Abstract
Insects have various color patterns on their bodies and have played major roles in elucidating the mechanisms of color pattern formation because of their suitability as experimental models. In particular, studies of Drosophila (fruit flies) and butterflies have produced a number of new findings. The logic of generation of a color pattern from the combination of the spatial information of body parts, the genes responsible for those processes, and the mechanism of generating a novel color pattern by cis-regulatory evolution have been elucidated by Drosophila studies. In butterfly studies, attempts to find color pattern genes through genome-wide analysis and functional analysis of color pattern genes using genome editing technology are producing new results. Theoretical models to explain complex eyespot patterning in butterflies have been developed and are awaiting verification with experimental results. A comprehensive model to explain general color pattern formation in insects and validation with empirical data is required.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Alexandre C, Baena-Lopez A, Vincent JP (2014) Patterning and growth control by membrane-tethered wingless. Nature 505:180–185
Ando T, Matsuda T, Goto K, Hara K, Ito A, Hirata J, Yatomi J, Kajitani R, Okuno M, Yamaguchi K, Kobayashi M, Takano T, Minakuchi Y, Seki M, Suzuki Y, Yano K, Itoh T, Shigenobu S, Toyoda A, Niimi T (2018) Repeated inversions within a pannier intron drive diversification of intraspecific colour patterns of ladybird beetles. Nat Commun 9:3893
Arnoult L, Su KFY, Manoel D, Minervino C, Magriña J, Gompel N, Prud’homme B (2013) Emergence and diversification of fly pigmentation through evolution of a gene regulatory module. Science 339:1423–1426
Brakefield PM, Gates J, Keys D, Kesbeke F, Wijngaarden PJ, Montelro A, French V, Carroll SB (1996) Development, plasticity and evolution of butterfly eyespot patterns. Nature 384:236–242
Brunetti CR, Selegue JE, Monteiro A, French V, Brakefield PM, Carroll SB (2001) The generation and diversification of butterfly eyespot color patterns. Curr Biol 11:1578–1585
Carroll SB (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134:25–36
Carroll SB, Gates J, Keys DN, Paddock SW, Panganiban GE, Selegue JE, Williams JA (1994) Pattern formation and eyespot determination in butterfly wings. Science 265:109–114
Carson HL, Hardy DE, Spieth HT, Stone WS (1970) The evolutionary biology of the Hawaiian Drosophilidae. In: Essays in evolution and genetics in honor of Theodosius Dobzhansky. North-Holland Publishing, Amsterdam, pp 437–543
Clarke CA, Sheppard PM (1972) The genetics of the mimetic butterfly Papilio polytes L. Phil Trans R Soc Lond B 263:431–458
Connahs H, Tlili S, van Creij J, Loo TY, Banerjee T, Saunders TE, Monteiro A (2019) Activation of butterfly eyespots by distal-less is consistent with a reaction-diffusion process. Development 146:dev169367
Cott HB (1940) Adaptive coloration in animals. Methuen, London
Dhungel B, Ohno Y, Matayoshi R, Iwasaki M, Taira W, Adhikari K, Gurung R, Otaki JM (2016) Distal-less induces elemental color patterns in Junonia butterfly wings. Zool Lett 2:4
Dufour HD, Koshikawa S, Finet C (2020) Temporal flexibility of gene regulatory network underlies a novel wing pattern in flies. Proc Natl Acad Sci USA 117:11589–11596
