1932

Abstract

This article reviews the latest developments in our understanding of the origin, development, and evolution of nymphalid butterfly eyespots. Recent contributions to this field include insights into the evolutionary and developmental origin of eyespots and their ancestral deployment on the wing, the evolution of eyespot number and eyespot sexual dimorphism, and the identification of genes affecting eyespot development and black pigmentation. I also compare features of old and more recently proposed models of eyespot development and propose a schematic for the genetic regulatory architecture of eyespots. Using this schematic I propose two hypotheses for why we observe limits to morphological diversity across these serially homologous traits.

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2015-01-07
2024-03-28
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Literature Cited

  1. Allen CE, Beldade P, Zwaan BJ, Brakefield PM. 1.  2008. Differences in the selection response of serially repeated color pattern characters: standing variation, development, and evolution. BMC Evol. Biol. 8:94 [Google Scholar]
  2. Arnoult L, Su KFY, Manoel D, Minervino C, Magrina J. 2.  et al. 2013. Emergence and diversification of fly pigmentation through evolution of a gene regulatory module. Science 339:1423–26 [Google Scholar]
  3. Averof M, Patel NH. 3.  1997. Crustacean appendage evolution associated with changes in Hox gene expression. Nature 388:682–86 [Google Scholar]
  4. Beldade P, Brakefield PM. 4.  2003. Concerted evolution and developmental integration in modular butterfly wing patterns. Evol. Dev. 5:169–79 [Google Scholar]
  5. Beldade P, Brakefield PM, Long AD. 5.  2002. Contribution of Distal-less to quantitative variation in butterfly eyespots. Nature 415:315–17 [Google Scholar]
  6. Beldade P, French V, Brakefield PM. 6.  2008. Developmental and genetic mechanisms for evolutionary diversification of serial repeats: eyespot size in Bicyclus anynana butterflies. J. Exp. Zool. B 310:191–201 [Google Scholar]
  7. Beldade P, Koops K, Brakefield PM. 7.  2002. Developmental constraints versus flexibility in morphological evolution. Nature 416:844–47 [Google Scholar]
  8. Beldade P, Koops K, Brakefield PM. 8.  2002. Modularity, individuality, and evo-devo in butterfly wings. Proc. Natl. Acad. Sci. USA 99:14262–67 [Google Scholar]
  9. Biehs B, Sturtevant MA, Bier E. 9.  1998. Boundaries in the Drosophila wing imaginal disc organize vein-specific genetic programs. Development 125:4245–57 [Google Scholar]
  10. Bier E. 10.  2000. Drawing lines in the Drosophila wing: initiation of wing vein development. Curr. Opin. Genet. Dev. 10:393–98 [Google Scholar]
  11. Blair SS. 11.  2007. Wing vein patterning in Drosophila and the analysis of intercellular signaling. Annu. Rev. Cell Dev. Biol. 23:293–319 [Google Scholar]
  12. Brakefield PM, French V. 12.  1995. Eyespot development on butterfly wings: the epidermal response to damage. Dev. Biol. 168:98–111 [Google Scholar]
  13. Brakefield PM, Gates J, Keys D, Kesbeke F, Wijngaarden PJ. 13.  et al. 1996. Development, plasticity, and evolution of butterfly eyespot patterns. Nature 384:236–42 [Google Scholar]
  14. Breuker CJ, Brakefield PM. 14.  2002. Female choice depends on size but not symmetry of dorsal eyespots in the butterfly Bicyclus anynana. Proc. R. Soc. B 269:1233–39 [Google Scholar]
