Skip to main content

Pigments in Insects

  • Chapter
  • First Online:
Pigments, Pigment Cells and Pigment Patterns

Abstract

Insects have an amazing variety of colors and patterns. It should be noted that pigments and/or genes involved in body color formation are markedly different between insects and vertebrates. Insect pigments have been traditionally classified into the following eight classes: melanins, ommochromes, pteridines, tetrapyrroles, carotenoids, flavonoids, papiliochromes, and quinones. Among them, melanins, ommochromes, and pteridines are three major pigments that are distributed in most insects. Insect melanins are secreted into cuticles, and dark-colored melanins are predominantly derived from dopamine, whereas light-colored melanins are mostly derived from N-β-alanyldopamine (NBAD) and/or N-acetyldopamine (NADA). Ommochromes are tryptophan-derived pigments restricted to invertebrates and are ubiquitous in the compound eyes of insects. Ommochromes and pteridines are accumulated within pigment granules ommochromasomes and pterinosomes, respectively. In recent years, much has been revealed at the molecular level about pigment synthesis and pattern formation in insects. In this review, we introduce the relationship between the pigments and insect color pattern, and summarize the genes involved in the pigment synthesis, transport, and patterning. Meanwhile, there are still many insects whose pigments have not been identified, and the future progress is expected in this field.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adelmann CH, Traunbauer AK, Chen B, Condon KJ, Chan SH, Kunchok T, Lewis CA, Sabatini DM (2020) MFSD12 mediates the import of cysteine into melanosomes and lysosomes. Nature 588:699–704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahmed-Braimah YH, Sweigart AL (2015) A single gene causes an interspecific difference in pigmentation in Drosophila. Genetics 200(1):331–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anbutsu H, Moriyama M, Nikoh N, Hosokawa T, Futahashi R, Tanahashi M, Meng XY, Kuriwada T, Mori N, Oshima K, Hattori M, Fujie M, Satoh N, Maeda T, Shigenobu S, Koga R, Fukatsu T (2017) Small genome symbiont underlies cuticle hardness in beetles. Proc Natl Acad Sci U S A 114(40):E8382–E8391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(1):3843

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arakane Y, Muthukrishnan S, Beeman RW, Kanost MR, Kramer KJ (2005) Laccase 2 is the phenoloxidase gene required for beetle cuticle tanning. Proc Natl Acad Sci U S A 102(32):11337–11342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arakane Y, Lomakin J, Beeman RW, Muthukrishnan S, Gehrke SH, Kanost MR, Kramer KJ (2009) Molecular and functional analyses of amino acid decarboxylases involved in cuticle tanning in Tribolium castaneum. J Biol Chem 284:16584–16594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arakane Y, Dittmer NT, Tomoyasu Y, Kramer KJ, Muthukrishnan S, Beeman RW, Kanost MR (2010) Identification, mRNA expression and functional analysis of several yellow family genes in Tribolium castaneum. Insect Biochem Mol Biol 40(3):259–266

    Article  CAS  PubMed  Google Scholar 

  • Arakane Y, Noh MY, Asano T, Kramer KJ (2016) Tyrosine metabolism for insect cuticle pigmentation and sclerotization. In: Cohen E, Moussian B (eds) Extracellular composite matrices in arthropods. Springer, New York, pp 165–220

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ashida M (1990) The prophenoloxidase cascade in insect immunity. Res Immunol 141(9):908–910

    Article  CAS  PubMed  Google Scholar 

  • Barbier M (1984) A substance which acts as a pH indicator from the moth Euchloron megaera L. J Chem Ecol 10(7):1109–1113

    Article  CAS  PubMed  Google Scholar 

  • Barek H, Sugumaran M, Ito S, Wakamatsu K (2018) Insect cuticular melanins are distinctly different from those of mammalian epidermal melanins. Pigment Cell Melanoma Res 31(3):384–392

    Article  CAS  PubMed  Google Scholar 

  • Bel Y, Porcarm M, Socha R, Nemec V, Ferre J (1997) Analysis of pteridines in Pyrrhocoris apterus (L.) (heteroptera, pyrrhocoridae) during development and in body - color mutants. Arch Insect Biochem Physiol 34:83–98

    Article  CAS  Google Scholar 

  • Bolognese A, Liberatore R, Scherillo G (1988) Photochemistry of ommochromes and related compounds. J Heterocyclic Chem 25:979–983

    Article  CAS  Google Scholar 

  • Bowie JH, Cameron DW, Findlay JA, Quartey JAK (1966) Haemolymph pigments of aphids. Nature 210:395–397

    Article  CAS  Google Scholar 

  • Braasch I, Schartl M, Volff JN (2007) Evolution of pigment synthesis pathways by gene and genome duplication in fish. BMC Evol Biol 11(7):74

    Article  CAS  Google Scholar 

  • Brodbeck D, Amherd R, Callaerts P, Hintermann E, Meyer UA, Affolter M (1998) Molecular and biochemical characterization of the aaNAT1 (Dat) locus in Drosophila melanogaster: differential expression of two gene products. DNA Cell Biol 17(7):621–633

    Article  CAS  PubMed  Google Scholar 

  • Bückmann D (1977) Morphological colour change (1): stage independent, optically induced ommochrome synthesis in larvae of the stick insect, Carausius morosus Br. J Comp Physiol 115(2):185–193

    Article  Google Scholar 

  • Bückmann D (1979) Morphological colour change (2): the effects of total and partial blinding on epidermal ommochrome content in the stick insect, Carausius morosus Br. J Comp Physiol 130(4):331–336

    Article  Google Scholar 

  • Burghardt F, Knüttel H, Becker M, Fiedler K (2000) Flavonoid wing pigments increase attractiveness of female common blue (Polyommatus icarus) butterflies to mate-searching males. Naturwissenschaften 87(7):304–307

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Cheli VT, Daniels RW, Godoy R, Hoyle DJ, Kandachar V, Starcevic M, Martinez-Agosto JA, Poole S, DiAntonio A, Lloyd VK, Chang HC, Krantz DE, Dell'Angelica EC (2010) Genetic modifiers of abnormal organelle biogenesis in a Drosophila model of BLOC-1 deficiency. Hum Mol Genet 19(5):861–878

    Article  CAS  PubMed  Google Scholar 

  • Cobbs C, Heath J, Stireman JO, Abbot P (2013) Carotenoids in unexpected places: gall midges, lateral gene transfer, and carotenoid biosynthesis in animals. Mol Phylogenet Evol 68(2):221–228

    Article  CAS  PubMed  Google Scholar 

  • Concha C, Wallbank RWR, Hanly JJ, Fenner J, Livraghi L, Rivera ES, Paulo DF, Arias C, Vargas M, Sanjeev M, Morrison C, Tian D, Aguirre P, Ferrara S, Foley J, Pardo-Diaz C, Salazar C, Linares M, Massardo D, Counterman BA, Scott MJ, Jiggins CD, Papa R, Martin A, McMillan WO (2019) Interplay between developmental flexibility and determinism in the evolution of mimetic Heliconius wing patterns. Curr Biol 29(23):3996–4009

