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Structural analysis of eyespots: dynamics of morphogenic signals that govern elemental positions in butterfly wings.

Otaki JM - BMC Syst Biol (2012)

Bottom Line: However, a detailed structural analysis of eyespots that can serve as a foundation for future studies is still lacking.It appears that signals are wider near the focus of the eyespot and become narrower as they expand.Natural colour patterns and previous experimental findings that are not easily explained by the conventional gradient model were also explained reasonably well by the formal mathematical simulations performed in this study.

View Article: PubMed Central - HTML - PubMed

Affiliation: The BCPH Unit of Molecular Physiology, Department of Chemistry, Biology and Marine Science, Faculty of Science, University of the Ryukyus, Nishihara, Okinawa 903-0213, Japan. otaki@sci.u-ryukyu.ac.jp

ABSTRACT

Background: To explain eyespot colour-pattern determination in butterfly wings, the induction model has been discussed based on colour-pattern analyses of various butterfly eyespots. However, a detailed structural analysis of eyespots that can serve as a foundation for future studies is still lacking. In this study, fundamental structural rules related to butterfly eyespots are proposed, and the induction model is elaborated in terms of the possible dynamics of morphogenic signals involved in the development of eyespots and parafocal elements (PFEs) based on colour-pattern analysis of the nymphalid butterfly Junonia almana.

Results: In a well-developed eyespot, the inner black core ring is much wider than the outer black ring; this is termed the inside-wide rule. It appears that signals are wider near the focus of the eyespot and become narrower as they expand. Although fundamental signal dynamics are likely to be based on a reaction-diffusion mechanism, they were described well mathematically as a type of simple uniformly decelerated motion in which signals associated with the outer and inner black rings of eyespots and PFEs are released at different time points, durations, intervals, and initial velocities into a two-dimensional field of fundamentally uniform or graded resistance; this produces eyespots and PFEs that are diverse in size and structure. The inside-wide rule, eyespot distortion, structural differences between small and large eyespots, and structural changes in eyespots and PFEs in response to physiological treatments were explained well using mathematical simulations. Natural colour patterns and previous experimental findings that are not easily explained by the conventional gradient model were also explained reasonably well by the formal mathematical simulations performed in this study.

Conclusions: In a mode free from speculative molecular interactions, the present study clarifies fundamental structural rules related to butterfly eyespots, delineates a theoretical basis for the induction model, and proposes a mathematically simple mode of long-range signalling that may reflect developmental mechanisms associated with butterfly eyespots.

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Colour-pattern analysis of tungstate-induced and heat-shock-induced modifications of major eyespots on dorsal and ventral surfaces. (A, B) Dorsal (A) and ventral (B) major eyespots and PFEs of the forewing. Four individuals were aligned according to the possible time sequence of development. Treatment modes are indicated above each wing portion; light blue arrowheads indicate PFEs. Smaller eyespots and PFEs that were dislocated closer to the eyespot focus were considered to represent earlier stages of development. The open area produced by tungstate treatment on the distal sides of smaller eyespots may be attributed to repulsion from PFEs located nearby. Note the size and structural changes of the eyespots. Additionally, note the positional and width changes in the PFEs. Modified from Otaki [27]. (C) Percentages of white foci, inner black core rings, yellow rings, and outer black rings of the major eyespots in the four individuals shown in B. The distal sides of the major eyespots were measured from the centres of the focal areas. (D) Relative distances of PFEs from the focus and relative PFE widths in the four individuals shown in B. The distance was measured from the centre of the focus to the nearest part of the PFEs. The distance and width of the "no treatment" individual were adjusted to 1.00, and other data were normalised accordingly.
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Figure 4: Colour-pattern analysis of tungstate-induced and heat-shock-induced modifications of major eyespots on dorsal and ventral surfaces. (A, B) Dorsal (A) and ventral (B) major eyespots and PFEs of the forewing. Four individuals were aligned according to the possible time sequence of development. Treatment modes are indicated above each wing portion; light blue arrowheads indicate PFEs. Smaller eyespots and PFEs that were dislocated closer to the eyespot focus were considered to represent earlier stages of development. The open area produced by tungstate treatment on the distal sides of smaller eyespots may be attributed to repulsion from PFEs located nearby. Note the size and structural changes of the eyespots. Additionally, note the positional and width changes in the PFEs. Modified from Otaki [27]. (C) Percentages of white foci, inner black core rings, yellow rings, and outer black rings of the major eyespots in the four individuals shown in B. The distal sides of the major eyespots were measured from the centres of the focal areas. (D) Relative distances of PFEs from the focus and relative PFE widths in the four individuals shown in B. The distance was measured from the centre of the focus to the nearest part of the PFEs. The distance and width of the "no treatment" individual were adjusted to 1.00, and other data were normalised accordingly.

Mentions: The eyespots in an individual butterfly that received a tungstate injection were smaller than those in non-treated individuals (Figure 4). The inner orange ring of the modified dorsal major eyespot was wider than that of a normal eyespot based on the proportion of the size of the whole eyespot (Figure 4A). Similar results were obtained for the modified ventral major eyespot (Figure 4B). These modified major eyespots exhibited a similar ring structure to the normal minor eyespots on the same wing surface (compare Figures 4C and 3D).