  15. Brunetti CR, Selegue JE, Monteiro A, French V, Brakefield PM, Carroll SB. 15.  2001. The generation and diversification of butterfly eyespot color patterns. Curr. Biol. 11:1578–85 [Google Scholar]
  16. Carroll SB, Gates J, Keys DN, Paddock SW, Panganiban GEF. 16.  et al. 1994. Pattern formation and eyespot determination in butterfly wings. Science 265:109–14 [Google Scholar]
  17. Chen B, Hrycaj S, Schinko JB, Podlaha O, Wimmer EA. 17.  et al. 2011. Pogostick: a new versatile piggyBac vector for inducible gene over-expression and down-regulation in emerging model systems. PLOS ONE 6:e18659 [Google Scholar]
  18. Costanzo K, Monteiro A. 18.  2007. The use of chemical and visual cues in female choice in the butterfly Bicyclus anynana. Proc. R. Soc. B 274:845–51 [Google Scholar]
  19. Darwin C. 19.  1871. The Descent of Man and Selection in Relation to Sex London: John Murray
  20. Dilao R, Sainhas J. 20.  2004. Modelling butterfly wing eyespot patterns. Proc. R. Soc. B 271:1565–69 [Google Scholar]
  21. Evans TM, Marcus JM. 21.  2006. A simulation study of the genetic regulatory hierarchy for butterfly eyespot focus determination. Evol. Dev. 8:273–83 [Google Scholar]
  22. Freitas R, Zhang GJ, Cohn MJ. 22.  2006. Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature 442:1033–37 [Google Scholar]
  23. French V, Brakefield PM. 23.  1992. The development of eyespot patterns on butterfly wings: morphogen sources or sinks?. Development 116:103–9 [Google Scholar]
  24. French V, Brakefield PM. 24.  1995. Eyespot development on butterfly wings: the focal signal. Dev. Biol. 168:112–23 [Google Scholar]
  25. Held LI. 25.  2013. Rethinking butterfly eyespots. Evol. Biol. 40:158–68 [Google Scholar]
  26. Keys DN, Lewis DL, Selegue JE, Pearson BJ, Goodrich LV. 26.  et al. 1999. Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 283:532–34 [Google Scholar]
  27. Kodandaramaiah U. 27.  2009. Eyespot evolution: phylogenetic insights from Junonia and related butterfly genera (Nymphalidae: Junoniini). Evol. Dev. 11:489–97 [Google Scholar]
  28. Kodandaramaiah U. 28.  2011. The evolutionary significance of butterfly eyespots. Behav. Ecol. 22:1264–71 [Google Scholar]
  29. Kopp A. 29.  2012. Dmrt genes in the development and evolution of sexual dimorphism. Trends Genet. 28:175–84 [Google Scholar]
  30. Kunte K, Zhang W, Tenger-Trolander A, Palmer DH, Martin A. 30.  et al. 2014. doublesex is a mimicry supergene. Nature 507:229–32 [Google Scholar]
  31. Liubicich DM, Serano JM, Pavlopoulos A, Kontarakis Z, Protas ME. 31.  et al. 2009. Knockdown of Parhyale Ultrabithorax recapitulates evolutionary changes in crustacean appendage morphology. Proc. Natl. Acad. Sci. USA 106:13892–96 [Google Scholar]
  32. Lyytinen A, Brakefield PM, Mappes J. 32.  2003. Significance of butterfly eyespots as an anti-predator device in ground-based and aerial attacks. Oikos 100:373–79 [Google Scholar]
  33. Marcellini S, Simpson P. 33.  2006. Two or four bristles: functional evolution of an enhancer of scute in Drosophilidae. PLOS Biol. 4:2252–61 [Google Scholar]
  34. Marcus JM, Evans TM. 34.  2008. A simulation study of mutations in the genetic regulatory hierarchy for butterfly eyespot focus determination. Biosystems 93:250–55 [Google Scholar]