    Article  CAS  PubMed  Google Scholar 

  • Crawford K, Quiroz JFD, Koenig KM, Ahuja N, Albertin CB, Rosenthal JJC (2020) Highly efficient knockout of a squid pigmentation gene. Curr Biol 30(17):3484–3490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dai FY, Qiao L, Tong XL, Cao C, Chen P, Chen J, Lu C, Xiang ZH (2010) Mutations of an arylalkylamine-N-acetyltransferase, Bm-iAANAT, are responsible for silkworm melanism mutant. J Biol Chem 285(25):19553–19560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dai F, Qiao L, Cao C, Liu X, Tong X, He S, Hu H, Zhang L, Wu S, Tan D, Xiang Z, Lu C (2015) Aspartate decarboxylase is required for a normal pupa pigmentation pattern in the silkworm, Bombyx mori. Sci Rep 5:10885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daimon T, Hirayama C, Kanai M, Ruike Y, Meng Y, Kosegawa E, Nakamura M, Tsujimoto G, Katsuma S, Shimada T (2010) The silkworm Green b locus encodes a quercetin 5-O-glucosyltransferase that produces green cocoons with UV-shielding properties. Proc Natl Acad Sci U S A 107(25):11471–11476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daniels EV, Murad R, Mortazavi A, Reed RD (2014) Extensive transcriptional response associated with seasonal plasticity of butterfly wing patterns. Mol Ecol 23(24):6123–6134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drapeau MD (2001) The family of yellow-related drosophila melanogaster proteins. Biochem Biophys Res Commun 281(3):611–613

    Article  CAS  PubMed  Google Scholar 

  • Dreesen TD, Johnson DH, Henikoff S (1988) The brown protein of Drosophila melanogaster is similar to the white protein and to components of active transport complexes. Mol Cell Biol 8(12):5206–5215

    CAS  PubMed  PubMed Central  Google Scholar 

  • Falcón-Pérez JM, Romero-Calderón R, Brooks ES, Krantz DE, Dell'Angelica EC (2007) The Drosophila pigmentation gene pink (p) encodes a homologue of human Hermansky-Pudlak syndrome 5 (HPS5). Traffic 8(2):154–168

    Article  PubMed  CAS  Google Scholar 

  • Ferguson LC, Jiggins CD (2009) Shared and divergent expression domains on mimetic Heliconius wings. Evol Dev 11(5):498–512

    Article  CAS  PubMed  Google Scholar 

  • Ferguson LC, Green J, Surridge A, Jiggins CD (2011a) Evolution of the insect yellow gene family. Mol Biol Evol 28(1):257–272

    Article  CAS  PubMed  Google Scholar 

  • Ferguson LC, Maroja L, Jiggins CD (2011b) Convergent, modular expression of ebony and tan in the mimetic wing patterns of Heliconius butterflies. Dev Genes Evol 221(5-6):297–308

    Article  PubMed  Google Scholar 

  • Ferré J, Silva FJ, Real MD, Ménsua JL (1986) Pigment patterns in mutants affecting biosynthesis of pteridines and xanthommatin in Drosophila melanogaster. Biochem Genet 24:545–569

    Article  PubMed  Google Scholar 

  • Feuda R, Marlétaz F, Bentley MA, Holland PW (2016) Conservation, duplication, and divergence of five opsin genes in insect evolution. Genome Biol Evol 8:579–587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Figon F, Casas J (2019) Ommochromes in invertebrates: biochemistry and cell biology. Biol Rev 94:156–183

    Article  Google Scholar 

  • Fitzpatrick PF (2003) Mechanism of aromatic amino acid hydroxylation. Biochemistry 42(48):14083–14091

    Article  CAS  PubMed  Google Scholar 

  • Ford KB (1942) Studies on the chemistry of pigments in the Lepidoptera, with reference to their bearing on systematics. 3. The red pigments of the Papilionidae. Proc R Soc Lond A 17:87–92

    Google Scholar 

  • Fujii T, Abe H, Katsuma S, Mita K, Shimada T (2008) Mapping of sex-linked genes onto the genome sequence using various aberrations of the Z chromosome in Bombyx mori. Insect Biochem Mol Biol 38(12):1072–1079

    Article  CAS  PubMed  Google Scholar 

  • Fujii T, Ozaki M, Masamoto T, Katsuma S, Abe H, Shimada T (2009) A Bombyx mandarina mutant exhibiting translucent larval skin is controlled by the molybdenum cofactor sulfurase gene. Genes Genet Syst 84(2):147–152

    Article  CAS  PubMed  Google Scholar 

  • Fujii T, Banno Y, Abe H, Katsuma S, Shimada T (2012) A homolog of the human Hermansky-Pudluck syndrome-5 (HPS5) gene is responsible for the oa larval translucent mutants in the silkworm, Bombyx mori. Genetica 140(10-12):463–468

    Article  CAS  PubMed  Google Scholar 

  • Fujii T, Abe H, Kawamoto M, Katsuma S, Banno Y, Shimada T (2013) Albino (al) is a tetrahydrobiopterin (BH4)-deficient mutant of the silkworm Bombyx mori. Insect Biochem Mol Biol 43(7):594–600

    Article  CAS  PubMed  Google Scholar 

  • Fujii T, Yamamoto K, Banno Y (2016) Molybdenum cofactor deficiency causes translucent integument, male-biased lethality, and flaccid paralysis in the silkworm Bombyx mori. Insect Biochem Mol Biol 73:20–26

    Article  CAS  PubMed  Google Scholar 

  • Fujii T, Yamamoto K, Banno Y (2018) Translucent larval integument and flaccid paralysis caused by genome editing in a gene governing molybdenum cofactor biosynthesis in Bombyx mori. Insect Biochem Mol Biol 99:11–16

    Article  CAS  PubMed  Google Scholar 

  • Futahashi R (2015) Molecular mechanisms underlying butterfly pattern formation. In: Yagi T (ed) Biology of butterfly pattern formation. Osaka Municipal Universities Press, Osaka, pp 35–66

    Google Scholar 

  • Futahashi R (2016) Color vision and color formation in dragonflies. Curr Opin Insect Sci 17:32–39

    Article  PubMed  Google Scholar 

  • Futahashi R (2017) Molecular mechanisms underlying color vision and color formation in dragonflies. In: Sekimura T, Nijhout HF (eds) Diversity and evolution of butterfly wing patterns: an integrative approach. Springer, Singapore, pp 303–321

    Chapter  Google Scholar 

  • Futahashi R (2020) Diversity of UV reflection patterns in Odonata. Front Ecol Evol 8:201

    Article  Google Scholar 

  • Futahashi R, Fujiwara H (2005) Melanin-synthesis enzymes coregulate stage-specific larval cuticular markings in the swallowtail butterfly, Papilio xuthus. Dev Genes Evol 215:519–529

    Article  CAS  PubMed  Google Scholar 

  • Futahashi R, Fujiwara H (2006) Expression of one isoform of GTP cyclohydrolase I coincides with the larval black markings of the swallowtail butterfly, Papilio xuthus. Insect Biochem Mol Biol 36(1):63–70

    Article  CAS  PubMed  Google Scholar 

  • Futahashi R, Fujiwara H (2007) Regulation of 20-hydroxyecdysone on the larval pigmentation and the expression of melanin synthesis enzymes and yellow gene of the swallowtail butterfly, Papilio xuthus. Insect Biochem Mol Biol 37(8):855–864

    Article  CAS  PubMed  Google Scholar 

  • Futahashi R, Fujiwara H (2008a) Juvenile hormone regulates butterfly larval pattern switches. Science 319(5866):1061

    Article  CAS  PubMed  Google Scholar 

  • Futahashi R, Fujiwara H (2008b) Identification of stage-specific larval camouflage associated genes in the swallowtail butterfly, Papilio xuthus. Dev Genes Evol 218(9):491–504

    Article  CAS  PubMed  Google Scholar 

  • Futahashi R, Sato J, Meng Y, Okamoto S, Daimon T, Yamamoto K, Suetsugu Y, Narukawa J, Takahashi H, Banno Y, Katsuma S, Shimada T, Mita K, Fujiwara H (2008) yellow and ebony are the responsible genes for the larval color mutants of the silkworm Bombyx mori. Genetics 180(4):1995–2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Futahashi R, Banno Y, Fujiwara H (2010) Caterpillar color patterns are determined by a two-phase melanin gene prepatterning process: new evidence from tan and laccase2. Evol Dev 12(2):157–167

