Abstract
Various organisms have color patterns on their body surfaces, and these color patterns are thought to contribute to physiological regulation, communication with conspecifics, and signaling with the environment. An adult fly of Drosophila guttifera (Insecta: Diptera: Drosophilidae) has melanin pigmentation patterns on its body and wings. Though D. guttifera has been used for research into color pattern formation, how its pupal development proceeds and when the pigmentation starts have not been well studied. In this study, we defined the pupal stages of D. guttifera and measured the pigment content of wing spots from the pupal period to the period after eclosion. Using a transgenic line which carries eGFP connected with an enhancer of yellow, a gene necessary for melanin synthesis, we analyzed the timing at which the yellow enhancer starts to drive eGFP. We also analyzed the distribution of Yellow-producing cells, as indicated by the expression of eGFP during pupal and young adult periods. The results suggested that Yellow-producing cells were removed from wings within 3 h after eclosion, and wing pigmentation continued without epithelial cells. Furthermore, the results of vein cutting experiments showed that the transport of melanin precursors through veins was necessary for wing pigmentation. These results showed the importance of melanin precursors transported through veins and of extracellular factors which were secreted from epithelial cells and left in the cuticle.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
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. doi:10.1126/science.1233749
Bainbridge SP, Bownes M (1981) Staging the metamorphosis of Drosophila melanogaster. J Embryol Exp Morphol 66:57–80
Biessmann H (1985) Molecular analysis of the yellow gene (y) region of Drosophila melanogaster. Proc Natl Acad Sci U S A 82:7369–7373
Cott HB (1940) Adaptive coloration in animals. Methuen, London
DeLean A, Munson PJ, Rodbard D (1978) Simultaneous analysis of families of sigmoidal curves: application to bioassay, radioligand assay, and physiological dose-response curves. Am J Phys 235:E97–102
Gibert J-M, Peronnet F, Schlötterer C (2007) Phenotypic plasticity in Drosophila pigmentation caused by temperature sensitivity of a chromatin regulator network. PLoS Genet 3:e30. doi:10.1371/journal.pgen.0030030
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. doi:10.1038/nature03235
Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, Cambridge
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. doi:10.1042/BJ20020272
Hirsh J, Davidson N (1981) Isolation and characterization of the dopa decarboxylase gene of Drosophila melanogaster. Mol Cell Biol 1:475–485. doi:10.1128/MCB.1.6.475
Hiruma K, Riddiford LM, Hopkins TL, Morgan TD (1985) Roles of dopa decarboxylase and phenoloxidase in the melanization of the tobacco hornworm and their control by 20-hydroxyecdysone. J Comp Physiol B 155:659–669. doi:10.1007/BF00694579
Hopkins TL, Kramer KJ (1992) Insect cuticle sclerotization. Annu Rev Entomol 37:273–302. doi:10.1146/annurev.en.37.010192.001421
Johnson SA, Milner MJ (1987) The final stages of wing development in Drosophila melanogaster. Tissue Cell 19:505–513. doi:10.1016/0040-8166(87)90044-9
Kimura K, Kodama A, Hayashi Y, Ohta T (2004) Activation of the cAMP/PKA signaling pathway is required for post-ecdysial cell death in wing epidermal cells of Drosophila melanogaster. Development 131:1597–1606. doi:10.1242/dev.01049
Kopp A (2009) Metamodels and phylogenetic replication: a systematic approach to the evolution of developmental pathways. Evolution 63:2771–2789. doi:10.1111/j.1558-5646.2009.00761.x
Kopp A (2011) Drosophila sex comb as a model of evolutionary innovations. Evol Dev 13:504–522. doi:10.1111/j.1525-142X.2011.00507.x
Koshikawa S (2015) Enhancer modularity and the evolution of new traits. Fly 9:155–159. doi:10.1080/19336934.2016.1151129
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 112:7524–7529. doi:10.1073/pnas.1509022112
Koshikawa S, Fukutomi Y, Matsumoto K (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: an integrative approach. Springer, New York in press
Kramer KJ, Hopkins TL (1987) Tyrosine metabolism for insect cuticle tanning. Arch Insect Biochem Physiol 6:279–301. doi:10.1002/arch.940060406
Kronforst MR, Barsh GS, Kopp A, Mallet J, Monteiro A, Mullen SP, Protas M, Rosenblum EB, Schneider CJ, Hoekstra HE (2012) Unraveling the thread of nature’s tapestry: the genetics of diversity and convergence in animal pigmentation. Pigment Cell Melanoma Res 25(4):411–433. doi:10.1111/j.1755-148X.2012.01014.x