  35. McGregor AP, Orgogozo V, Delon I, Zanet J, Srinivasan DG. 35.  et al. 2007. Morphological evolution through multiple cis-regulatory mutations at a single gene. Nature 448:587–90 [Google Scholar]
  36. Merilaita S, Vallin A, Kodandaramaiah U, Dimitrova M, Ruuskanen S, Laaksonen T. 36.  2011. Number of eyespots and their intimidating effect on naive predators in the peacock butterfly. Behav. Ecol. 22:1326–31 [Google Scholar]
  37. Monteiro A. 37.  2008. Alternative models for the evolution of eyespots and of serial homology on lepidopteran wings. BioEssays 30:358–66 [Google Scholar]
  38. Monteiro A. 38.  2012. Gene regulatory networks reused to build novel traits. BioEssays 34:181–86 [Google Scholar]
  39. Monteiro A, Brakefield P, French V. 39.  1997. Butterfly eyespots: the genetics and development of the color rings. Evol. Int. J. Org. Evol. 51:1207–16 [Google Scholar]
  40. Monteiro A, Chen B, Ramos DM, Oliver JC, Tong X. 40.  et al. 2013. Distal-less regulates eyespot patterns and melanization in Bicyclus butterflies. J. Exp. Zool. B 320:321–31 [Google Scholar]
  41. Monteiro A, French V, Smit G, Brakefield P, Metz J. 41.  2001. Butterfly eyespot patterns: evidence for specification by a morphogen diffusion gradient. Acta Biotheor. 49:77–88 [Google Scholar]
  42. Monteiro A, Glaser G, Stockslager S, Glansdorp N, Ramos D. 42.  2006. Comparative insights into questions of lepidopteran wing pattern homology. BMC Dev. Biol. 6:52 [Google Scholar]
  43. Monteiro A, Podlaha O. 43.  2009. Wings, horns, and butterfly eyespots: How do complex traits evolve?. PLOS Biol. 7:2e1000037 [Google Scholar]
  44. Monteiro A, Prijs J, Bax M, Hakkaart T, Brakefield P. 44.  2003. Mutants highlight the modular control of butterfly eyespot patterns. Evol. Dev. 5:180–87 [Google Scholar]
  45. Monteiro A, Prudic KL. 45.  2010. Multiple approaches to study color pattern evolution in butterflies. Trends Evol. Biol. 2:e2 [Google Scholar]
  46. Monteiro AF, Brakefield PM, French V. 46.  1994. The evolutionary genetics and developmental basis of wing pattern variation in the butterfly Bicyclus anynana. Evol. Int. J. Org. Evol. 48:1147–57 [Google Scholar]
  47. Nijhout HF. 47.  1978. Wing pattern formation in Lepidoptera—a model. J. Exp. Zool. 206:119–36 [Google Scholar]
  48. Nijhout HF. 48.  1980. Pattern formation on lepidopteran wings: determination of an eyespot. Dev. Biol. 80:267–74 [Google Scholar]
  49. Nijhout HF. 49.  1990. A comprehensive model for colour pattern formation in butterflies. Proc. R. Soc. B 239:81–113 [Google Scholar]
  50. Nijhout HF. 50.  1991. The Development and Evolution of Butterfly Wing Patterns Washington, DC: Smithson. Inst. Press
  51. Nijhout HF. 51.  2001. Elements of butterfly wing patterns. J. Exp. Zool. 291:213–25 [Google Scholar]
  52. Oliver JC, Beaulieu JM, Gall LF, Piel WH, Monteiro A. 52.  2014. Nymphalid eyespot serial homologues originate as a few individualized modules. Proc. R. Soc. B 281:20133262 [Google Scholar]
  53. Oliver JC, Monteiro A. 53.  2011. On the origins of sexual dimorphism in butterflies. Proc. R. Soc. B 278:1981–88 [Google Scholar]
  54. Oliver JC, Robertson KA, Monteiro A. 54.  2009. Accomodating natural and sexual selection in butterfly wing pattern evolution. Proc. R. Soc. B 276:2369–75 [Google Scholar]