    Article  CAS  PubMed  Google Scholar 

  • Futahashi R, Tanaka K, Matsuura Y, Tanahashi M, Kikuchi Y, Fukatsu T (2011) Laccase2 is required for cuticular pigmentation in stinkbugs. Insect Biochem Mol Biol 41(3):191–196

    Article  CAS  PubMed  Google Scholar 

  • Futahashi R, Shirataki H, Narita T, Mita K, Fujiwara H (2012a) Comprehensive microarray-based analysis for stage-specific larval camouflage pattern-associated genes in the swallowtail butterfly, Papilio xuthus. BMC Biol 10:46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Futahashi R, Kurita R, Mano H, Fukatsu T (2012b) Redox alters yellow dragonflies into red. Proc Natl Acad Sci U S A 109(31):12626–12631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Futahashi R, Kawahara-Miki R, Kinoshita M, Yoshitake K, Yajima S, Arikawa K, Fukatsu T (2015) Extraordinary diversity of visual opsin genes in dragonflies. Proc Natl Acad Sci U S A 112(11):E1247–E1256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Futahashi R, Yamahama Y, Kawaguchi M, Mori N, Ishii D, Okude G, Hirai Y, Kawahara-Miki R, Yoshitake K, Yajima S, Hariyama T, Fukatsu T (2019) Molecular basis of wax-based color change and UV reflection in dragonflies. elife 8:e43045

    Article  PubMed  PubMed Central  Google Scholar 

  • Galván I, Jorge A, Edelaar P, Wakamatsu K (2015) Insects synthesize pheomelanin. Pigment Cell Melanoma Res 28(5):599–602

    Article  PubMed  Google Scholar 

  • 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 color pattern polymorphism in the harlequin ladybird. Curr Biol 28(20):3296–3302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geyer PK, Spana C, Corces VG (1986) On the molecular mechanism of gypsy-induced mutations at the yellow locus of Drosophila melanogaster. EMBO J 5(10):2657–2662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gibert JM, Peronnet F, Schlötterer C (2007) Phenotypic plasticity in Drosophila pigmentation caused by temperature sensitivity of a chromatin regulator network. PLoS Genet 3:e30

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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(7025):481–487

    Article  CAS  PubMed  Google Scholar 

  • Gorman MJ, Arakane Y (2010) Tyrosine hydroxylase is required for cuticle sclerotization and pigmentation in Tribolium castaneum. Insect Biochem Mol Biol 40(3):267–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grant P, Maga T, Loshakov A, Singhal R, Wali A, Nwankwo J, Baron K, Johnson D (2016) An eye on trafficking genes: identification of four eye color mutations in Drosophila. G3 (Bethesda) 6(10):3185–3196

    Article  CAS  PubMed Central  Google Scholar 

  • Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, New York

    Google Scholar 

  • Grubbs N, Haas S, Beeman RW, Lorenzen MD (2015) The ABCs of eye color in Tribolium castaneum: orthologs of the Drosophila white, scarlet, and brown genes. Genetics 199(3):749–759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(Pt 1):333–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han Q, Robinson H, Li J (2012) Biochemical identification and crystal structure of kynurenine formamidase from Drosophila melanogaster. Biochem J 446(2):253–260

    Article  CAS  PubMed  Google Scholar 

  • Harris DA, Kim K, Nakahara K, Vasquez-Doorman C, Carthew RW (2011) Cargo sorting to lysosome-related organelles regulates siRNA-mediated gene silencing. J Cell Biol 194:77–87

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henze MJ, Lind O, Wilts BD, Kelber A (2019) Pterin-pigmented nanospheres create the colours of the polymorphic damselfly Ischnura elegans. J R Soc Interface 16(153):20180785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(2):111–123

    Article  CAS  PubMed  Google Scholar 

  • Hines HM, Papa R, Ruiz M, Papanicolaou A, Wang C, Nijhout HF, McMillan WO, Reed RD (2012) Transcriptome analysis reveals novel patterning and pigmentation genes underlying Heliconius butterfly wing pattern variation. BMC Genomics 13:288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirayama C, Ono H, Meng Y, Shimada T, Daimon T (2013) Flavonoids from the cocoon of Rondotia menciana. Phytochemistry 94:108–112

    Article  CAS  PubMed  Google Scholar 

  • Hirayama C, Mase K, Iizuka T, Takasu Y, Okada E, Yamamoto K (2018) Deficiency of a pyrroline-5-carboxylate reductase produces the yellowish green cocoon 'Ryokuken' of the silkworm, Bombyx mori. Heredity 120(5):422–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hiruma K, Riddiford LM, Hopkins TL, Morgan TD (1985) Roles of dopa decarboxylase and phenoloxidase in the melanization of tobacco hornworm and their control by 20-hydroxyecdysone. J Comp Physiol B 155:659–669

    Article  CAS  PubMed  Google Scholar 

  • Hopkins TL, Ahmad SA (1991) Flavonoid wing pigments in grasshoppers. Experientia 47:1089–1091

    Article  CAS  Google Scholar 

  • Iijima T, Kajitani R, Komata S, Lin CP, Sota T, Itoh T, Fujiwara H (2018) Parallel evolution of Batesian mimicry supergene in two Papilio butterflies, P. polytes and P. memnon. Sci Adv 4(4):eaao5416

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Iijima T, Yoda S, Fujiwara H (2019) The mimetic wing pattern of Papilio polytes butterflies is regulated by a doublesex-orchestrated gene network. Commun Biol 2:257

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ito K, Katsuma S, Yamamoto K, Kadono-Okuda K, Mita K, Shimada T (2010) Yellow-e determines the color pattern of larval head and tail spots of the silkworm Bombyx mori. J Biol Chem 285(8):5624–5629

    Article  CAS  PubMed  Google Scholar 

  • Ito K, Kidokoro K, Katsuma S, Shimada T, Yamamoto K, Mita K, Kadono-Okuda K (2012) Positional cloning of a gene responsible for the cts mutation of the silkworm, Bombyx mori. Genome 55(7):493–504

    Article  CAS  PubMed  Google Scholar 

  • Jeong S, Rebeiz M, Andolfatto P, Werner T, True J, Carroll SB (2008) The evolution of gene regulation underlies a morphological difference between two Drosophila sister species. Cell 132(5):783–793

    Article  CAS  PubMed  Google Scholar 

  • Jin H, Seki T, Yamaguchi J, Fujiwara H (2019) Prepatterning of Papilio xuthus caterpillar camouflage is controlled by three homeobox genes: clawless, abdominal-A, and Abdominal-B. Sci Adv 5(4):eaav7569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joron M, Frezal L, Jones RT, Chamberlain NL, Lee SF, Haag CR, Whibley A, Becuwe M, Baxter SW, Ferguson L, Wilkinson PA, Salazar C, Davidson C, Clark R, Quail MA, Beasley H, Glithero R, Lloyd C, Sims S, Jones MC, Rogers J, Jiggins CD, French-Constant RH (2011) Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477:203–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kato T, Sawada H, Yamamoto T, Mase K, Nakagoshi M (2006) Pigment pattern formation in the quail mutant of the silkworm, Bombyx mori: parallel increase of pteridine biosynthesis and pigmentation of melanin and ommochromes. Pigment Cell Res 19(4):337–345

    Article  CAS  PubMed  Google Scholar 

  • Kayser H (1985) Pigments. Comprehensive insect physiology. In: Kerkut GA, Gilbert LI (eds) Biochemistry and pharmacology, vol. 10. Pergamon, New York, pp 367–415

    Google Scholar 

  • Kikkawa H (1941) Mechanism of pigment formation in Bombyx and Drosophila. Genetics 26(6):587–607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim N, Kim J, Park D, Rosen C, Dorsett D, Yim J (1996) Structure and expression of wild-type and suppressible alleles of the Drosophila purple gene. Genetics 142(4):1157–1168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim H, Kim K, Yim J (2013) Biosynthesis of drosopterins, the red eye pigments of Drosophila melanogaster. IUBMB Life 65(4):334–340