Fukutomi Y, Koshikawa S (2018) Present and future of research on pattern formation of insects (in Japanese). Sanshi-Konchu Biotech 87:95–102
Fukutomi Y, Matsumoto K, Agata K, Funayama N, Koshikawa S (2017) Pupal development and pigmentation process of a polka-dotted fruit fly, Drosophila guttifera (Insecta, Diptera). Dev Genes Evol 227:171–180
Fukutomi Y, Matsumoto K, Funayama N, Koshikawa S (2018) Methods for staging pupal periods and measurement of wing pigmentation of Drosophila guttifera. J Vis Exp 131:e56935
Fukutomi Y, Kondo S, Toyoda A, Shigenobu S, Koshikawa S (2021) Transcriptome analysis reveals wingless regulates neural development and signaling genes in the region of wing pigmentation of the polka-dotted fruit fly. FEBS J 288:115–126
Futahashi R, Osanai-Futahashi M (2021) Pigments in insects. In: Pigments, pigment cells and pigment patterns. Springer, Singapore, pp 3–43
Gautier M, Yamaguchi J, Foucaud J, Loiseau A, Ausset A, Facon B, Gschloessl B, Lagnel J, Loire E, Parrinello H, Severac D, Lopez-Roques C, Donnadieu C, Manno M, Berges H, Gharbi K, Lawson-Handley L, Zang LS, Vogel H, Estoup A, Prud’homme B (2018) The genomic basis of colour pattern polymorphism in the harlequin ladybird. Curr Biol 28:3296–3302
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
Han Q, Fang J, Ding H, Johnson JK, Christensen BM, Li J (2002) Identification of Drosophila melanogaster yellow-f and yellow-f2 proteins as dopachrome-conversion enzymes. Biochem J 368:333–340
Hinaux H, Bachem K, Battistara M, Rossi M, Xin Y, Jaenichen R, Le Poul Y, Arnoult L, Kobler JM, Grunwald Kadow IC, Rodermund L, Prud’homme B, Gompel N (2018) Revisiting the developmental and cellular role of the pigmentation gene yellow in Drosophila using a tagged allele. Dev Biol 438:111–123
Ito K, Katsuma S, Kuwazaki S, Jouraku A, Fujimoto T, Sahara K, Yasukochi Y, Yamamoto K, Tabunoki H, Yokoyama T, Kadono-Okuda K (2016) Mapping and recombination analysis of two moth colour mutations, black moth and wild wing spot, in the silkworm Bombyx mori. Heredity 116:52–59
Iwata M, Otaki JM (2016) Spatial patterns of correlated scale size and scale color in relation to color pattern elements in butterfly wings. J Insect Physiol 85:32–45
Izumitani HF, Kusaka Y, Koshikawa S, Toda MJ, Katoh T (2016) Phylogeography of the subgenus Drosophila (Diptera: Drosophilidae): evolutionary history of faunal divergence between the old and the new worlds. PLoS One 11:e0160051
Jeong S, Rokas A, Carroll SB (2006) Regulation of body pigmentation by the abdominal-B Hox protein and its gain and loss in Drosophila evolution. Cell 125:1387–1399
Joron M, Papa R, Beltrán M, Chamberlain N, Mavárez J, Baxter S, Abanto M, Bermingham E, Humphray SJ, Rogers J, Beasley H (2006) A conserved supergene locus controls colour pattern diversity in Heliconius butterflies. PLoS Biol 4:e303
Keys DN, Lewis DL, Selegue JE, Pearson BJ, Goodrich LV, Johnson RL, Gates J, Scott MP, Carroll SB (1999) Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 283:532–534
Kopp A, Duncun I, Carroll SB (2000) Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408:553–559
Koshikawa S (2015) Enhancer modularity and the evolution of new traits. Fly (Austin) 9:155–159
Koshikawa S (2020) Evolution of wing pigmentation in Drosophila: diversity, physiological regulation, and cis-regulatory evolution. Dev Growth Diff 62:269–278
