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

Abstract

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.

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

“…Likely interpretations would be that the major eyespot organizers need extracellular supporting materials to propagate morphogenic signals and that the anterior side alone that was covered with the pupal case cannot expand without the help of the posterior side. These interpretations are consistent with the previous chapter that describes synergistic signal amplification and expansion processes in this eyespot [26]. Indeed, the anterior side of the major eyespot appeared to be more sensitive to the present treatments and also to physical damage [26] than the posterior side despite the fact that the anterior side is physically hidden.…”

“…When the anterior eyespot focus was physically damaged by a stainless needle, the major eyespot was reduced in size not only in the anterior side but also in the posterior side, suggesting synergistic interactions of signals from two adjacent organizers. When the posterior eyespot focus was damaged, similar effect was observed, but it was much less effective [26]. In the present study, the ball placed on the posterior portion of the major eyespot appears to be at least as effective as physical damage at the posterior focus, suggesting the importance of distortion in developmental fate determination.…”

“…The degrees of size reduction in the major eyespot in response to the ball treatment may be compared with the damage-induced changes in the previous study [26]. When the anterior eyespot focus was physically damaged by a stainless needle, the major eyespot was reduced in size not only in the anterior side but also in the posterior side, suggesting synergistic interactions of signals from two adjacent organizers.…”

“…It is surprising that the miniaturization of the major eyespot by the present operations is more efficient than the physical damage treatment [26], despite the fact that the present operations are less invasive. Likely interpretations would be that the major eyespot organizers need extracellular supporting materials to propagate morphogenic signals and that the anterior side alone that was covered with the pupal case cannot expand without the help of the posterior side.…”

“…Importantly, the background area has a light orange coloration and does not harbor anything like semi-element or pseudoelement, which probably exists in the blue pansy butterfly, J. orithya (Linnaeus, 1758) [21][22][23]. Furthermore, several versions of color-pattern modifications in response to various treatments have already been known in the peacock pansy butterfly; it has been used for the injections of sodium tungstate, and ecdysteroid and for temperature shock [24] and for physical damage [25,26]. The scale-size and scale-color distributions have also been recorded in detail in this species [27].…”