    Article  CAS  PubMed  Google Scholar 

  • Kiuchi T, Banno Y, Katsuma S, Shimada T (2011) Mutations in an amino acid transporter gene are responsible for sex-linked translucent larval skin of the silkworm, Bombyx mori. Insect Biochem Mol Biol 41(9):680–687

    Article  CAS  PubMed  Google Scholar 

  • Koch PB, Keys DN, Rocheleau T, Aronstein K, Blackburn M, Carroll SB, French-Constant RH (1998) Regulation of dopa decarboxylase expression during colour pattern formation in wild-type and melanic tiger swallowtail butterflies. Development 125(12):2303–2313

    Article  CAS  PubMed  Google Scholar 

  • Koch PB, Behnecke B, French-Constant RH (2000) The molecular basis of melanism and mimicry in a swallowtail butterfly. Curr Biol 10(10):591–594

    Article  CAS  PubMed  Google Scholar 

  • Kômoto N, Sezutsu H, Yukuhiro K, Banno Y, Fujii H (2003) Mutations of the silkworm molybdenum cofactor sulfurase gene, og, cause translucent larval skin. Insect Biochem Mol Biol 33(4):417–427

    Article  PubMed  CAS  Google Scholar 

  • Kômoto N, Quan GX, Sezutsu H, Tamura T (2009) A single-base deletion in an ABC transporter gene causes white eyes, white eggs, and translucent larval skin in the silkworm w-3(oe) mutant. Insect Biochem Mol Biol 39(2):152–156

    Article  PubMed  CAS  Google Scholar 

  • KonDo Y, Yoda S, Mizoguchi T, Ando T, Yamaguchi J, Yamamoto K, Banno Y, Fujiwara H (2017) Toll ligand Spätzle3 controls melanization in the stripe pattern formation in caterpillars. Proc Natl Acad Sci U S A 114(31):8336–8341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kopp A, Duncan I, Godt D, Carroll SB (2000) Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408(6812):553–559

    Article  CAS  PubMed  Google Scholar 

  • 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 U S A 112(24):7524–7529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krajíček J, Kozlík P, Exnerová A, Stys P, Bursová M, Cabala R, Bosáková Z (2014) Capillary electrophoresis of pterin derivatives responsible for the warning coloration of Heteroptera. J Chromatogr A 1336:94–100

    Article  PubMed  CAS  Google Scholar 

  • Kronforst MR, Papa R (2015) The functional basis of wing patterning in Heliconius butterflies: the molecules behind mimicry. Genetics 200(1):1–19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(7491):229–232

    Article  CAS  PubMed  Google Scholar 

  • 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 U S A 116(48):24174–24183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindgren J, Nilsson DE, Sjövall P, Jarenmark M, Ito S, Wakamatsu K, Kear BP, Schultz BP, Sylvestersen RL, Madsen H, LaFountain JR Jr, Alwmark C, Eriksson ME, Hall SA, Lindgren P, Rodríguez-Meizoso I, Ahlberg P (2019) Fossil insect eyes shed light on trilobite optics and the arthropod pigment screen. Nature 573(7772):122–125

    Article  CAS  PubMed  Google Scholar 

  • Linzen B (1974) The Tryptophan→Ommochrome pathway in insects. Adv Insect Physiol 10:117–246

    Article  CAS  Google Scholar 

  • Liu C, Yamamoto K, Cheng TC, Kadono-Okuda K, Narukawa J, Liu SP, Han Y, Futahashi R, Kidokoro K, Noda H, Kobayashi I, Tamura T, Ohnuma A, Banno Y, Dai FY, Xiang ZH, Goldsmith MR, Mita K, Xia QY (2010) Repression of tyrosine hydroxylase is responsible for the sex-linked chocolate mutation of the silkworm, Bombyx mori. Proc Natl Acad Sci U S A 107(29):12980–12985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Lemonds TR, Popadić A (2014) The genetic control of aposematic black pigmentation in hemimetabolous insects: insights from Oncopeltus fasciatus. Evol Dev 16(5):270–277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Lemonds TR, Marden JH, Popadić A (2016) A pathway analysis of melanin patterning in a hemimetabolous insect. Genetics 203(1):403–413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu SH, Luo J, Yang BJ, Wang AY, Tang J (2019) karmoisin and cardinal ortholog genes participate in the ommochrome synthesis of Nilaparvata lugens (Hemiptera: Delphacidae). Insect Sci 26(1):35–43

    Article  CAS  PubMed  Google Scholar 

  • Lloyd V, Ramaswami M, Krämer H (1998) Not just pretty eyes: Drosophila eye-colour mutations and lysosomal delivery. Trends Cell Biol 8:257–259

    Article  CAS  PubMed  Google Scholar 

  • Lorenzen MD, Brown SJ, Denell RE, Beeman RW (2002) Cloning and characterization of the Tribolium castaneum eye-color genes encoding tryptophan oxygenase and kynurenine 3-monooxygenase. Genetics 160(1):225–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makino K, Satoh K, Koike M, Ueno N (1952) Sex in Pieris rapae L. and the pteridine content of their wings. Nature 170:933–934

    Article  CAS  PubMed  Google Scholar 

  • Maoka T, Kawase N, Ueda T, Nishida R (2020) Carotenoids of dragonflies, from the perspective of comparative biochemical and chemical ecological studies. Biochem Syst Ecol 89:104001

    Article  CAS  Google Scholar 

  • Martin A, Reed RD (2010) wingless and aristaless2 define a developmental ground plan for moth and butterfly wing pattern evolution. Mol Biol Evol 27:2864–2878

    Article  CAS  PubMed  Google Scholar 

  • Martin A, Reed RD (2014) Wnt signaling underlies evolution and development of the butterfly wing pattern symmetry systems. Dev Biol 395:367–378

    Article  CAS  PubMed  Google Scholar 

  • 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 U S A 109:12632–12637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Massey JH, Akiyama N, Bien T, Dreisewerd K, Wittkopp PJ, Yew JY, Takahashi A (2019a) Pleiotropic effects of ebony and tan on pigmentation and cuticular hydrocarbon composition in Drosophila melanogaster. Front Physiol 10:518

    Article  PubMed  PubMed Central  Google Scholar 

  • Massey JH, Chung D, Siwanowicz I, Stern DL, Wittkopp PJ (2019b) The yellow gene influences Drosophila male mating success through sex comb melanization. elife 8:e49388

    Article  PubMed  PubMed Central  Google Scholar 

  • Masuoka Y, Maekawa K (2016) Gene expression changes in the tyrosine metabolic pathway regulate caste-specific cuticular pigmentation of termites. Insect Biochem Mol Biol 74:21–31

    Article  CAS  PubMed  Google Scholar 

  • Matsuoka Y, Monteiro A (2018) Melanin pathway genes regulate color and morphology of butterfly wing scales. Cell Rep 24(1):56–65

    Article  CAS  PubMed  Google Scholar 

  • 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 U S A 114(40):10701–10706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McLean JR, Krishnakumar S, O'Donnell JM (1993) Multiple mRNAs from the Punch locus of Drosophila melanogaster encode isoforms of GTP cyclohydrolase I with distinct N-terminal domains. J Biol Chem 268(36):27191–27197

    Article  CAS  PubMed  Google Scholar 

  • Meng Y, Katsuma S, Mita K, Shimada T (2009a) Abnormal red body coloration of the silkworm, Bombyx mori, is caused by a mutation in a novel kynureninase. Genes Cells 14(2):129–140