Koshikawa S, Giorgianni MW, Vaccaro K, Kassner VA, Yoder JH, Werner T, Carroll SB (2015) Gain of cis-regulatory activities underlies novel domains of wingless gene expression in Drosophila. Proc Natl Acad Sci USA 112:7524–7529
Koshikawa S, Matsumoto K, Fukutomi Y (2017) Drosophila guttifera as a model system for unraveling color pattern formation. In: Sekimura T, Nijhout HF (eds) Diversity and evolution of butterfly wing patterns. Springer, Singapore, pp 287–301
Kunte K, Zhang W, Tenger-Trolander A, Palmer DH, Martin A, Reed RD, Mullen SP, Kronforst MR (2014) doublesex is a mimicry supergene. Nature 507:229–232
Lewis JJ, Geltman RC, Pollak PC, Rondem KE, Van Belleghem SM, Hubisz MJ, Munn PR, Zhang L, Benson C, Mazo-Vargas A, Danko CG, Counterman BA, Papa R, Reed RD (2019) Parallel evolution of ancient, pleiotropic enhancers underlies butterfly wing pattern mimicry. Proc Natl Acad Sci USA 116:24174–24183
Linsley EG (1959) Mimetic form and coloration in the Cerambycidae (Coleoptera). Ann Entomol Soc Am 52:125–131
Marcus JM, Ramos DM, Monteiro A (2004) Germline transformation of the butterfly Bicyclus anynana. Proc R Soc Lond B 271(Suppl 5):S263–S265
Markow TA, O’Grady P (2006) Drosophila: a guide to species identification and use. Academic Press, New York
Martin A, Reed RD (2014) Wnt signaling underlies evolution and development of the butterfly wing pattern symmetry systems. Dev Biol 395:367–378
Martin A, Papa R, Nadeau NJ, Hill RI, Counterman BA, Halder G, Jiggins CD, Kronforst MR, Long AD, McMillan WO, Reed RD (2012) Diversification of complex butterfly wing patterns by repeated regulatory evolution of a Wnt ligand. Proc Natl Acad Sci USA 109:12632–12637
Mazo-Vargas A, Concha C, Livraghi L, Massardo D, Wallbank RWR, Zhang L, Papador JD, Martinez-Najera D, Jiggins CD, Kronforst MR, Breuker CJ, Reed RD, Patel NH, McMillan WO, Martin A (2017) Macroevolutionary shifts of WntA function potentiate butterfly wing-pattern diversity. Proc Natl Acad Sci USA 114:10701–10706
Meinhardt H (1982) Models of biological pattern formation. Academic Press, London
Monteiro A (2015) Origin, development, and evolution of butterfly eyespots. Annu Rev Entomol 60:253–271
Monteiro A, Chen B, Ramos DM, Oliver JC, Tong X, Guo M, Wang WK, Fazzino L, Kamal F (2013) Distal-less regulates eyespot patterns and melanization in Bicyclus butterflies. J Exp Zool B 320:321–331
Nadeau NJ, Pardo-Diaz C, Whibley A, Supple MA, Saenko SV, Wallbank RW, Wu GC, Maroja L, Ferguson L, Hanly JJ, Hines H, Salazar C, Merrill RM, Dowling AJ, Llaurens V, Joron M, WO MM, Jiggins CD (2016) The gene cortex controls mimicry and crypsis in butterflies and moths. Nature 534:106–110
Nijhout HF (1980) Pattern formation on lepidopteran wings: determination of an eyespot. Dev Biol 80:267–274
Nijhout HF (1990) A comprehensive model for colour pattern formation in butterflies. Proc R Soc Lond B 239:81–113
Nijhout HF (2001) Elements of butterfly wing patterns. J Exp Zool (Mol Dev Evol) 291:213–225
Nijhout HF (2002) The nature of robustness in development. BioEssays 24:553–563
Nijhout HF (2017) The common developmental origin of eyespots and parafocal elements and a new model mechanism for color pattern formation. In: Sekimura T, Nijhout HF (eds) Diversity and evolution of butterfly wing patterns. Springer, Singapore, pp 3–9
