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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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The time course of signal release and propagation for eyespots and parafocal elements (PFEs) on the dorsal forewing as proposed by the induction model. The three signals are released at different time points and are propagated autonomously. The mechanisms of signal settlement are unclear in this figure. Note that in this figure, the PFE signal is released before pupation, whereas the eyespot signal is released after pupation. However, this appears to be true only for the forewing; all signals may be released before pupation in the hindwing. Reproduced from Otaki [15]
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Figure 2: The time course of signal release and propagation for eyespots and parafocal elements (PFEs) on the dorsal forewing as proposed by the induction model. The three signals are released at different time points and are propagated autonomously. The mechanisms of signal settlement are unclear in this figure. Note that in this figure, the PFE signal is released before pupation, whereas the eyespot signal is released after pupation. However, this appears to be true only for the forewing; all signals may be released before pupation in the hindwing. Reproduced from Otaki [15]

Mentions: The induction model is briefly reviewed here as a starting point for the present study (Figure 2) [15]. One of the main characteristics of the induction model is heterochronic signal release. Each dark ring of an eyespot and PFE is determined by an independent signal that is sequentially released at different time points from the prospective eyespot focus. The signal is basically autonomous and mostly independent of the focal activity. Once released, each slowly moving signal settles at a particular position. The signal induces itself at close proximity and induces inhibitory signals at distant positions both while it is moving and after it settles.


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

Otaki JM - BMC Syst Biol (2012)

The time course of signal release and propagation for eyespots and parafocal elements (PFEs) on the dorsal forewing as proposed by the induction model. The three signals are released at different time points and are propagated autonomously. The mechanisms of signal settlement are unclear in this figure. Note that in this figure, the PFE signal is released before pupation, whereas the eyespot signal is released after pupation. However, this appears to be true only for the forewing; all signals may be released before pupation in the hindwing. Reproduced from Otaki [15]
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: The time course of signal release and propagation for eyespots and parafocal elements (PFEs) on the dorsal forewing as proposed by the induction model. The three signals are released at different time points and are propagated autonomously. The mechanisms of signal settlement are unclear in this figure. Note that in this figure, the PFE signal is released before pupation, whereas the eyespot signal is released after pupation. However, this appears to be true only for the forewing; all signals may be released before pupation in the hindwing. Reproduced from Otaki [15]
Mentions: The induction model is briefly reviewed here as a starting point for the present study (Figure 2) [15]. One of the main characteristics of the induction model is heterochronic signal release. Each dark ring of an eyespot and PFE is determined by an independent signal that is sequentially released at different time points from the prospective eyespot focus. The signal is basically autonomous and mostly independent of the focal activity. Once released, each slowly moving signal settles at a particular position. The signal induces itself at close proximity and induces inhibitory signals at distant positions both while it is moving and after it settles.

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