    Article  CAS  PubMed  Google Scholar 

  • Meng Y, Katsuma S, Daimon T, Banno Y, Uchino K, Sezutsu H, Tamura T, Mita K, Shimada T (2009b) The silkworm mutant lemon (lemon lethal) is a potential insect model for human sepiapterin reductase deficiency. J Biol Chem 284(17):11698–11705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miura K, Shinoda T, Yura M, Nomura S, Kamiya K, Yuda M, Chinzei Y (1998) Two hexameric cyanoprotein subunits from an insect, Riptortus clavatus. Sequence, phylogeny and developmental and juvenile hormone regulation. Eur J Biochem 258(3):929–940

    Article  CAS  PubMed  Google Scholar 

  • Monteiro A, Prudic KL (2010) Multiple approaches to study color pattern evolution in butterflies. Trends Evol Biol 2:e2

    Article  Google Scholar 

  • Montell I, Rasmuson A, Rasmuson B, Holmgren P (1992) Uptake and incorporation in pteridines of externally supplied GTP in normal and pigment-deficient eyes of Drosophila melanogaster. Biochem Genet 30(1-2):61–75

    Article  CAS  PubMed  Google Scholar 

  • Moran NA, Jarvik T (2010) Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328(5978):624–627

    Article  CAS  PubMed  Google Scholar 

  • Mullins C, Hartnell LM, Bonifacino JS (2000) Distinct requirements for the AP-3 adaptor complex in pigment granule and synaptic vesicle biogenesis in Drosophila melanogaster. Mol Gen Genet 263(6):1003–1014

    Article  CAS  PubMed  Google Scholar 

  • Mun S, Noh MY, Kramer KJ, Muthukrishnan S, Arakane Y (2020) Gene functions in adult cuticle pigmentation of the yellow mealworm, Tenebrio molitor. Insect Biochem Mol Biol 117:103291

    Article  CAS  PubMed  Google Scholar 

  • 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, French-Constant RH, Llaurens V, Joron M, McMillan WO, Jiggins CD (2016) The gene cortex controls mimicry and crypsis in butterflies and moths. Nature 534(7605):106–110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakagoshi M, Masada M, Tsutsue M (1984) The nature of the seasonal colour dimorphism in the scorpion fly, Panorpa japonica Thunberg. Insect Biochem 14(6):615–618

    Article  CAS  Google Scholar 

  • Nakagoshi M, Kondo R, Sawada H, Takikawa S, Yoshida A (2002) Pteridines and pigment granules of wing scales concerned with sexual difference in wing’s capability reflecting near-UV rays in the Japanese cabbage butterfly Pieris rapae crucibora. In: Milstien S, Kapatos G, Levine RA, Shane B (eds) Chemistry and biology of pteridines and folates. Springer, Boston, pp 229–234

    Chapter  Google Scholar 

  • Nash D, Hu S, Leonard NJ, Tiong SY, Fillips D (1994) The raspberry locus of Drosophila melanogaster includes an inosine monophosphate dehydrogenase like coding sequence. Genome 37(2):333–244

    Article  CAS  PubMed  Google Scholar 

  • Navrotskaya V, Wnorowski A, Turski W, Oxenkrug G (2018) Effect of kynurenic acid on pupae viability of Drosophila melanogaster cinnabar and cardinal eye color mutants with altered tryptophan-kynurenine metabolism. Neurotox Res 34(2):324–331

    Article  CAS  PubMed  Google Scholar 

  • Nijhout HF (1997) Ommochrome pigmentation of the linea and rosa seasonal forms of Precis coenia (Lepidoptera: Nymphalidae). Arch Insect Biochem Physiol 36:215–222

    Article  CAS  Google Scholar 

  • Nikoh N, Tsuchida T, Maeda T, Yamaguchi K, Shigenobu S, Koga R, Fukatsu T (2018) Genomic insight into symbiosis-induced insect color change by a facultative bacterial endosymbiont, Candidatus Rickettsiella viridis. MBio 9(3):e00890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ninomiya Y, Tanaka K, Hayakawa Y (2006) Mechanisms of black and white stripe pattern formation in the cuticles of insect larvae. J Insect Physiol 52:638–645

    Article  CAS  PubMed  Google Scholar 

  • Nishide Y, Kageyama D, Hatakeyama M, Yokoi K, Jouraku A, Tanaka H, Koga R, Futahashi R, Fukatsu T (2020) Diversity and function of multicopper oxidase genes in the stinkbug Plautia stali. Sci Rep 10(1):3464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishikawa H, Iga M, Yamaguchi J, Saito K, Kataoka H, Suzuki Y, Sugano S, Fujiwara H (2013) Molecular basis of wing coloration in a Batesian mimic butterfly, Papilio polytes. Sci Rep 3:3184

    Article  PubMed  PubMed Central  Google Scholar 

  • 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(4):405–409

    Article  CAS  PubMed  Google Scholar 

  • Noh MY, Kramer KJ, Muthukrishnan S, Beeman RW, Kanost MR, Arakane Y (2015) Loss of function of the yellow-e gene causes dehydration-induced mortality of adult Tribolium castaneum. Dev Biol 399(2):315–324

    Article  CAS  PubMed  Google Scholar 

  • Noh MY, Koo B, Kramer KJ, Muthukrishnan S, Arakane Y (2016) Arylalkylamine N-acetyltransferase 1 gene (TcAANAT1) is required for cuticle morphology and pigmentation of the adult red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 79:119–129

    Article  CAS  PubMed  Google Scholar 

  • Noh MY, Kim SH, Gorman MJ, Kramer KJ, Muthukrishnan S, Arakane Y (2020) Yellow-g and yellow-g2 proteins are required for egg desiccation resistance and temporal pigmentation in the Asian tiger mosquito, Aedes albopictus. Insect Biochem Mol Biol 117:103386

    Article  CAS  Google Scholar 

  • Nováková E, Moran NA (2012) Diversification of genes for carotenoid biosynthesis in aphids following an ancient transfer from a fungus. Mol Biol Evol 29(1):313–323

    Article  PubMed  CAS  Google Scholar 

  • O’Donnell AF, Tiong S, Nash D, Clark DV (2000) The Drosophila melanogaster ade5 gene encodes a bifunctional enzyme for two steps in the de novo purine synthesis pathway. Genetics 154(3):1239–1253

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Hare K, Murphy C, Levis R, Rubin GM (1984) DNA sequence of the white locus of Drosophila melanogaster. J Mol Biol 180(3):437–455

    Article  PubMed  Google Scholar 

  • Okude G, Futahashi R (2021) Pigmentation and color pattern diversity in Odonata. Curr Opin Genet Dev 69:14–20

    Article  CAS  PubMed  Google Scholar 

  • Okude G, Futahashi R, Kawahara-Miki R, Yoshitake K, Yajima S, Fukatsu T (2017) Electroporation-mediated RNA interference reveals a role of multicopper oxidase 2 gene in dragonfly’s cuticular pigmentation. Appl Entomol Zool 52:379–387

    Article  CAS  Google Scholar 

  • Osanai-Futahashi M, Tatematsu K, Yamamoto K, Narukawa J, Uchino K, Kayukawa T, Shinoda T, Banno Y, Tamura T, Sezutsu H (2012a) Identification of the Bombyx red egg gene reveals involvement of a novel transporter family gene in late steps of the insect ommochrome biosynthesis pathway. J Biol Chem 287(21):17706–17714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osanai-Futahashi M, Ohde T, Hirata J, Uchino K, Futahashi R, Tamura T, Niimi T, Sezutsu H (2012b) A visible dominant marker for insect transgenesis. Nat Commun 3:1295

    Article  PubMed  CAS  Google Scholar 

  • Osanai-Futahashi M, Tatematsu KI, Futahashi R, Narukawa J, Takasu Y, Kayukawa T, Shinoda T, Ishige T, Yajima S, Tamura T, Yamamoto K, Sezutsu H (2016) Positional cloning of a Bombyx pink-eyed white egg locus reveals the major role of cardinal in ommochrome synthesis. Heredity 116(2):135–145

