Live cell imaging of butterfly pupal and larval wings in vivo

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Ohno, Yoshikazu ^a   Otaki, Joji M ^a  

^a UNIVERSITY OF THE RYUKYUS   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BUTTERFLY; CELL DIFFERENTIATION; CELL DIVISION; CELL SURFACE; CUTICLE; ENDOPLASMIC RETICULUM; EPITHELIUM CELL; FEMALE; FLUORESCENCE IMAGING; FORELIMB; IN VIVO STUDY; JUNONIA ORITHYA; LARVAL STAGE; MITOCHONDRION; NONHUMAN; POLYPLOIDY; PUPA; ZIZEERIA MAHA; ANIMAL; COLOR; CYTOLOGY; GENETICS; LARVA; PIGMENTATION; WING;

ANIMALS; BUTTERFLIES; CELL DIFFERENTIATION; COLOR; LARVA; PIGMENTATION; PUPA; WINGS, ANIMAL;

EID: 84939195494     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128332     Document Type: Article

References (56)

1. Nijhout HF (1991) The development and evolution of butterfly wing patterns. Washington: Smithsonian Institution Press. 297 p.
2. Ghiradella H (1998) Hairs, bristles and scales. In: Harrison FW, Locke M, editors. Microscopic anatomy of invertebrates, Volume 11: Insecta. New York: John Wiley & Sons. pp. 257-287.
3. Kristensen NP, Simonsen TJ (2003) Hairs and scales. In: Kristensen NP, editor. Lepidoptera, moths and butterflies: morphology, physiology, and development. Handbook of zoology, Volume IV, Anthropoda: Insecta. Berlin: Walter de Gruyter. pp. 9-22.
4. Iwata M, Ohno Y, Otaki JM (2014) Real-time in vivo imaging of butterfly wing development: revealing the cellular dynamics of the pupal wing tissue. PLoS ONE 9: e89500. doi: 10.1371/journal.pone.0089500 PMID: 24586829
5. Henke K (1946) Über die verschiedenen Zellteilungsvorgange in der Entwicklung des beschuppten Flügelepithels der Mehlmotte Ephestia kühniella Z. Biologisches Zentralblatt 65: 120-135. (In German) PMID: 20249535
6. Henke K, Pohley H-J (1952) Differentielle Zellteilungen und Polyploedie bei der Schuppenbildung der Mehlmotte Ephestia kühniella. Z Naturforsch Abt B 7: 65-79. (In German)
7. Cho EH, Nijhout HF (2012) Development of polyploidy of scale-building cells in the wings of Manduca sexta. Arthropod Struct Dev 42, 37-46. doi: 10.1016/j.asd.2012.09.003 PMID: 23017249
8. Kuntze H (1935) Die Flügelentwicklung bei Philosamia cynthia Drury, mit besonderer Berücksichtigung des Geäders der Lakunen und der Tracheensysteme. Z Morphol Ökol Tiere 30: 544-572. (In German)
9. Kühn A (1954) Vorlesungen unber Entwicklungsphysiologie. Berlin: Springer-Verlag. (In German)
10. Greenstein ME (1972) The ultrastructure of developing wings in the giant silkmoth, Hyalophora cecropia. II. Scale-forming and socket-forming cells. J Morphol 136: 23-52. PMID: 5009131
11. Yoshida A, Shinkawa T, Aoki K (1983) Periodical arrangement on lepidopteran (butterfly and moth) wings. Proc Jpn Acad 59B: 236-239.
12. Yoshida A, Aoki K (1989) Scale arrangement pattern in a lepidopteran wing. 1. Periodic cellular pattern in the pupal wing of Pieris rapae. Dev Growth Differ 31: 601-609.
13. Nijhout HF (2001) Elements of butterfly wing patterns. J Exp Zool 291: 213-225. PMID: 11598911
14. Otaki JM (2012) Color pattern analysis of nymphalid butterfly wings: Revision of the nymphalid groundplan. Zool Sci 29: 568-576. doi: 10.2108/zsj.29.568 PMID: 22943780
15. Taira W, Kinjo S, Otaki JM (2015) The marginal band system in nymphalid butterfly wings. Zool Sci 32:38-46. doi: 10.2108/zs140058 PMID: 25660695
16. Tokita CK, Oliver JC, Monteiro A (2013) A survey of eyespot sexual dimorphism across nymphalid butterflies. Int J Evol Biol 2013: 926702. doi: 10.1155/2013/926702 PMID: 24381783