Nishikawa H, Iijima T, Kajitani R, Yamaguchi J, Ando T, Suzuki Y, Sugano S, Fujiyama A, Kosugi S, Hirakawa H, Tabata S, Ozaki K, Morimoto H, Ihara K, Obara M, Hori H, Itoh T, Fujiwara H (2015) A genetic mechanism for female-limited Batesian mimicry in Papilio butterfly. Nat Genet 47:405–409
O’Grady PM, DeSalle R (2018) Phylogeny of the genus Drosophila. Genetics 209:1–25
Ohno Y, Otaki JM (2015) Spontaneous long-range calcium waves in developing butterfly wings. BMC Dev Biol 15:17
Otaki JM (2011) Color-pattern analysis of eyespots in butterfly wings: a critical examination of morphogen gradient models. Zool Sci 28:403–413
Otaki JM (2017) Self-similarity, distortion waves, and the essence of morphogenesis: a generalized view of color pattern formation in butterfly wings. In: Sekimura T, Nijhout HF (eds) Diversity and evolution of butterfly wing patterns. Springer, Singapore, pp 119–152
Özsu N, Chan QY, Chen B, Gupta MD, Monteiro A (2017) Wingless is a positive regulator of eyespot color patterns in Bicyclus anynana butterflies. Dev Biol 429:177–185
Parchure A, Vyas N, Mayor S (2018) Wnt and hedgehog: secretion of lipid-modified morphogens. Trends Cell Biol 28:157–170
Patterson JT, Wagner RP, Wharton LT (1943) The Drosophilidae of the southwest. University of Texas, Texas
Rebeiz M, Williams TM (2017) Using Drosophila pigmentation traits to study the mechanisms of cis-regulatory evolution. Curr Opin Insect Sci 19:1–7
Reed RD, Serfas MS (2004) Butterfly wing pattern evolution is associated with changes in a notch/distal-less temporal pattern formation process. Curr Biol 14:1159–1166
Reed RD, Papa R, Martin A, Hines HM, Counterman BA, Pardo-Diaz C, Jiggins CD, Chamberlain NL, Kronforst MR, Chen R, Halder G, Nijhout HF, McMillan WO (2011) optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 333:1137–1141
Roeske MJ, Camino EM, Grover S, Rebeiz M, Williams TM (2018) Cis-regulatory evolution integrated the Bric-Ã -brac transcription factors into a novel fruit fly gene regulatory network. elife 7:e32273
Rogers WA, Salomone JR, Tacy DJ, Camino EM, Davis KA, Rebeiz M, Williams TM (2013) Recurrent modification of a conserved cis-regulatory element underlies fruit fly pigmentation diversity. PLoS Genet 9:e1003740
Rogers WA, Grover S, Stringer SJ, Parks J, Rebeiz M, Williams TM (2014) A survey of the trans-regulatory landscape for Drosophila melanogaster abdominal pigmentation. Dev Biol 385:417–432
Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, Oxford
Setoguchi S, Takamori H, Aotsuka T, Sese J, Ishikawa Y, Matsuo T (2014) Sexual dimorphism and courtship behavior in Drosophila prolongata. J Ethol 32:91–102
Sherratt TN (2008) The evolution of Müllerian mimicry. Naturwissenschaften 95:681–695
Stern DL, Orgogozo V (2008) The loci of evolution: how predictable is genetic evolution? Evolution 62:2155–2177
Taira W, Otaki JM (2016) Butterfly wings are three-dimensional: pupal cuticle focal spots and their associated structures in Junonia butterflies. PLoS One 11:e0146348
Tong X, Lindemann A, Monteiro A (2012) Differential involvement of hedgehog signaling in butterfly wing and eyespot development. PLoS One 7:e51087
Tong X, Hrycaj S, Podlaha O, Popadic A, Monteiro A (2014) Over-expression of Ultrabithorax alters embryonic body plan and wing patterns in the butterfly Bicyclus anynana. Dev Biol 394:357–366
True JR, Edwards KA, Yamamoto D, Carroll SB (1999) Drosophila wing melanin patterns form by vein-dependent elaboration of enzymatic prepatterns. Curr Biol 9:1382–1391
