyespot determination in butterfly wings. Science 1994, 265: 109–114. https://doi.org/10.1126/science.7912449.
- 138Brunetti CR, Selegue JE, Monteiro A, French V, Brakefield PM, Carroll SB. The generation and diversification of butterfly eyespot color patterns. Curr Biol 2001, 11: 1578–1585. https://doi.org/10.1016/S0960-9822(01)00502-4.
- 139Chen L, DeVries AL, Cheng CH. Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. Proc Natl Acad Sci USA 1997, 94: 3811–3816.
- 140McCulloch KJ, Osorio D, Briscoe AD. Sexual dimorphism in the compound eye of Heliconius erato: a nymphalid butterfly with at least five spectral classes of photoreceptor. J Exp Biol 2016, 219: 2377–2387. https://doi.org/10.1242/jeb.136523.
- 141Oliver JC, Robertson KA, Monteiro A. Accommodating natural and sexual selection in butterfly wing pattern evolution. Proc R Soc B 2009, 276: 2369–2375. https://doi.org/10.1098/rspb.2009.0182.
- 142Su S, Lim M, Kunte K. Prey from the eyes of predators: color discriminability of aposematic and mimetic butterflies from an avian visual perspective. Evolution (N Y) 2015, 69: 2985–2994. https://doi.org/10.1111/evo.12800.
- 143Ohsaki N. Preferential predation of female butterflies and the evolution of Batesian mimicry. Nature 1995, 378: 173–175.
- 144Cohen B, McGuffin ME, Pfeifle C, Segal D, Cohen SM. Apterous, a gene required for imaginal disc development in Drosophila encodes a member of the LIM family of developmental regulatory proteins. Genes Dev 1992, 6: 715–729.
- 145Diaz-Benjumea FJ, Cohen SM. Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Cell 1993, 75: 741–752.
- 146Blair SS, Brower DL, Thomas JB, Zavortink M. The role of apterous in the control of dorsoventral compartmentalization and PS integrin gene expression in the developing wing of Drosophila. Development 1994, 120: 1805–1815.
- 147Kim J, Irvine KD, Carroll SB. Cell recognition, signal induction, and symmetrical gene activation at the dorsal–ventral boundary of the developing Drosophila wing. Cell 1995, 82: 795–802.
- 148Brabant MC, Fristrom D, Bunch TA, Brower DL. Distinct spatial and temporal functions for PS integrins during Drosophila wing morphogenesis. Development 1996, 122: 3307–3317.
- 149Danen EHJ, Sonnenberg A. Integrins in regulation of tissue development and function. J Pathol 2003, 200: 471–480. https://doi.org/10.1002/path.1416.
- 150Araujo H. Integrins modulate Sog activity in the Drosophila wing. Development 2003, 130: 3851–3864. https://doi.org/10.1242/dev.00613.