17. Kodandaramaiah U, Lindenfors P, Tullberg BS (2013) Deflective and intimidating eyespots: a comparative study of eyespot size and position in Junonia butterflies. Ecol Evol 3: 4518-4524. doi: 10.1002/ece3.831 PMID: 24340191
18. Nijhout HF (1980) Ontogeny of the color pattern on the wings of Precis coenia. Dev Biol 80: 275-288. PMID: 7192661
19. Nijhout HF (1980) Pattern formation on lepidopteran wings: determination of an eyespot. Dev Biol 80: 267-274. PMID: 7004953
20. Nijhout HF (1985) Cautery-induced colour patterns in Precis coenia (Lepidoptera: Nymphalidae). J Embryol Exp Morphol 86: 191-203. PMID: 4031740
21. French V, Brakefield PM (1992) The development of eyespot patterns on butterfly wings: morphogen sources or sinks? Development 116: 103-109.
22. Brakefield PM, French V (1995) Eyespot development on butterfly wings: the epidermal response to damage. Dev Biol 168: 98-111. PMID: 7883082
23. 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. doi: 10.1186/1741-7007-8-111 PMID: 20796293
24. Otaki JM, Ogasawara T, Yamamoto H (2005) Tungstate-induced color-pattern modifications of butterfly wings are independent of stress response and ecdysteroid effect. Zool Sci 22: 635-644. PMID: 15988157
25. Mahdi SH, Gima S, Tomita Y, Yamasaki H, Otaki JM (2010) Physiological characterization of the cold-shock-induced humoral factor for wing color-pattern changes in butterflies. J Insect Physiol 56: 1022-1031. doi: 10.1016/j.jinsphys.2010.02.013 PMID: 20206631
26. Dhungel B, Otaki JM (2013) Larval temperature experience determines sensitivity to cold-shock-induced wing color pattern changes in the blue pansy butterfly Junonia orithya. J Thermal Biol 38: 427-433.
27. Otaki JM (2007) Reversed type of color-pattern modifications of butterfly wings: a physiological mechanism of wing-wide color-pattern determination. J Insect Physiol 53: 526-537. PMID: 17400241
28. Otaki JM (2011) Artificially induced colour-pattern changes in butterflies: dynamic signal interactions. Sci Rep 1: 111. doi: 10.1038/srep00111 PMID: 22355628
29. Otaki JM (2012) Structural analysis of eyespots: dynamics of morphogenic signals that govern elemental positions in butterfly wings. BMC Syst Biol 6: 17. doi: 10.1186/1752-0509-6-17 PMID: 22409965
30. 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. PMID: 7912449
31. Brakefield PM, Gates J, Keys D, Kesbeke F, Wijngaarden PJ, Monteiro A, French V, Carroll SB (1996) Development, plasticity and evolution of butterfly eyespot patterns. Nature 384: 236-242. PMID: 12809139
32. Beldade P, Brakefield PM, Long AD (2002) Contribution of Distal-less to quantitative variation in butterfly eyespots. Nature 415: 315-318. PMID: 11797007
33. 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. PMID: 15242612
34. Monteiro A, Glaser G, Stockslager S, Glansdrop N, Ramos D (2006) Comparative insights into questions of lepidopteran wing pattern homology. BMC Dev Biol 6: 52. PMID: 17090321
35. Shirai LT, Saenko SV, Keller RA, Jerónimo MA, Brakefield PM, Descimon H, Wahlberg N, Beldade P (2012) Evolutionary history of the recruitment of conserved developmental genes in association to the formation and diversification of a novel trait. BMC Evol Biol 12: 21. doi: 10.1186/1471-2148-12-21 PMID: 22335999
36. 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 Mol Dev Evol 320: 321-331. doi: 10.1002/jez.b.22503 PMID: 23633220
37. Otaki JM, Ogasawara T, Yamamoto H (2005) Morphological comparison of pupal wing cuticle patterns in butterflies. Zool Sci 22: 21-34. PMID: 15684580
