Contact-Mediated Eyespot Color-Pattern Changes in the Peacock Pansy Butterfly: Contributions of Mechanical Force and Extracellular Matrix to Morphogenic Signal Propagation

Otaki, Joji M.

doi:10.5772/intechopen.70098

Cited by 8 publications

(29 citation statements)

References 58 publications

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“…The present results may be explained by a reaction-diffusion mechanism as a part of the induction model, but not by the conventional gradient model. A different set of experiments that removed the surface contact from the posterior side of the hindwing major eyespot results in miniaturization of both the anterior and posterior sides of the eyespot [51], suggesting synergistic interactions between the two focal signals that are consistent with the present study.…”

Section: Discussionsupporting

confidence: 86%

Synergistic Damage Response of the Double-Focus Eyespot in the Hindwing of the Peacock Pansy Butterfly

Iwasaki¹,

Otaki²

2017

Lepidoptera

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Eyespot color patterns in butterfly wings are determined by the putative morphogenic signals from organizers. Previous experiments using physical damage to the forewing eyespots of the peacock pansy butterfly, Junonia almana (Linnaeus, 1758), suggested that the morphogenic signals dynamically interact with each other, involving enhancement of activation signals and interactions between activation and inhibitory signals. Here, we focused on the large double-focus fusion eyespot on the hindwing of J. almana to test the involvement of the proposed signal interactions. Early damage at a single focus of the prospective double-focus eyespot produced a smaller but circular eyespot, suggesting the existence of synergistic interactions between the signals from two sources. Late damage at a single focus reduced the size of the inner core disk but simultaneously enlarged the outermost black ring. Damage at two nearby sites in the background induced an extensive black area, possibly as a result of the synergistic enhancement of the two induced signals. These results confirmed the previous forewing results and provided further evidence for the long-range and synergistic interactive nature of the morphogenic signals that may be explained by a reaction-diffusion mechanism as a part of the induction model for color-pattern formation in butterfly wings.

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Section: Discussionsupporting

confidence: 86%

Synergistic Damage Response of the Double-Focus Eyespot in the Hindwing of the Peacock Pansy Butterfly

Iwasaki¹,

Otaki²

2017

Lepidoptera

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“…1). Because this species has a large posterior eyespot on its hindwing, which is the target of the present study, eyespot responses were more robust than those of J. almana used in the previous study [67]. Second, various materials (17 treatment modes in contrast to just 5 in the previous study [67]) were tested.…”

Section: Introductionmentioning

confidence: 93%

“…Because this species has a large posterior eyespot on its hindwing, which is the target of the present study, eyespot responses were more robust than those of J. almana used in the previous study [67]. Second, various materials (17 treatment modes in contrast to just 5 in the previous study [67]) were tested. Third, physicochemical properties of various materials were measured according to the water contact angle of the material surface, which represents the repellency or hydrophobicity of the material surface.…”

Section: Introductionmentioning

confidence: 93%

“…Second, the size of the pupal cuticle spots is roughly proportional to adult eyespot size [42]. Third, eyespot color patterns are sensitive not only to physical damage but also to physical distortion of the wing epithelium [11,67].…”

Section: Introductionmentioning

confidence: 99%

“…Although the distortion hypothesis should be examined experimentally, another interesting aspect of eyespot changes is that eyespots respond to contact with materials on the wing tissue at the pupal stage [67]. Focusing on the hindwing eyespots of the peacock pansy butterfly, Junonia almana, it has been demonstrated that its minor eyespots respond differently to contact with materials such as plastic film, glass, silicone glassine paper, and medical adhesive tape; the latter two materials exhibit a strong eyespot-reducing ability.…”

Section: Introductionmentioning

confidence: 99%

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Butterfly eyespot color pattern formation requires physical contact of the pupal wing epithelium with extracellular materials for morphogenic signal propagation

Otaki

2020

BMC Dev Biol

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Background: Eyespot color pattern formation on butterfly wings is sensitive to physical damage and physical distortion as well as physical contact with materials on the surface of wing epithelial tissue at the pupal stage. Contact-mediated eyespot color pattern changes may imply a developmental role of the extracellular matrix in morphogenic signal propagation. Here, we examined eyespot responses to various contact materials, focusing on the hindwing posterior eyespots of the blue pansy butterfly, Junonia orithya. Results: Contact with various materials, including both nonbiological and biological materials, induced eyespot enlargement, reduction, or no change in eyespot size, and each material was characterized by a unique response profile. For example, silicone glassine paper almost always induced a considerable reduction, while glass plates most frequently induced enlargement, and plastic plates generally produced no change. The biological materials tested here (fibronectin, polylysine, collagen type I, and gelatin) resulted in various responses, but polylysine induced more cases of enlargement, similar to glass plates. The response profile of the materials was not readily predictable from the chemical composition of the materials but was significantly correlated with the water contact angle (water repellency) of the material surface, suggesting that the surface physical chemistry of materials is a determinant of eyespot size. When the proximal side of a prospective eyespot was covered with a size-reducing material (silicone glassine paper) and the distal side and the organizer were covered with a material that rarely induced size reduction (plastic film), the proximal side of the eyespot was reduced in size in comparison with the distal side, suggesting that signal propagation but not organizer activity was inhibited by silicone glassine paper. Conclusions: These results suggest that physical contact with an appropriate hydrophobic surface is required for morphogenic signals from organizers to propagate normally. The binding of the apical surface of the epithelium with an opposing surface may provide mechanical support for signal propagation. In addition to conventional molecular morphogens, there is a possibility that mechanical distortion of the epithelium that is propagated mechanically serves as a nonmolecular morphogen to induce subsequent molecular changes, in accordance with the distortion hypothesis for butterfly wing color pattern formation.

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Developmental dynamics of butterfly wings: real-time in vivo whole-wing imaging of twelve butterfly species

Iwata

Tsutsumi

Otaki

2018

Sci Rep

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Colour pattern development of butterfly wings has been studied from several different approaches. However, developmental changes in the pupal wing tissues have rarely been documented visually. In this study, we recorded real-time developmental changes of the pupal whole wings of 9 nymphalid, 2 lycaenid, and 1 pierid species in vivo, from immediately after pupation to eclosion, using the forewing-lift method. The developmental period was roughly divided into four sequential stages. At the very early stage, the wing tissue was transparent, but at the second stage, it became semi-transparent and showed dynamic peripheral adjustment and slow low-frequency contractions. At this stage, the wing peripheral portion diminished in size, but simultaneously, the ventral epithelium expanded in size. Likely because of scale growth, the wing tissue became deeply whitish at the second and third stages, followed by pigment deposition and structural colour expression at the fourth stage. Some red or yellow (light-colour) areas that emerged early were “overpainted” by expanding black areas, suggesting the coexistence of two morphogenic signals in some scale cells. The discal spot emerged first in some nymphalid species, as though it organised the entire development of colour patterns. These results indicated the dynamic wing developmental processes common in butterflies.

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Contact-Mediated Eyespot Color-Pattern Changes in the Peacock Pansy Butterfly: Contributions of Mechanical Force and Extracellular Matrix to Morphogenic Signal Propagation

Cited by 8 publications

References 58 publications

Synergistic Damage Response of the Double-Focus Eyespot in the Hindwing of the Peacock Pansy Butterfly

Synergistic Damage Response of the Double-Focus Eyespot in the Hindwing of the Peacock Pansy Butterfly

Butterfly eyespot color pattern formation requires physical contact of the pupal wing epithelium with extracellular materials for morphogenic signal propagation

Developmental dynamics of butterfly wings: real-time in vivo whole-wing imaging of twelve butterfly species

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