Socket Array Irregularities and Wing Membrane Distortions at the Eyespot Foci of Butterfly Wings Suggest Mechanical Signals for Color Pattern Determination
<p>Wing color patterns of the Blue Pansy butterfly <span class="html-italic">J. orithya</span>. (<b>a</b>) Dorsal wings. Males have a single blue form (right), and females have blue and brown forms (middle and left, respectively). In each wing, there are two eyespots, the anterior and posterior ones. Potential eyespot foci are named the first, second, third, fourth, fifth, and sixth focal areas from the anterior to posterior sides. An asterisk indicates the background area where physical damage was made to induce ectopic color patterns. (<b>b</b>) Dorsal cover scale image. Dorsal cover scales were removed at once from the wings with transparent adhesive tape for the purpose of illustrating wing veins and compartments. Scales along the wing veins are not present in this image, highlighting the wing veins. The anterior and posterior eyespot foci are located in the compartments M<sub>1</sub> and CuA<sub>1</sub>, respectively.</p> "> Figure 2
<p>Forewing eyespots. (<b>a</b>) The anterior eyespot (an arrow). (<b>b</b>) Magnification of the anterior eyespot shown in (<b>a</b>). (<b>c</b>) Focal area of (<b>b</b>). (<b>d</b>) Focal area without scales. An arrow indicates the location of the focal area, nearly at the end of the midline. This is a contralateral wing from the wing shown in (<b>a</b>–<b>c</b>). The following e and f are also contralateral wings. Thus, the wing margin is to the right. (<b>e</b>) Magnification of (<b>d</b>). (<b>f</b>) Magnification of (<b>e</b>). An arrow indicates a relatively large socket interval in the focal area. (<b>g</b>) The posterior eyespot (an arrow). (<b>h</b>) Magnification of the posterior eyespot shown in (<b>g</b>). (<b>i</b>) Focal area of (<b>h</b>). Scale directions appeared to be somewhat irregular. (<b>j</b>) Focal area without scales. An arrow indicates the location of the focal area, nearly at the end of the midline. This is a contralateral wing from the wing shown in (<b>g</b>–<b>i</b>). The following (<b>k</b>,<b>l</b>) are also contralateral wings. Thus, the wing margin is to the right. (<b>k</b>) Magnification of (<b>j</b>). (<b>l</b>) Magnification of (<b>k</b>). An arrow indicates a relatively large socket interval in the focal area.</p> "> Figure 3
<p>Anterior eyespot in the hindwing (female). (<b>a</b>) The anterior eyespot of an individual. (<b>b</b>) Magnification of the focal area of the posterior eyespot shown in (<b>a</b>). White focal scales are positioned without disorganization. (<b>c</b>) The eyespot area without scales. An arrow indicates the focal area at the end of the midline. This eyespot is identical to the one shown in (<b>a</b>,<b>b</b>). (<b>d</b>) Magnification of (<b>c</b>). (<b>e</b>) Magnification of (<b>d</b>). An arrow indicates an area of socket array irregularities. (<b>f</b>) Magnification of (<b>e</b>). An arrow indicates an area of socket array irregularities. (<b>g</b>) The anterior eyespot of another individual. (<b>h</b>) Magnification of the focal area of the posterior eyespot shown in (<b>g</b>). Blue and white focal scales are positioned without disorganization. (<b>i</b>) The eyespot without scales. An arrow indicates the focal area at the end of the midline. This eyespot is identical to the one shown in (<b>g</b>,<b>h</b>). (<b>j</b>) Magnification of (<b>i</b>). Arrows indicate distortions of the wing membrane. (<b>k</b>) Magnification of (<b>j</b>). Arrows indicate distortions of the wing membrane. (<b>l</b>) Magnification of (<b>k</b>).</p> "> Figure 4
<p>Posterior eyespot in the hindwing (male). (<b>a</b>) The posterior eyespot. (<b>b</b>) Magnification of the focal area of the posterior eyespot shown in (<b>a</b>). White focal scales are disorganized in direction. (<b>c</b>) The eyespot area without scales. The arrow indicates the focal area at the end of the midline. This eyespot is identical to the one shown in (<b>a</b>,<b>b</b>). (<b>d</b>) Magnification of (<b>c</b>). An arrow indicates an area of disorder. (<b>e</b>) Magnification of (<b>d</b>). Arrows indicate striking distortions of the wing membrane, one of which is associated with the unusual arrangement of socket arrays. (<b>f</b>) Magnification of (<b>e</b>). Arrows indicate striking distortions of the basal membrane. (<b>g</b>) Magnification of (<b>f</b>). (<b>h</b>) Another magnification of (<b>f</b>).</p> "> Figure 5