Structural analysis of eyespots: dynamics of morphogenic signals that govern elemental positions in butterfly wings.

Otaki JM - BMC Syst Biol (2012)

Colour-pattern analysis of tungstate-induced and heat-shock-induced modifications of major eyespots on dorsal and ventral surfaces. (A, B) Dorsal (A) and ventral (B) major eyespots and PFEs of the forewing. Four individuals were aligned according to the possible time sequence of development. Treatment modes are indicated above each wing portion; light blue arrowheads indicate PFEs. Smaller eyespots and PFEs that were dislocated closer to the eyespot focus were considered to represent earlier stages of development. The open area produced by tungstate treatment on the distal sides of smaller eyespots may be attributed to repulsion from PFEs located nearby. Note the size and structural changes of the eyespots. Additionally, note the positional and width changes in the PFEs. Modified from Otaki [27]. (C) Percentages of white foci, inner black core rings, yellow rings, and outer black rings of the major eyespots in the four individuals shown in B. The distal sides of the major eyespots were measured from the centres of the focal areas. (D) Relative distances of PFEs from the focus and relative PFE widths in the four individuals shown in B. The distance was measured from the centre of the focus to the nearest part of the PFEs. The distance and width of the "no treatment" individual were adjusted to 1.00, and other data were normalised accordingly.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3368778&req=5

Figure 4: Colour-pattern analysis of tungstate-induced and heat-shock-induced modifications of major eyespots on dorsal and ventral surfaces. (A, B) Dorsal (A) and ventral (B) major eyespots and PFEs of the forewing. Four individuals were aligned according to the possible time sequence of development. Treatment modes are indicated above each wing portion; light blue arrowheads indicate PFEs. Smaller eyespots and PFEs that were dislocated closer to the eyespot focus were considered to represent earlier stages of development. The open area produced by tungstate treatment on the distal sides of smaller eyespots may be attributed to repulsion from PFEs located nearby. Note the size and structural changes of the eyespots. Additionally, note the positional and width changes in the PFEs. Modified from Otaki [27]. (C) Percentages of white foci, inner black core rings, yellow rings, and outer black rings of the major eyespots in the four individuals shown in B. The distal sides of the major eyespots were measured from the centres of the focal areas. (D) Relative distances of PFEs from the focus and relative PFE widths in the four individuals shown in B. The distance was measured from the centre of the focus to the nearest part of the PFEs. The distance and width of the "no treatment" individual were adjusted to 1.00, and other data were normalised accordingly.
Mentions: The eyespots in an individual butterfly that received a tungstate injection were smaller than those in non-treated individuals (Figure 4). The inner orange ring of the modified dorsal major eyespot was wider than that of a normal eyespot based on the proportion of the size of the whole eyespot (Figure 4A). Similar results were obtained for the modified ventral major eyespot (Figure 4B). These modified major eyespots exhibited a similar ring structure to the normal minor eyespots on the same wing surface (compare Figures 4C and 3D).

Bottom Line: However, a detailed structural analysis of eyespots that can serve as a foundation for future studies is still lacking.It appears that signals are wider near the focus of the eyespot and become narrower as they expand.Natural colour patterns and previous experimental findings that are not easily explained by the conventional gradient model were also explained reasonably well by the formal mathematical simulations performed in this study.

View Article: PubMed Central - HTML - PubMed

Affiliation: The BCPH Unit of Molecular Physiology, Department of Chemistry, Biology and Marine Science, Faculty of Science, University of the Ryukyus, Nishihara, Okinawa 903-0213, Japan. otaki@sci.u-ryukyu.ac.jp

ABSTRACT

Background: To explain eyespot colour-pattern determination in butterfly wings, the induction model has been discussed based on colour-pattern analyses of various butterfly eyespots. However, a detailed structural analysis of eyespots that can serve as a foundation for future studies is still lacking. In this study, fundamental structural rules related to butterfly eyespots are proposed, and the induction model is elaborated in terms of the possible dynamics of morphogenic signals involved in the development of eyespots and parafocal elements (PFEs) based on colour-pattern analysis of the nymphalid butterfly Junonia almana.

Results: In a well-developed eyespot, the inner black core ring is much wider than the outer black ring; this is termed the inside-wide rule. It appears that signals are wider near the focus of the eyespot and become narrower as they expand. Although fundamental signal dynamics are likely to be based on a reaction-diffusion mechanism, they were described well mathematically as a type of simple uniformly decelerated motion in which signals associated with the outer and inner black rings of eyespots and PFEs are released at different time points, durations, intervals, and initial velocities into a two-dimensional field of fundamentally uniform or graded resistance; this produces eyespots and PFEs that are diverse in size and structure. The inside-wide rule, eyespot distortion, structural differences between small and large eyespots, and structural changes in eyespots and PFEs in response to physiological treatments were explained well using mathematical simulations. Natural colour patterns and previous experimental findings that are not easily explained by the conventional gradient model were also explained reasonably well by the formal mathematical simulations performed in this study.

Conclusions: In a mode free from speculative molecular interactions, the present study clarifies fundamental structural rules related to butterfly eyespots, delineates a theoretical basis for the induction model, and proposes a mathematically simple mode of long-range signalling that may reflect developmental mechanisms associated with butterfly eyespots.

Show MeSH
Related in: MedlinePlus