Morphometric analysis of nymphalid butterfly wings: Number, size and arrangement of scales, and their implications for tissue-size determination

Entomological Science

Volumn 17, Issue 2, 2014, Pages 207-218

  Dhungel, Bidur ^a   Otaki, Joji M ^a  

^a UNIVERSITY OF THE RYUKYUS   (Japan)

Author keywords

Allometry; Developmental plasticity; Isometry; Lepidoptera; Morphogenic signal; Nymphalidae; Scale cell

Indexed keywords

EID: 84897961121     PISSN: 13438786     EISSN: 14798298     Source Type: Journal    
DOI: 10.1111/ens.12046     Document Type: Article

References (58)

1. Azevedo RBR, French V, Partridge L (2002) Temperature modulates epidermal cell size in Drosophila melanogaster. Journal of Insect Physiology 48, 231-237.
2. Beldade P, Brakefield PM (2003) Concerted evolution and developmental integration in modular butterfly wing patterns. Evolution and Development 5, 169-179.
3. Beldade P, Koops K, Brakefield PM (2002) Modularity, individuality, and evo-devo in butterfly wings. Proceedings of the National Academy of Sciences of the United States of America 99, 14 262-14 267.
4. Brakefield PM, French V (1995) Eyespot development on butterfly wings: the epidermal response to damage. Developmental Biology 168, 98-111.
5. Cho EH, Nijhout HF (2012) Development of polyploidy of scale-building cells in the wings of Manduca sexta. Arthropod Structure and Development 42, 37-46.
6. Conlon I, Raff M (1999) Size control in animal development. Cell 96, 235-244.
7. Dahmann C, Basler K (1999) Compartment boundaries: at the edge of development. Trends in Genetics 15, 320-326.
8. de Moed GH, de Jong G, Scharloo W (1997) Environmental effects on body size variation in Drosophila melanogaster and its cellular basis. Genetic Research 70, 35-43.
9. 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. Zoological Science 26, 758-764.
10. Edgar BA, Nijhout HF (2004) Growth and cell cycle control in Drosophila. In: Hall MN, Raff M, Thomas G (eds) Cell Growth: Control of Cell Size, pp 23-83. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
11. Follette PJ, Duronio RJ, O'Farrell PH (1998) Fluctuations in cyclin E levels are required for multiple rounds of endocycle S phase in Drosophila. Current Biology 8, 235-238.
12. Frankino WA, Zwaan BJ, Stern DL, Brakefield PM (2005) Natural selection and developmental constraints in the evolution of allometries. Science 307, 718-720.
13. Frankino WA, Zwaan BJ, Stern DL, Brakefield PM (2007) Internal and external constraints in the evolution of morphological allometries in a butterfly. Evolution 61, 2958-2970.
14. French V, Brakefield PM (1995) Eyespot development on butterfly wings: the focal signal. Developmental Biology 168, 112-123.
15. Gatti M, Baker BS (1989) Genes controlling essential cell-cycle functions in Drosophila melanogaster. Genes and Development 3, 438-453.
16. Ghiradella H (1998) Hairs, bristles and scales. In: Harrison FW, Locke M (eds) Microscopic Anatomy of Invertebrates, Volume 11: Insecta, pp 257-287. John Wiley & Sons, New York.
17. González-Gaitán M, Capdevila MP, García-Bellido A (1994) Cell proliferation patterns in the wing imaginal disc of Drosophila. Mechanisms of Development 46, 183-200.
18. Greenstein ME (1972) The ultrastructure of developing wings in the giant silkmoth, Hyalophora cecropia. II. Scale-forming and socket-forming cells. Journal of Morphology 136, 23-52.
19. Hayashi S (1996) A Cdc2 dependent checkpoint maintains diploidy in Drosophila. Development 122, 1051-1058.
20. 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.)
21. Henke K, Pohley H-J (1952) Differentielle Zellteilungen und Polyploedie bei der Schuppenbildung der Mehlmotte Ephestia kühniella. Zeitschrift für Naturforschung Section B 7, 65-79. (In German.)
22. Janssen JM, Monteiro A, Brakefield PM (2001) Correlations between scale structure and pigmentation in butterfly wings. Evolution and Development 3, 415-423.
23. Koch PB, Lorenz U, Brakefield PM, ffrench-Constant RH (2000) Butterfly wing pattern mutants: developmental heterochrony and co-ordinately regulated phenotypes. Development Genes and Evolution 210, 536-544.
24. Kristensen NP, Simonsen TJ (2003) Hairs and scales. In: Kristensen NP (ed.) Lepidoptera, Moths and Butterflies: Morphology, Physiology, and Development. Handbook of Zoology, Volume IV, Arthropoda: Insecta, pp 9-22. Walter de Gruyter, Berlin.
25. Kusaba K, Otaki JM (2009) Positional dependence of scale size and shape in butterfly wings: wing-wide phenotypic coordination of colour-pattern elements and background. Journal of Insect Physiology 55, 174-182.
26. Milán M, Cohen SM (2000) Subdividing cell populations in the developing limbs of Drosophila: do wing veins and leg segments define units of growth control? Developmental Biology 217, 1-9.
27. Milán M, Perez L, Cohen SM (2002) Short-range cell interactions and cell survival in the Drosophila wing. Developmental Cell 2, 797-805.