  55. Oliver JC, Tong X-L, Gall LF, Piel WH, Monteiro A. 55.  2012. A single origin for nymphalid butterfly eyespots followed by widespread loss of associated gene expression. PLOS Genet. 8:e1002893 [Google Scholar]
  56. Olofsson M, Jakobsson S, Wiklund C. 56.  2013. Bird attacks on a butterfly with marginal eyespots and the role of prey concealment against the background. Biol. J. Linn. Soc. 109:290–97 [Google Scholar]
  57. Olofsson M, Lovlie H, Tibblin J, Jakobsson S, Wiklund C. 57.  2013. Eyespot display in the peacock butterfly triggers antipredator behaviors in naive adult fowl. Behav. Ecol. 24:305–10 [Google Scholar]
  58. Olofsson M, Vallin A, Jakobsson S, Wiklund C. 58.  2010. Marginal eyespots on butterfly wings deflect bird attacks under low light intensities with UV wavelengths. PLOS ONE 5:5e10798 [Google Scholar]
  59. Otaki JM. 59.  2011. Color-pattern analysis of eyespots in butterfly wings: a critical examination of morphogen gradient models. Zool. Sci. 28:403–13 [Google Scholar]
  60. Otaki JM. 60.  2011. Generation of butterfly wing eyespot patterns: a model for morphological determination of eyespot and parafocal element. Zool. Sci. 28:817–27 [Google Scholar]
  61. Otaki JM. 61.  2012. Color pattern analysis of nymphalid butterfly wings: revision of the nymphalid groundplan. Zool. Sci. 29:568–76 [Google Scholar]
  62. Otaki JM, Ogasawara T, Yamamoto H. 62.  2005. Morphological comparison of pupal wing cuticle patterns in butterflies. Zool. Sci. 22:21–34 [Google Scholar]
  63. Pinheiro CEG, Antezana MA, Machado LP. 63.  2014. Evidence for the deflective function of eyespots in wild Junonia evarete Cramer (Lepidoptera, Nymphalidae). Neotrop. Entomol. 43:39–47 [Google Scholar]
  64. Poulton EB. 64.  1890. The Colours of Animals: Their Meaning and Use, Especially Considered in the Case of Insects London: Kegan Paul, Trench, Trübner
  65. Prudic KL, Jeon C, Cao H, Monteiro A. 65.  2011. Developmental plasticity in sexual roles of butterfly species drives mutual sexual ornamentation. Science 331:73–75 [Google Scholar]
  66. Robertson KA, Monteiro A. 66.  2005. Female Bicyclus anynana butterflies choose males on the basis of their dorsal UV-reflective eyespot pupils. Proc. R. Soc. B 272:1541–46 [Google Scholar]
  67. Ruvinsky I, Gibson-Brown JJ. 67.  2000. Genetic and developmental bases of serial homology in vertebrate limb evolution. Development 127:5233–44 [Google Scholar]
  68. Saenko SV, Brakefield PM, Beldade P. 68.  2010. Single locus affects embryonic segment polarity and multiple aspects of an adult evolutionary novelty. BMC Biol. 8:111d [Google Scholar]
  69. Saenko SV, Marialva MSP, Beldade P. 69.  2011. Involvement of the conserved Hox gene Antennapedia in the development and evolution of a novel trait. EvoDevo 2:9 [Google Scholar]
  70. Shirai LT, Saenko SV, Keller RA, Jeronimo MA, Brakefield PM. 70.  et al. 2012. Evolutionary history of the recruitment of conserved developmental genes in association to the formation and diversification of a novel trait. BMC Evol. Biol. 12:21 [Google Scholar]
  71. Sourakov A. 71.  2013. Two heads are better than one: False head allows Calycopis cecrops (Lycaenidae) to escape predation by a jumping spider, Phidippus pulcherrimus (Salticidae). J. Nat. Hist. 47:1047–54 [Google Scholar]