    Article  CAS  PubMed  Google Scholar 

  • Osorio D, Vorobyev M (2008) A review of the evolution of animal colour vision and visual communication signals. Vis Res 48:2042–2051

    Article  CAS  PubMed  Google Scholar 

  • Palmer DH, Kronforst MR (2019) A shared genetic basis of mimicry across swallowtail butterflies points to ancestral co-option of doublesex. Nat Commun 11(1):6

    Article  CAS  Google Scholar 

  • Panettieri S, Gjinaj E, John G, Lohman DJ (2018) Different ommochrome pigment mixtures enable sexually dimorphic Batesian mimicry in disjunct populations of the common palmfly butterfly, Elymnias hypermnestra. PLoS One 13(9):e0202465

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Park D, Park S, Yim J (2000) Molecular characterization of Drosophila melanogaster dihydropteridine reductase. Biochim Biophys Acta 1492(1):247–251

    Article  CAS  PubMed  Google Scholar 

  • Peng CL, Mazo-Vargas A, Brack BJ, Reed RD (2020) Multiple roles for laccase2 in butterfly wing pigmentation, scale development, and cuticle tanning. Evol Dev 22(4):336–341

    Article  CAS  PubMed  Google Scholar 

  • Prum RO, Cole JA, Torres RH (2004) Blue integumentary structural colours in dragonflies (Odonata) are not produced by incoherent Tyndall scattering. J Exp Biol 207:3999–4009

    Article  PubMed  Google Scholar 

  • Quan GX, Kim I, Kômoto N, Sezutsu H, Ote M, Shimada T, Kanda T, Mita K, Kobayashi M, Tamura T (2002) Characterization of the kynurenine 3-monooxygenase gene corresponding to the white egg 1 mutant in the silkworm Bombyx mori. Mol Gen Genomics 267(1):1–9

    Article  CAS  Google Scholar 

  • Reaume AG, Knecht DA, Chovnick A (1991) The rosy locus in Drosophila melanogaster: xanthine dehydrogenase and eye pigments. Genetics 129(4):1099–1109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rebeiz M, Pool JE, Kassner VA, Aquadro CF, Carroll SB (2009) Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 326(5960):1663–1667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reed RD, McMillan WO, Nagy LM (2008) Gene expression underlying adaptive variation in Heliconius wing patterns: non-modular regulation of overlapping cinnabar and vermilion prepatterns. Proc Biol Sci 275(1630):37–45

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Riddiford LM, Palli SR, Hiruma K, Li W, Green J, Hice RH, Wolfgang WJ, Webb BA (1990) Developmental expression, synthesis, and secretion of insecticyanin by the epidermis of the tobacco hornworm, Manduca sexta. Arch Insect Biochem Physiol 14(3):171–190

    Article  CAS  PubMed  Google Scholar 

  • Riedel F, Vorkel D, Eaton S (2011) Megalin-dependent yellow endocytosis restricts melanization in the Drosophila cuticle. Development 138(1):149–158

    Article  CAS  PubMed  Google Scholar 

  • Saenko SV, Brakefield PM, Beldade P (2010) Single locus affects embryonic segment polarity and multiple aspects of an adult evolutionary novelty. BMC Biol 8:111

    Article  PubMed  PubMed Central  Google Scholar 

  • Sakudoh T, Tsuchida K, Kataoka H (2005) BmStart1, a novel carotenoid-binding protein isoform from Bombyx mori, is orthologous to MLN64, a mammalian cholesterol transporter. Biochem Biophys Res Commun 336(4):1125–1135

    Article  CAS  PubMed  Google Scholar 

  • Sakudoh T, Sezutsu H, Nakashima T, Kobayashi I, Fujimoto H, Uchino K, Banno Y, Iwano H, Maekawa H, Tamura T, Kataoka H, Tsuchida K (2007) Carotenoid silk coloration is controlled by a carotenoid-binding protein, a product of the Yellow blood gene. Proc Natl Acad Sci U S A 104(21):8941–8946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakudoh T, Iizuka T, Narukawa J, Sezutsu H, Kobayashi I, Kuwazaki S, Banno Y, Kitamura A, Sugiyama H, Takada N, Fujimoto H, Kadono-Okuda K, Mita K, Tamura T, Yamamoto K, Tsuchida K (2010) A CD36-related transmembrane protein is coordinated with an intracellular lipid-binding protein in selective carotenoid transport for cocoon coloration. J Biol Chem 285(10):7739–7751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakudoh T, Kuwazaki S, Iizuka T, Narukawa J, Yamamoto K, Uchino K, Sezutsu H, Banno Y, Tsuchida K (2013) CD36 homolog divergence is responsible for the selectivity of carotenoid species migration to the silk gland of the silkworm Bombyx mori. J Lipid Res 54(2):482–495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santoro P, Parisi G (1986) A new enzyme from Drosophila melanogaster: in vitro conversion of xanthommatin into its dihydroform by means of xanthommatin reductase. J Exp Zool 239:169–173

    Article  CAS  Google Scholar 

  • Sawada H, Nakagoshi M, Reinhardt RK, Ziegler I, Koch PB (2002) Hormonal control of GTP cyclohydrolase I gene expression and enzyme activity during color pattern development in wings of Precis coenia. Insect Biochem Mol Biol 32(6):609–615

    Article  CAS  PubMed  Google Scholar 

  • Schmidt FS, Skerra A (1994) The bilin-binding protein of Pieris brassicae. cDNA sequence and regulation of expression reveal distinct features of this insect pigment protein. Eur J Biochem 219(3):855–863

    Article  CAS  PubMed  Google Scholar 

  • Schopf R, Mignat C, Hedden P (1982) As to the food quality of spruce needles for forest damaging insects. 18. Resorption of secondary plant metabolites by the sawfly Gilpinia hercyniae Htg (Hym., Diprionidae). Z Angew Entomol 93:244–257

    Article  CAS  Google Scholar 

  • Searles LL, Ruth RS, Pret AM, Fridell RA, Ali AJ (1990) Structure and transcription of the Drosophila melanogaster vermilion gene and several mutant alleles. Mol Cell Biol 10(4):1423–1431

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shirataki H, Futahashi R, Fujiwara H (2010) Species-specific coordinated gene expression and trans-regulation of larval color pattern in three swallowtail butterflies. Evol Dev 12(3):305–314

    Article  CAS  PubMed  Google Scholar 

  • Sloan DB, Moran NA (2012) Endosymbiotic bacteria as a source of carotenoids in whiteflies. Biol Lett 8(6):986–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spana EP, Abrams AB, Ellis KT, Klein JC, Ruderman BT, Shi AH, Zhu D, Stewart A, May S (2020) Speck, first identified in Drosophila melanogaster in 1910, is encoded by the Arylalkalamine N-Acetyltransferase (AANAT1) gene. G3 10(9):3387–3398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stavenga DG, Leertouwer HL, Wilts BD (2014) The colouration toolkit of the pipevine swallowtail butterfly, Battus philenor: thin films, papiliochromes, and melanin. J Comp Phys A 200:547–561

    Article  CAS  Google Scholar 

  • Sugahara R, Tanaka S (2019) Yellowing and YPT gene expression in the desert locust, Schistocerca gregaria: effects of developmental stages and fasting. Arch Insect Biochem Physiol 101(2):e21551

    Article  PubMed  CAS  Google Scholar 

  • Sugahara R, Tsuchiya W, Yamazaki T, Tanaka S, Shiotsuki T (2020) Recombinant yellow protein of the takeout family and albino-related takeout protein specifically bind to lutein in the desert locust. Biochem Biophys Res Commun 522(4):876–880

    Article  CAS  PubMed  Google Scholar 

  • Sugumaran M (2002) Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects. Pigment Cell Res 15(1):2–9

