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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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Wing colour patterns of Junonia almana. Each eyespot (ES) is referred to as indicated for convenience. Terms for eyespot substructures and peripheral elements are indicated on the right side.
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Figure 1: Wing colour patterns of Junonia almana. Each eyespot (ES) is referred to as indicated for convenience. Terms for eyespot substructures and peripheral elements are indicated on the right side.

Mentions: Throughout this paper, I focus on the eyespots and parafocal elements (PFEs) of the peacock pansy butterfly, Junonia almana (Figure 1). The eyespots of this nymphalid butterfly have several notable features that are not found in the eyespots of other butterflies. Specifically, unlike some satyrine butterflies, including Bicyclus and Ypthima, that exhibit "typical" symmetric eyespots, J. almana shows remarkable intra-individual variation in eyespot size and morphology [26,27]. This variation makes morphological comparison between eyespots both possible and fruitful. Based on a colour-pattern analysis of J. almana, I present a simple descriptive mathematical model to explain the possible behaviour of morphogenic signals in light of the induction model that is consistent with both observational and experimental results.


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

Otaki JM - BMC Syst Biol (2012)

Wing colour patterns of Junonia almana. Each eyespot (ES) is referred to as indicated for convenience. Terms for eyespot substructures and peripheral elements are indicated on the right side.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Wing colour patterns of Junonia almana. Each eyespot (ES) is referred to as indicated for convenience. Terms for eyespot substructures and peripheral elements are indicated on the right side.
Mentions: Throughout this paper, I focus on the eyespots and parafocal elements (PFEs) of the peacock pansy butterfly, Junonia almana (Figure 1). The eyespots of this nymphalid butterfly have several notable features that are not found in the eyespots of other butterflies. Specifically, unlike some satyrine butterflies, including Bicyclus and Ypthima, that exhibit "typical" symmetric eyespots, J. almana shows remarkable intra-individual variation in eyespot size and morphology [26,27]. This variation makes morphological comparison between eyespots both possible and fruitful. Based on a colour-pattern analysis of J. almana, I present a simple descriptive mathematical model to explain the possible behaviour of morphogenic signals in light of the induction model that is consistent with both observational and experimental results.

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