<p>Anterior and posterior eyespots in the unexpanded forewing (female). (<b>a</b>) The whole unexpanded forewing. (<b>b</b>) Magnification of the anterior eyespot shown in (<b>a</b>). (<b>c</b>) Magnification of the posterior eyespot shown in (<b>a</b>). (<b>d</b>) The anterior eyespot without scales. This is a contralateral wing from the wing shown in (<b>a</b>–<b>c</b>). Panels (<b>e</b>–<b>i</b>) also show images of the contralateral wing. Thus, the wing margin is to the left. (<b>e</b>) Magnification of (<b>d</b>). An arrow indicates the focal area, which is nearly at the end of the midline. (<b>f</b>) Magnification of (<b>e</b>). An arrow indicates a socket interval disorder. (<b>g</b>) Posterior eyespot without scales. (<b>h</b>) Magnification of the focal area of the posterior eyespot shown in (<b>g</b>). An arrow indicates the focal area, which is nearly at the end of the midline. (<b>i</b>) Magnification of (<b>h</b>). Arrows indicate irregularities in socket intervals.</p> "> Figure 6
<p>Anterior and posterior eyespots in the unexpanded hindwing (female). (<b>a</b>) The whole unexpanded hindwing. (<b>b</b>) Magnification of the anterior eyespot shown in (<b>a</b>). (<b>c</b>) Magnification of the posterior eyespot shown in (<b>a</b>). (<b>d</b>) The anterior eyespot area without scales. This is a contralateral wing from the wing shown in (<b>a</b>–<b>c</b>). (<b>e</b>) Magnification of (<b>d</b>). An arrow indicates the focal area. (<b>f</b>) Magnification of (<b>e</b>). An arrow indicates a socket interval disorder. (<b>g</b>) The posterior eyespot area without scales. This wing is obtained from an individual different from that of (<b>a</b>–<b>f</b>). (<b>h</b>) Magnification of the focal area of the posterior eyespot shown in (<b>g</b>). An arrow indicates the focal area, which is nearly at the end of the midline. (<b>i</b>) Magnification of (<b>h</b>). An arrow indicates disorders of socket intervals. (<b>j</b>) The posterior (fifth) eyespot area without scales from yet another individual. (<b>k</b>) Magnification of the focal area of the posterior eyespot shown in (<b>j</b>). An arrow indicates the focal area. (<b>l</b>) Magnification of (<b>k</b>). An arrow indicates irregularities in socket intervals.</p> "> Figure 7
<p>Potential focal areas in the unexpanded forewing. (<b>a</b>) The first focal area. (<b>b</b>) Magnification of the first focal area shown in (<b>a</b>). (<b>c</b>) Magnification of (<b>b</b>). (<b>d</b>) The third focal area. (<b>e</b>) Magnification of (<b>d</b>). (<b>f</b>) Magnification of (<b>e</b>). (<b>g</b>) The fourth focal area. (<b>h</b>) Magnification of the focal area shown in (<b>g</b>). (<b>i</b>) Magnification of (<b>h</b>).</p> "> Figure 8
<p>Potential focal areas in the unexpanded hindwing. (<b>a</b>) The first focal area. (<b>b</b>) Magnification of the first focal area shown in (<b>a</b>). (<b>c</b>) Magnification of (<b>b</b>). (<b>d</b>) The third focal area. (<b>e</b>) Magnification of (<b>d</b>). (<b>f</b>) Magnification of (<b>e</b>). (<b>g</b>) The fourth focal area. (<b>h</b>) Magnification of the focal area shown in (<b>g</b>). (<b>i</b>) Magnification of (<b>h</b>).</p> "> Figure 9
<p>Damage-induced hindwing color patterns. (<b>a</b>) A whole male wing with a damage-induced black spot. An arrow indicates the induced spot. (<b>b</b>) Magnification of the damage-induced black spot shown in (<b>a</b>). An arrow indicates the damaged point. (<b>c</b>) Magnification of (<b>b</b>). Scales are disordered in direction and density. (<b>d</b>) Damaged area without scales. The damaged area is indicated by an arrow. (<b>e</b>) Magnification of (<b>d</b>). Arrows indicate socket irregularities in the direction and substantial distortions of the wing membrane. (<b>f</b>) Magnification of (<b>e</b>). (<b>g</b>) A wing with a damage-induced orange area (an arrow). (<b>h</b>) Magnification of (<b>g</b>). There are black scales at the center (an arrow). (<b>i</b>) Magnification of (<b>h</b>). (<b>j</b>) A damaged area without scales. The arrow indicates the area of socket array irregularities. (<b>k</b>) Magnification of (<b>j</b>). An arrow indicates the area of socket array irregularity. (<b>l</b>) Magnification of (<b>k</b>). An arrow indicates an isolated socket with large intervals.</p> "> Figure 10