38. Otaki JM, Yamamoto H (2004) Species-specific color-pattern modifications of butterfly wings. Dev Growth Differ 46: 1-14. PMID: 15008850
39. Otaki JM (2008) Physiologically induced color-pattern changes in butterfly wings: mechanistic and evolutionary implications. J Insect Physiol 55: 174-182. doi: 10.1016/j.jinsphys.2008.11.006 PMID: 19071130
40. Hiyama A, Taira W, Otaki JM (2012) Color-pattern evolution in response to environmental stress in butterflies. Front Genet 3: 15. doi: 10.3389/fgene.2012.00015 PMID: 22363341
41. Kusaba K, Otaki JM (2009) Positional dependence of scale size and shape in butterfly wings: wing-wide phenotypic coordination of color-pattern elements and background. J Insect Physiol 55: 174-182. doi: 10.1016/j.jinsphys.2008.11.006 PMID: 19071130
42. Dhungel B, Otaki JM (2013) Morphometric analysis of nymphalid butterfly wings: number, size and arrangement of scales, and their implications for tissue-size determination. Entomol Sci 17: 207-218.
43. Kornberg TB, Roy S (2014) Cytonemes as specialized signaling filopodia. Development 141: 729-736. doi: 10.1242/dev.086223 PMID: 24496611
44. Nie J, Mahato S, Zelhof AC (2015) Imaging the Drosphila retina: zwitterionic buffers PIPES and HEPES induce morphological artifacts in tissue fixation. BMC Dev Biol 15: 10. doi: 10.1186/s12861-015-0056-y PMID: 25645690
45. Dhungel B, Otaki JM (2009) Local pharmacological effects of tungstate on the color-pattern determination of butterfly wings: a possible relationship between the eyespot and parafocal element. Zool Sci 26: 758-764. doi: 10.2108/zsj.26.758 PMID: 19877835
46. Nardi J, Magee-Adams SM (1986) Formation of scale spacing patterns in a moth wing, I: Epithelial feet may mediate cell rearrangement. Dev Biol 116: 278-290.
47. Locke M, Huie P (1981) Epidermal feet in insect morphogenesis. Nature 293: 733-735. PMID: 7197325
48. Locke M, Huie P (1981) Epidermal feet in pupal segment morphogenesis. Tissue Cell 13: 787-803. PMID: 7330857
49. Locke M (1985) The structure of epidermal feet during their development. Tissue Cell 17: 901-921. PMID: 18620153
50. Delhanty P, Locke M (1989) The development of epidermal feet in preparation for metamorphosis in an insect. Tissue Cell 21: 891-909. PMID: 18620287
51. Ohno Y, Otaki JM (2015) Spontaneous long-range calcium waves in developing butterfly wings. BMC Dev Biol 15: 17. doi: 10.1186/s12861-015-0067-8 PMID: 25888365
52. Hiyama A, Iwata M, Otaki JM (2010) Rearing the pale grass blue Zizeeria maha (Lepidoptera, Lycaenidae): Toward the establishment of a lycaenid model system for butterfly physiology and genetics. Entomol Sci 13:293-302.
53. Taira W, Nohara C, Hiyama A, Otaki JM (2014) Fukushima's biological impacts: the case of the pale grass blue butterfly. J Hered 105:710-722. doi: 10.1093/jhered/esu013 PMID: 25124816
54. Nardi JB, Kafatos FC (1976) Polarity and gradients in lepidopteran wing epidermis. II. The differential adhesiveness model: gradient of a non-diffusible cell surface parameter. J Embryol Exp Morphol 36: 489-512. PMID: 796405
55. Dhungel B, Otaki JM (2013) Baculovirus-mediated gene transfer in butterfly wings in vivo: an efficient expression system with an anti-gp64 antibody. BMC Biotechnol 13: 27. doi: 10.1186/1472-6750-13-27 PMID: 23522444
56. Ando T, Fujiwara H (2013) Electroporation-mediated somatic transgenesis for rapid functional analysis in insects. Development 140: 454-458. doi: 10.1242/dev.085241 PMID: 23250219