Turing AM (1952) The chemical basis of morphogenesis. Phil Trans R Soc Lond B 237:37–72
Van Belleghem SM, Rastas P, Papanicolaou A, Martin SH, Arias CF, Supple MA, Hanly JJ, Mallet J, Lewis JJ, Hines HM, Ruiz M, Salazar C, Linares M, Moreira GRP, Jiggins CD, Counterman BA, McMillan WO, Papa R (2017) Complex modular architecture around a simple toolkit of wing pattern genes. Nat Ecol Evol 1:52
van’t Hof AE, Campagne P, Rigden DJ, Yung CJ, Lingley J, Quail MA, Hall N, Darby AC, Saccheri IJ (2016) The industrial melanism mutation in British peppered moths is a transposable element. Nature 534:102–105
Wallbank RW, Baxter SW, Pardo-Diaz C, Hanly JJ, Martin SH, Mallet J, Dasmahapatra KK, Salazar C, Joron M, Nadeau N, McMillan WO, Jiggins CD (2016) Evolutionary novelty in a butterfly wing pattern through enhancer shuffling. PLoS Biol 14:e1002353
Werner T, Koshikawa S, Williams TM, Carroll SB (2010) Generation of a novel wing colour pattern by the wingless morphogen. Nature 464:1143–1148
Werner T, Steenwinkel T, Jaenike J (2018) The encyclopedia of north American Drosophilids volume 1: Drosophilids of the Midwest and Northeast. Michigan Technological University, Houghton
Williams TM, Selegue JE, Werner T, Gompel N, Kopp A, Carroll SB (2008) The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila. Cell 134:610–623
Wittkopp PJ, True JR, Carroll SB (2002) Reciprocal functions of the Drosophila yellow and ebony proteins in the development and evolution of pigment patterns. Development 129:1849–1858
Wittkopp PJ, Carroll SB, Kopp A (2003) Evolution in black and white: genetic control of pigment patterns in Drosophila. Trends Genet 19:495–504
Yamaguchi J, Banno Y, Mita K, Yamamoto K, Ando T, Fujiwara H (2013) Periodic Wnt1 expression in response to ecdysteroid generates twin-spot markings on caterpillars. Nat Commun 4:1857
Yassin A, Delaney EK, Reddiex AJ, Seher TD, Bastide H, Appleton NC, Lack JB, David JR, Chenoweth SF, Pool JE, Kopp A (2016) The pdm3 locus is a hotspot for recurrent evolution of female-limited color dimorphism in Drosophila. Curr Biol 26:2412–2422
Zhang L, Reed RD (2016) Genome editing in butterflies reveals that spalt promotes and Distal-less represses eyespot colour patterns. Nat Commun 15:11769
Zhang L, Mazo-Vargas A, Reed RD (2017) Single master regulatory gene coordinates the evolution and development of butterfly color and iridescence. Proc Natl Acad Sci USA 114:10707–10712
Acknowledgements
We thank Ryo Futahashi for giving us an opportunity to write this chapter, Toshiya Ando for helpful comments, and Elizabeth Nakajima for comments and English editing. This chapter is partially based on our review article published in the Japanese language (Fukutomi and Koshikawa 2018). Part of the writing was supported by KAKENHI (17Â K19427, 18H02486, 18Â J20452).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Fukutomi, Y., Koshikawa, S. (2021). Mechanism of Color Pattern Formation in Insects. In: Hashimoto, H., Goda, M., Futahashi, R., Kelsh, R., Akiyama, T. (eds) Pigments, Pigment Cells and Pigment Patterns. Springer, Singapore. https://doi.org/10.1007/978-981-16-1490-3_12
Download citation
DOI: https://doi.org/10.1007/978-981-16-1490-3_12
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-16-1489-7
Online ISBN: 978-981-16-1490-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)