  72. Stevens M. 72.  2005. The role of eyespots as anti-predator mechanisms, principally demonstrated in the Lepidoptera. Biol. Rev. 80:573–88 [Google Scholar]
  73. Stevens M, Hardman CJ, Stubbins CL. 73.  2008. Conspicuousness, not eye mimicry, makes “eyespots” effective antipredator signals. Behav. Ecol. 19:525–31 [Google Scholar]
  74. Stevens M, Hopkins E, Hinde W, Adcock A, Connolly Y. 74.  et al. 2007. Field experiments on the effectiveness of ‘eyespots’ as predator deterrents. Anim. Behav. 74:1215–27 [Google Scholar]
  75. Stevens M, Ruxton GD. 75.  2014. Do animal eyespots really mimic eyes?. Curr. Zool. 60:26–36 [Google Scholar]
  76. Stevens M, Stubbins CL, Hardman CJ. 76.  2008. The anti-predator function of ‘eyespots’ on camouflaged and conspicuous prey. Behav. Ecol. Sociobiol. 62:1787–93 [Google Scholar]
  77. Stoehr AM, Walker JF, Monteiro A. 77.  2013. Spalt expression and the development of melanic color patterns in pierid butterflies. EvoDevo 4:6 [Google Scholar]
  78. Tokita CK, Oliver JC, Monteiro A. 78.  2013. A survey of eyespot sexual dimorphism across nymphalid butterflies. Int. J. Evol. Biol. 2013:926702 [Google Scholar]
  79. Tomoyasu Y, Wheeler SR, Denell RE. 79.  2005. Ultrabithorax is required for membranous wing identity in the beetle Tribolium castaneum. Nature 433:643–47 [Google Scholar]
  80. Tong X, Lindemann A, Monteiro A. 80.  2012. Differential involvement of Hedgehog signaling in butterfly wing and eyespot development. PLOS ONE 7:e51087 [Google Scholar]
  81. Vallin A, Jakobsson S, Lind J, Wiklund C. 81.  2005. Prey survival by predator intimidation: an experimental study of peacock butterfly defence against blue tits. Proc. R. Soc. B 272:1203–7 [Google Scholar]
  82. Vlieger L, Brakefield PM. 82.  2007. The deflection hypothesis: Eyespots on the margins of butterfly wings do not influence predation by lizards. Biol. J. Linn. Soc. 92:661–67 [Google Scholar]
  83. Wahlberg N, Leneveu J, Kodandaramaiah U, Pena C, Nylin S. 83.  et al. 2009. Nymphalid butterflies diversify following near demise at the cretaceous/tertiary boundary. Proc. R. Soc. B 276:4295–302 [Google Scholar]
  84. Weatherbee SD, Halder G, Kim J, Hudson A, Carroll S. 84.  1998. Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. Genes Dev. 12:1474–82 [Google Scholar]
  85. Werner T, Koshikawa S, Williams TM, Carroll SB. 85.  2010. Generation of a novel wing colour pattern by the Wingless morphogen. Nature 464:1143–48 [Google Scholar]
  86. Westerman EL, Hodgins-Davis A, Dinwiddie A, Monteiro A. 86.  2012. Biased learning affects mate choice in a butterfly. Proc. Natl. Acad. Sci. USA 109:10948–53 [Google Scholar]
  87. Williams TM, Carroll SB. 87.  2009. Genetic and molecular insights into the development and evolution of sexual dimorphism. Nat. Rev. Genet. 10:797–804 [Google Scholar]
  88. Wittkopp PJ, Beldade P. 88.  2009. Development and evolution of insect pigmentation: genetic mechanisms and the potential consequences of pleiotropy. Semin. Cell Dev. Biol. 20:65–71 [Google Scholar]
  89. Wittkopp PJ, True JR, Carroll SB. 89.  2002. Reciprocal functions of the Drosophila yellow and ebony proteins in the development and evolution of pigment patterns. Development 129:1849–58 [Google Scholar]
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