28. Mirth CK, Riddiford LM (2007) Size assessment and growth control: how adult size is determined in insects. BioEssays 29, 344-355.
29. Monteiro A, Glaser G, Stockslager S, Glansdrop N, Ramos D (2006) Comparative insights into questions of lepidopteran wing pattern homology. BMC Developmental Biology 6, 52.
30. Monteiro A, Prijs J, Bax M, Hakkaart T, Brakefield PM (2003) Mutants highlight the modular control of butterfly eyespot patterns. Evolution and Development 5, 180-187.
31. Neufeld TP, de la Cruz AF, Johnston LA, Edgar BA (1998) Coordination of growth and cell division in the Drosophila wing. Cell 93, 1183-1193.
32. Nijhout HF (1980a) Ontogeny of the color pattern on the wings of Precis coenia. Developmental Biology 80, 275-288.
33. Nijhout HF (1980b) Pattern formation on lepidopteran wings: determination of an eyespot. Developmental Biology 80, 267-274.
34. Nijhout HF (1991) The Development and Evolution of Butterfly Wing Patterns. Smithsonian Institution Press, Washington, DC.
35. Nijhout HF (2001) Elements of butterfly wing patterns. Journal of Experimental Zoology 291, 213-225.
36. O'Farrell PH (2004) How metazoans reach their full size: the natural history of bigness. In: Hall MN, Raff M, Thomas G (eds) Cell Growth: Control of Cell Size, pp 1-22. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Otaki JM (2008) Physiologically induced colour-pattern changes in butterfly wings: mechanistic and evolutionary implications. Journal of Insect Physiology 54, 1099-1112.
38. Otaki JM (2009) Colour-pattern analysis of parafocal elements in butterfly wings. Entomological Science 12, 74-83.
39. Otaki JM (2011a) Colour-pattern analysis of eyespots in butterfly wings: a critical examination of morphogen gradient models. Zoological Science 28, 403-413.
40. Otaki JM (2011b) Generation of butterfly wing eyespot patterns: a model for morphological determination of eyespot and parafocal element. Zoological Science 28, 817-827.
41. Otaki JM (2011c) Artificially induced changes of butterfly wing colour patterns: dynamic signal interactions in eyespot development. Scientific Reports 1, 111.
42. Otaki JM (2012a) Colour pattern analysis of nymphalid butterfly wings: revision of the nymphalid groundplan. Zoological Science 29, 568-576.
43. Otaki JM (2012b) Structural analysis of eyespots: dynamics of morphogenic signals that govern elemental positions in butterfly wings. BMC Systems Biology 6, 17.
44. Otaki JM, Ogasawara T, Yamamoto H (2005) Morphological comparison of pupal wing cuticle patterns in butterflies. Zoological Science 22, 21-34.
45. Partridge L, Barrie B, Fowler K, French V (1994) Evolution and development of body size and cell size in Drosophila melanogaster in response to temperature. Evolution 48, 1269-1276.
46. Powell JR (1974) Temperature related genetic divergence in Drosophila body size. Journal of Heredity 65, 257-258.
47. Raff MC (1996) Size control: the regulation of cell numbers in animal development. Cell 86, 173-175.
48. Saenko SV, Brakefield PM, Beldade P (2010) Single locus affects embryonic segment polarity and multiple aspects of an adult evolutionary novelty. BMC Biology 8, 111.
49. Sekimura T, Zhu M, Cook J, Maini PK, Murray JD (1999) Pattern formation of scale cells in lepidoptera by differential origin-dependent cell adhesion. Bulletin of Mathematical Biology 61, 807-828.
50. Simonsen TJ, Kristensen NP (2003) Scale length/wing length correlation in Lepidoptera (Insecta). Journal of Natural History 37, 673-679.
51. Süffert F (1937) Die Geschichte der Bildungs zellen im Puppen-flügelepithel bei einem Tagschmetterling. Biologisches Zentralblatt 57, 615-628. (In German.)
52. Takayama E, Yoshida A (1997) Color pattern formation on the wing of the butterfly Pieris rapae. 1. Cautery induced alteration of scale color and delay of arrangement formation. Development Growth and Differentiation 39, 23-31.
53. Vukusic P, Sambles JR, Lawrence CR (2000) Colour mixing in wing scales of a butterfly. Nature 404, 457.
54. Weigmann K, Cohen SM, Lehner CF (1997) Cell-cycle progression, growth and patterning in imaginal discs despite inhibition of cell division after inactivation of Drosophila Cdc2 kinase. Development 124, 3555-3563.
55. Weiss A, Herzig A, Jacobs H, Lehner CF (1998) Continuous cyclin E expression inhibits progression through endoreduplication cycles in Drosophila. Current Biology 8, 239-242.
56. Yoshida A (1988) [Scale arrangement on lepidopteran wings]. Special Bulletin of the Lepidopterological Society of Japan 6, 447-464. (In Japanese.)
57. Yoshida A, Aoki K (1989) Scale arrangement pattern in a lepidopteran wing. 1. Periodic cellular pattern in the pupal wing of Pieris rapae. Development Growth and Differentiation 31, 601-609.
58. Yoshida A, Shinkawa T, Aoki K (1983) Periodical arrangement on lepidopteran (butterfly and moth) wings. Proceedings of the Japan Academy 59B, 236-239.