    Article  CAS  PubMed  Google Scholar 

  • Takahashi A, Takano-Shimizu T (2011) Divergent enhancer haplotype of ebony on inversion In(3R)Payne associated with pigmentation variation in a tropical population of Drosophila melanogaster. Mol Ecol 20(20):4277–4287

    Article  CAS  PubMed  Google Scholar 

  • Takahashi A, Takahashi K, Ueda R, Takano-Shimizu T (2007) Natural variation of ebony gene controlling thoracic pigmentation in Drosophila melanogaster. Genetics 177(2):1233–1237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tatematsu K, Yamamoto K, Uchino K, Narukawa J, Iizuka T, Banno Y, Katsuma S, Shimada T, Tamura T, Sezutsu H, Daimon T (2011) Positional cloning of silkworm white egg 2 (w-2) locus shows functional conservation and diversification of ABC transporters for pigmentation in insects. Genes Cells 16(4):331–342

    Article  CAS  PubMed  Google Scholar 

  • Tearle RG, Belote JM, McKeown M, Baker BS, Howells AJ (1989) Cloning and characterization of the scarlet gene of Drosophila melanogaster. Genetics 122(3):595–606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian L, Rahman SR, Ezray BD, Franzini L, Strange JP, Lhomme P, Hines HM (2019) A homeotic shift late in development drives mimetic color variation in a bumble bee. Proc Natl Acad Sci U S A 116(24):11857–11865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tillyard RJ (1917) The biology of dragonflies. Cambridge University Press, Cambridge

    Google Scholar 

  • Timmermans MJ, Baxter SW, Clark R, Heckel DG, Vogel H, Collins S, Papanicolaou A, Fukova I, Joron M, Thompson MJ, Jiggins CD, French-Constant RH, Vogler AP (2014) Comparative genomics of the mimicry switch in Papilio dardanus. Proc Biol Sci 281(1787):20140465

    PubMed  PubMed Central  Google Scholar 

  • Tomoda A, Yoneyama Y, Yamaguchi T, Shirao E, Kawasaki K (1990) Mechanism of coloration of human lenses induced by near-ultraviolet-photo-oxidized 3-hydroxykynurenine. Ophthalmic Res 22(3):152–159

    Article  CAS  PubMed  Google Scholar 

  • True JR, Edwards KA, Yamamoto D, Carroll SB (1999) Drosophila wing melanin patterns form by vein-dependent elaboration of enzymatic prepatterns. Curr Biol 9(23):1382–1391

    Article  CAS  PubMed  Google Scholar 

  • True JR, Yeh SD, Hovemann BT, Kemme T, Meinertzhagen IA, Edwards TN, Liou SR, Han Q, Li J (2005) Drosophila tan encodes a novel hydrolase required in pigmentation and vision. PLoS Genet 1(5):e63

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tsuchida T (2016) Molecular basis and ecological relevance of aphid body colors. Curr Opin Insect Sci 17:74–80

    Article  PubMed  Google Scholar 

  • Tsuchida T, Koga R, Horikawa M, Tsunoda T, Maoka T, Matsumoto S, Simon JC, Fukatsu T (2010) Symbiotic bacterium modifies aphid body color. Science 330(6007):1102–1104

    Article  CAS  PubMed  Google Scholar 

  • Tsujita M, Sakurai S (1965) Purification of the three specific soluble chromoproteins from chromogranules in hypodermal cells of the silkworm larva. Proc Jpn Acad 41:225–229

    Article  CAS  Google Scholar 

  • Umbers KD, Fabricant SA, Gawryszewski FM, Seago AE, Herberstein ME (2014) Reversible colour change in Arthropoda. Biol Rev 89(4):820–848

    Article  PubMed  Google Scholar 

  • Umebachi Y (1985) Papiliochrome, a new pigment group of butterfly. Zool Sci 2:163–174

    CAS  Google Scholar 

  • Umebachi Y (2000) The pigment of animals. Uchida-Rohkakuho, Tokyo

    Google Scholar 

  • 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(3):52

    Article  PubMed  Google Scholar 

  • van der Burg KRL, Lewis JJ, Brack BJ, Fandino RA, Mazo-Vargas A, Reed RD (2020) Genomic architecture of a genetically assimilated seasonal color pattern. Science 370(6517):721–725

    Article  PubMed  CAS  Google Scholar 

  • 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(7605):102–105

    Article  CAS  Google Scholar 

  • Vargas-Lowman A, Armisen D, Burguez Floriano CF, da Rocha Silva Cordeiro I, Viala S, Bouchet M, Bernard M, Le Bouquin A, Santos ME, Berlioz-Barbier A, Salvador A, Figueiredo Moreira FF, Bonneton F, Khila A (2019) Cooption of the pteridine biosynthesis pathway underlies the diversification of embryonic colors in water striders. Proc Natl Acad Sci U S A 116(38):19046–19054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Veron JE, O’Farrell AF, Dixon B (1974) The fine structure of Odonata chromatophores. Tissue Cell 6(4):613–626

    Article  CAS  PubMed  Google Scholar 

  • Vigneron A, Masson F, Vallier A, Balmand S, Rey M, Vincent-Monégat C, Aksoy E, Aubailly-Giraud E, Zaidman-Rémy A, Heddi A (2014) Insects recycle endosymbionts when the benefit is over. Curr Biol 24:2267–2273

    Article  CAS  PubMed  Google Scholar 

  • Walter MF, Black BC, Afshar G, Kermabon AY, Wright TR, Biessmann H (1991) Temporal and spatial expression of the yellow gene in correlation with cuticle formation and dopa decarboxylase activity in Drosophila development. Dev Biol 147:32–45

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Zhao C, Bai L, Deng X, Wu C (2008) Reduction of drosopterin content caused by a 45-nt insertion in Henna pre-mRNA of Drosophila melanogaster. Sci China Life Sci 51(8):702–710

    Article  CAS  Google Scholar 

  • Wang L, Kiuchi T, Fujii T, Daimon T, Li M, Banno Y, Katsuma S, Shimada T (2013a) Reduced expression of the dysbindin-like gene in the Bombyx mori ov mutant exhibiting mottled translucency of the larval skin. Genome 56(2):101–108

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Kiuchi T, Fujii T, Daimon T, Li M, Banno Y, Kikuta S, Kikawada T, Katsuma S, Shimada T (2013b) Mutation of a novel ABC transporter gene is responsible for the failure to incorporate uric acid in the epidermis of ok mutants of the silkworm, Bombyx mori. Insect Biochem Mol Biol 43(7):562–571

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Yin Y, Wang K, Cao J, Cheng T, Liu C, Zhang Y, Zhu Y (2020) Bombyx mori monocarboxylate transporter 9 (BmMCT9) is involved in the transport of uric acid in silkworm integument. Genes Cells 25(1):33–40

    Article  CAS  PubMed  Google Scholar 

  • Warren WD, Palmer S, Howells AJ (1996) Molecular characterization of the cinnabar region of Drosophila melanogaster: identification of the cinnabar transcription unit. Genetica 98(3):249–262

    Article  CAS  PubMed  Google Scholar 

  • Watt WB (1964) Pteridine components of wing pigmentation in the butterfly Colias eurytheme. Nature 201:1326–1327

    Article  CAS  PubMed  Google Scholar 

  • Watt WB (1973) Adaptive significance of pigment polymorphisms in Colias butterflies. III. Progress in the study of the ‘alba’ variant. Evolution 27:537–548

    PubMed  Google Scholar 

  • Werner T, Koshikawa S, Williams TM, Carroll SB (2010) Generation of a novel wing colour pattern by the Wingless morphogen. Nature 464(7292):1143–1148

