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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 eyespots on the ventral forewing. (A-C) There are three eyespots on the same wing surface: 1st (minor), 2nd (minor), and 3rd (major). The eyespots are enlarged to similar sizes in these photographs. Refer to Figure 1 for their relationship on the wing. Note the differences in the ring width proportions. Modified from Otaki [14]. (D) Ring width ratios in the three eyespots shown in A-C. Small eyespots have wider yellow-ring width proportions. Modified from Otaki [14]. (E) Relationship between eyespot size and ring width. As the eyespot size becomes larger, the inner black ring becomes wider and the yellow ring narrower. Modified from Otaki [14]. (F) The major (3rd) eyespot and other nearby elemental positions on the ventral forewing. The blue arrow indicates the element that could block the propagation of the eyespot signal proximally. (G) A wing identical to that shown in F; however, the wing is illuminated from the bottom upward so that both the dorsal and ventral colour patterns can be simultaneously observed. The blue arrow indicates the position identical to that shown in F. The red arrow indicates the edge of the outer black ring on the dorsal side.
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Figure 3: Colour-pattern analysis of eyespots on the ventral forewing. (A-C) There are three eyespots on the same wing surface: 1st (minor), 2nd (minor), and 3rd (major). The eyespots are enlarged to similar sizes in these photographs. Refer to Figure 1 for their relationship on the wing. Note the differences in the ring width proportions. Modified from Otaki [14]. (D) Ring width ratios in the three eyespots shown in A-C. Small eyespots have wider yellow-ring width proportions. Modified from Otaki [14]. (E) Relationship between eyespot size and ring width. As the eyespot size becomes larger, the inner black ring becomes wider and the yellow ring narrower. Modified from Otaki [14]. (F) The major (3rd) eyespot and other nearby elemental positions on the ventral forewing. The blue arrow indicates the element that could block the propagation of the eyespot signal proximally. (G) A wing identical to that shown in F; however, the wing is illuminated from the bottom upward so that both the dorsal and ventral colour patterns can be simultaneously observed. The blue arrow indicates the position identical to that shown in F. The red arrow indicates the edge of the outer black ring on the dorsal side.

Mentions: The inside-wide rule applies almost universally to the well-developed eyespots of nymphalid butterflies, though small or immature eyespots (sensu Otaki [15]) represent exceptions to this rule. The ring widths of three eyespots of different sizes on the ventral forewings were examined for the purpose of discussing this point more quantitatively. The widths of the inner core rings clearly increased in relation to eyespot size (Figure 3A-E) [15], which likely caused the width of the light rings to decrease in relation to eyespot size. These structural differences among eyespots of different sizes may be mainly due to differences in focal activity [4]. Therefore, the spontaneous velocity-loss mechanism mainly explains the formation of small or immature eyespots.


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 eyespots on the ventral forewing. (A-C) There are three eyespots on the same wing surface: 1st (minor), 2nd (minor), and 3rd (major). The eyespots are enlarged to similar sizes in these photographs. Refer to Figure 1 for their relationship on the wing. Note the differences in the ring width proportions. Modified from Otaki [14]. (D) Ring width ratios in the three eyespots shown in A-C. Small eyespots have wider yellow-ring width proportions. Modified from Otaki [14]. (E) Relationship between eyespot size and ring width. As the eyespot size becomes larger, the inner black ring becomes wider and the yellow ring narrower. Modified from Otaki [14]. (F) The major (3rd) eyespot and other nearby elemental positions on the ventral forewing. The blue arrow indicates the element that could block the propagation of the eyespot signal proximally. (G) A wing identical to that shown in F; however, the wing is illuminated from the bottom upward so that both the dorsal and ventral colour patterns can be simultaneously observed. The blue arrow indicates the position identical to that shown in F. The red arrow indicates the edge of the outer black ring on the dorsal side.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Colour-pattern analysis of eyespots on the ventral forewing. (A-C) There are three eyespots on the same wing surface: 1st (minor), 2nd (minor), and 3rd (major). The eyespots are enlarged to similar sizes in these photographs. Refer to Figure 1 for their relationship on the wing. Note the differences in the ring width proportions. Modified from Otaki [14]. (D) Ring width ratios in the three eyespots shown in A-C. Small eyespots have wider yellow-ring width proportions. Modified from Otaki [14]. (E) Relationship between eyespot size and ring width. As the eyespot size becomes larger, the inner black ring becomes wider and the yellow ring narrower. Modified from Otaki [14]. (F) The major (3rd) eyespot and other nearby elemental positions on the ventral forewing. The blue arrow indicates the element that could block the propagation of the eyespot signal proximally. (G) A wing identical to that shown in F; however, the wing is illuminated from the bottom upward so that both the dorsal and ventral colour patterns can be simultaneously observed. The blue arrow indicates the position identical to that shown in F. The red arrow indicates the edge of the outer black ring on the dorsal side.
Mentions: The inside-wide rule applies almost universally to the well-developed eyespots of nymphalid butterflies, though small or immature eyespots (sensu Otaki [15]) represent exceptions to this rule. The ring widths of three eyespots of different sizes on the ventral forewings were examined for the purpose of discussing this point more quantitatively. The widths of the inner core rings clearly increased in relation to eyespot size (Figure 3A-E) [15], which likely caused the width of the light rings to decrease in relation to eyespot size. These structural differences among eyespots of different sizes may be mainly due to differences in focal activity [4]. Therefore, the spontaneous velocity-loss mechanism mainly explains the formation of small or immature eyespots.

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