Lees AD (1942) Homology of the campaniform organs on the wing of Drosophila melanogaster. Nature 150:375–375. doi:10.1038/150375a0
Link N, Chen P, Lu WJ, Pogue K, Chuong A, Mata M, Checketts J, Abrams JM (2007) A collective form of cell death requires homeodomain interacting protein kinase. J Cell Biol 178:567–574. doi:10.1083/jcb.200702125
Massey JH, Wittkopp PJ (2016) The genetic basis of pigmentation differences within and between Drosophila species. Curr Top Dev Biol 119:27–61. doi:10.1016/bs.ctdb.2016.03.004
Mills MG, Patterson LB (2009) Not just black and white: pigment pattern development and evolution in vertebrates. Semin Cell Dev Biol 20:72–81. doi:10.1016/j.semcdb.2008.11.012
Neckameyer WS, White K (1993) Drosophila tyrosine hydroxylase is encoded by the pale locus. J Neurogenet 8:189–199. doi:10.3109/01677069309083448
Nijhout HF (1985) The developmental physiology of color patterns in Lepidoptera. Adv Insect Physiol 18:181–247. doi:10.1016/S0065-2806(08)60041-7
Pass G (2000) Accessory pulsatile organs: evolutionary innovation in insects. Annu Rev Entomol 45:495–518. doi:10.1146/annurev.ento.45.1.495
Perttunen V (1955) The blood circulation and the accessory pulsatile organs in the wings of Drosophila funebris and D. melanogaster (Dipt., Drosophilidae). Ann Entomol Fennici 21:78–88
Riedel RF, Vorkel D, Eaton S (2011) Megalin-dependent yellow endocytosis restricts melanization in the Drosophila cuticle. Development 138:149–158. doi:10.1242/dev.056309
Riley PA (1997) Melanin. Int J Biochem Cell Biol 29:1235–1239. doi:10.1016/S1357-2725(97)00013-7
Robertson CW (1936) The metamorphosis of Drosophila melanogaster, including an accurately timed account of the principal morphological changes. J Morphol 59:351–399. doi:10.1002/jmor.1050590207
Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, Oxford
Sugumaran M (2002) Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects. Pigment Cell Res 15:2–9. doi:10.1034/j.1600-0749.2002.00056.x
Tadokoro R, Murai H, Sakai KI, Okui T, Yokota Y, Takahashi Y (2016) Melanosome transfer to keratinocyte in the chicken embryonic skin is mediated by vesicle release associated with Rho-regulated membrane blebbing. Sci Rep 6:38277. doi:10.1038/srep38277
Tögel M, Pass G, Paululat A (2008) The Drosophila wing hearts originate from pericardial cells and are essential for wing maturation. Dev Biol 318:29–37. doi:10.1016/j.ydbio.2008.02.043
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. doi:10.1016/S0960-9822(00)80083-4
Walter MF, Zeineh LL, Black BC, McIvor WE, Wright TR, Biessmann H (1996) Catecholamine metabolism and in vitro induction of premature cuticle melanization in wild type and pigmentation mutants of Drosophila melanogaster. Arch Insect Biochem Physiol 31:219–233. doi:10.1002/(SICI)1520-6327(1996)31:2<219::AID-ARCH9>3.0.CO;2-U
Werner T, Koshikawa S, Williams TM, Carroll SB (2010) Generation of a novel wing colour pattern by the Wingless morphogen. Nature 464:1143–1148. doi:10.1038/nature08896
Wittkopp PJ, Beldade P (2009) Development and evolution of insect pigmentation: genetic mechanisms and the potential consequences of pleiotropy. Sem Cell Dev Biol 20:65–71. doi:10.1016/j.semcdb.2008.10.002
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. doi:10.1016/S0168-9525(03)00194-X
Wright TRF (1987) The genetics of biogenic amine metabolism, sclerotization, and melanization in Drosophila melanogaster. Adv Genet 24:127–222. doi:10.1016/S0065-2660(08)60008-5
Acknowledgements
We thank Sean B. Carroll and Thomas Werner for providing fly stocks; Victoria A. Kassner, Mayumi Futamata, Tadao Usui, and Masayoshi Watada for establishing the rearing system of D. guttifera; Tsuyoshi Katahata and Machiko Teramoto for fly stock maintenance; Tadashi Uemura, Naoyuki Fuse, Takeshi Inoue, and Norito Shibata for their scientific advice; and Elizabeth Nakajima for English editing. This work was supported by KAKENHI 15K18586, The Sumitomo Foundation, and The Narishige Zoological Science Award.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Claude Desplan
Electronic supplementary material
ESM 1
(PDF 278 kb)
Rights and permissions
About this article
Cite this article
Fukutomi, Y., Matsumoto, K., Agata, K. et al. Pupal development and pigmentation process of a polka-dotted fruit fly, Drosophila guttifera (Insecta, Diptera). Dev Genes Evol 227, 171–180 (2017). https://doi.org/10.1007/s00427-017-0578-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00427-017-0578-3