    Article  CAS  PubMed  Google Scholar 

  • Westerman EL, VanKuren NW, Massardo D, Tenger-Trolander A, Zhang W, Hill RI, Perry M, Bayala E, Barr K, Chamberlain N, Douglas TE, Buerkle N, Palmer SE, Kronforst MR (2018) Aristaless controls butterfly wing color variation used in mimicry and mate choice. Curr Biol 28(21):3469–3474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams RA, Mamotte CD, Burnett JR (2008) Phenylketonuria: an inborn error of phenylalanine metabolism. Clin Biochem Rev 29(1):31–41

    PubMed  PubMed Central  Google Scholar 

  • Wilson A (1986) Flavonoid pigments and wing color in Melanargia galathea. J Chem Ecol 12(1):49–68

    Article  CAS  PubMed  Google Scholar 

  • Wilson A (1987) Flavonoid pigments in chalkhill blue (Lysandra coridon Poda) and other lycaenid butterflies. J Chem Ecol 13(3):473–493

    Article  CAS  PubMed  Google Scholar 

  • Wilts BD, Matsushita A, Arikawa K, Stavenga DG (2015) Spectrally tuned structural and pigmentary coloration of birdwing butterfly wing scales. J R Soc Interface 12:20150717

    Article  PubMed  PubMed Central  Google Scholar 

  • Wittkopp PJ, True JR, Carroll SB (2002a) Reciprocal functions of the Drosophila Yellow and Ebony proteins in the development and evolution of pigment patterns. Development 129:1849–1858

    Article  CAS  PubMed  Google Scholar 

  • Wittkopp PJ, Vaccaro K, Carroll SB (2002b) Evolution of yellow gene regulation and pigmentation in Drosophila. Curr Biol 12(18):1547–1556

    Article  CAS  PubMed  Google Scholar 

  • Wittkopp PJ, Williams BL, Selegue JE, Carroll SB (2003) Drosophila pigmentation evolution: divergent genotypes underlying convergent phenotypes. Proc Natl Acad Sci U S A 100(4):1808–1813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wittkopp PJ, Stewart EE, Arnold LL, Neidert AH, Haerum BK, Thompson EM, Akhras S, Smith-Winberry G, Shefner L (2009) Intraspecific polymorphism to interspecific divergence: genetics of pigmentation in Drosophila. Science 326(5952):540–544

    Article  CAS  PubMed  Google Scholar 

  • Woronik A, Tunström K, Perry MW, Neethiraj R, Stefanescu C, Celorio-Mancera MP, Brattström O, Hill J, Lehmann P, Käkelä R, Wheat CW (2019) A transposable element insertion is associated with an alternative life history strategy. Nat Commun 10(1):5757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wright TRF (1987) The genetics of biogenic amine metabolism, sclerotization, and melanization in Drosophila melanogaster. Adv Genet 24:127–222

    Article  CAS  PubMed  Google Scholar 

  • Xiao D, Chen X, Tian R, Wu M, Zhang F, Zang L, Harwood JD, Wang S (2020) Molecular and potential regulatory mechanisms of melanin synthesis in Harmonia axyridis. Int J Mol Sci 21(6):E2088

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Yang M, Wang Y, Liu Q, Liu Z, Jiang F, Wang H, Guo X, Zhang J, Kang L (2019) A β-carotene-binding protein carrying a red pigment regulates body-color transition between green and black in locusts. elife 8:e41362

    Article  PubMed  PubMed Central  Google Scholar 

  • Yassin A, Bastide H, Chung H, Veuille M, David JR, Pool JE (2016a) Ancient balancing selection at tan underlies female colour dimorphism in Drosophila erecta. Nat Commun 7:10400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yassin A, Delaney EK, Reddiex AJ, Seher TD, Bastide H, Appleton NC, Lack JB, David JR, Chenoweth SF, Pool JE, Kopp A (2016b) The pdm3 locus is a hotspot for recurrent evolution of female-limited color dimorphism in Drosophila. Curr Biol 26(18):2412–2422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoda S, Yamaguchi J, Mita K, Yamamoto K, Banno Y, Ando T, Daimon T, Fujiwara H (2014) The transcription factor Apontic-like controls diverse colouration pattern in caterpillars. Nat Commun 5:4936

    Article  CAS  PubMed  Google Scholar 

  • Yoda S, Otaguro E, Nobuta M, Fujiwara H (2020) Molecular mechanisms underlying pupal protective color switch in Papilio polytes butterflies. Front Ecol Evol 8:51

    Article  Google Scholar 

  • Yoshioka S, Kinoshita S (2006) Structural or pigmentary? Origin of the distinctive white stripe on the blue wing of a Morpho butterfly. Proc Biol Sci 273(1583):129–134

    PubMed  Google Scholar 

  • Yuasa M, Kiuchi T, Banno Y, Katsuma S, Shimada T (2016) Identification of the silkworm quail gene reveals a crucial role of a receptor guanylyl cyclase in larval pigmentation. Insect Biochem Mol Biol 68:33–40

    Article  CAS  PubMed  Google Scholar 

  • Zhan S, Guo Q, Li M, Li M, Li J, Miao X, Huang Y (2010) Disruption of an N-acetyltransferase gene in the silkworm reveals a novel role in pigmentation. Development 137(23):4083–4090

    Article  CAS  PubMed  Google Scholar 

  • Zhan S, Zhang W, Niitepõld K, Hsu J, Haeger JF, Zalucki MP, Altizer S, de Roode JC, Reppert SM, Kronforst MR (2014) The genetics of monarch butterfly migration and warning colouration. Nature 514(7522):317–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Reed RD (2016) Genome editing in butterflies reveals that spalt promotes and Distal-less represses eyespot colour patterns. Nat Commun 7:11769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Martin A, Perry MW, van der Burg KR, Matsuoka Y, Monteiro A, Reed RD (2017a) Genetic basis of melanin pigmentation in butterfly wings. Genetics 205(4):1537–1550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Mazo-Vargas A, Reed RD (2017b) Single master regulatory gene coordinates the evolution and development of butterfly color and iridescence. Proc Natl Acad Sci U S A 114(40):10707–10712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Kiuchi T, Wang L, Kawamoto M, Suzuki Y, Sugano S, Banno Y, Katsuma S, Shimada T (2017c) Bm-muted, orthologous to mouse muted and encoding a subunit of the BLOC-1 complex, is responsible for the otm translucent mutation of the silkworm Bombyx mori. Gene 629:92–100

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Kiuchi T, Hirayama C, Katsuma S, Shimada T (2018) Bombyx ortholog of the Drosophila eye color gene brown controls riboflavin transport in Malpighian tubules. Insect Biochem Mol Biol 92:65–72

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Li H, Du J, Zhang J, Shen J, Cai W (2019a) Three melanin pathway genes, TH, yellow, and aaNAT, regulate pigmentation in the twin-spotted assassin bug, Platymeris biguttatus (Linnaeus). Int J Mol Sci 20(11):E2728

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Wang XX, Feng ZJ, Cong HS, Chen ZS, Li YD, Yang WM, Zhang SQ, Shen LF, Tian HG, Feng Y, Liu TX (2019b) Superficially similar adaptation within one species exhibits similar morphological specialization but different physiological regulations and origins. Front Cell Dev Biol 8:300

    Article  Google Scholar 

  • Zhao Y, Zhang H, Li Z, Duan J, Jiang J, Wang Y, Zhan S, Akinkurolere RO, Xu A, Qian H, Miao X, Tan A, Huang Y (2012) A major facilitator superfamily protein participates in the reddish brown pigmentation in Bombyx mori. J Insect Physiol 58(11):1397–1405

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Kohji Tanaka for photo of gynandromorphic dragonfly, Genta Okude for helpful comments of the manuscript. The writing was partly supported by JSPS KAKENHI (JP18H02491 and JP20H04936).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ryo Futahashi .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Futahashi, R., Osanai-Futahashi, M. (2021). Pigments 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_1

Download citation

Publish with us

Policies and ethics