<p>Damage-induced color patterns in the unexpanded hindwing. (<b>a</b>) A whole male wing with a damage-induced black spot. An arrow indicates the induced spot. (<b>b</b>) Magnification of the damage-induced black spot shown in (<b>a</b>). (<b>c</b>) Magnification of (<b>b</b>). (<b>d</b>) Damaged area without scales. The damaged area is indicated by an arrow. (<b>e</b>) Magnification of (<b>d</b>). An arrow indicates the damaged area of the wing membrane. (<b>f</b>) Magnification of (<b>e</b>). There are many socket array irregularities (an arrow). (<b>g</b>) Wing with a damage-induced orange area (an arrow). (<b>h</b>) Magnification of (<b>g</b>). An arrow indicates the damaged area. (<b>i</b>) Magnification of (<b>h</b>). An arrow indicates the damaged area. (<b>j</b>) A damaged area without scales. An arrow indicates the area of socket array irregularities. (<b>k</b>) Magnification of (<b>j</b>). An arrow indicates the area of socket array irregularities. (<b>l</b>) Magnification of (<b>k</b>). An arrow indicates the irregular socket intervals.</p> "> Figure 11
<p>Female anterior eyespot focal areas of the nonrandom sampling group via light microscopy and SEM. Four representative samples are shown. Each line of panels contains images of a single individual. (<b>a</b>) Eyespot focal area of individual No. 30. (<b>b</b>,<b>c</b>) Wing membrane distortions at a branching point of socket arrays (arrows). (<b>d</b>) Magnification of (<b>b</b>). (<b>e</b>) Magnification of (<b>c</b>). (<b>f</b>) Eyespot focal area of individual No. 36. (<b>g</b>) Socket arrays with many branching points. Arrows indicate ridges or furrows parallel to socket arrays. (<b>h</b>) Socket arrays with irregularities and wing membrane distortion (an arrow). (<b>i</b>) Socket arrays with displaced sockets (arrows). (<b>j</b>) Magnification of (<b>h</b>). (<b>k</b>) Eyespot focal area of individual No. 39. (<b>l</b>) Socket arrays with many branches. (<b>m</b>) A displaced socket with wing membrane distortion (an arrow). (<b>n</b>) Magnifiction of (<b>m</b>). (<b>o</b>) A socket with the wing membrane distortion at a branching point of socket arrays. (<b>p</b>) Eyespot focal area of individual No. 42. (<b>q</b>) Socket arrays with an irregular socket at a branching point (an arrowhead). Ridges perpendicular to socket arrays are indicated (arrows). (<b>r</b>) Socket arrays with perpendicular ridges (arrows) and a parallel furrow (an arrowhead). (<b>s</b>,<b>t</b>) Magnification of q.</p> "> Figure 12
<p>Female anterior eyespot focal areas of the random sampling group via light microscopy and SEM. Four representative samples are shown. Each line of panels contains images of a single individual. (<b>a</b>) Eyespot focal area of individual No. 12. (<b>b</b>) Socket arrays with irregularities. Long (an arrow) and short (an arrowhead) socket intervals are indicated. (<b>c</b>) Socket arrays with an extra socket (an arrow) and wing membrane distortion (an arrowhead). (<b>d</b>,<b>e</b>) Magnification of (<b>c</b>). (<b>f</b>) Eyespot focal area of individual No. 17. (<b>g</b>) Socket arrays with many branching points. (<b>h</b>) Socket arrays with a long socket interval (an arrow) and a displaced socket at a branching point (an arrowhead). (<b>i</b>) Magnification of (<b>h</b>) (left side). (<b>j</b>) Magnification of (<b>h</b>). (<b>k</b>) Eyespot focal area of individual No. 23. (<b>l</b>) Socket arrays with a relatively small number of branching points. (<b>m</b>) Magnification of (<b>l</b>). (<b>n</b>) Socket array with an irregular socket (an arrow). (<b>o</b>) Magnification of (<b>n</b>). (<b>p</b>) Eyespot focal area of individual No. 43. (<b>q</b>) Socket arrays with branching points. (<b>r</b>) Magnification of (<b>q</b>). (<b>s</b>) Magnification of (<b>q</b>). A displaced socket at a branching point is indicated by an arrow. (<b>t</b>) Magnification of (<b>s</b>). An isolated large socket is shown.</p> "> Figure 13
<p>Physical distortions and mechanical signals. (<b>a</b>) Illustration of the physical distortions of the wing membrane detected in this study. The distortion is located at the tip of the midline. (<b>b</b>) Possible mechanical forces from the wing veins, the marginal band organizer, and the discal organizer (left). The prospective eyespot organizer then pushes back to balance forces (right). (<b>c</b>) Feedback and reinforcement of the mechanical signals from the prospective eyespot organizer. Reinforcement indicates further secretion of the cuticle to bind to the pupal cuticle focal spot more tightly and the polyploidization of organizing cells.</p> ">
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Butterflies and Wing Specimens
2.2. Nomenclature
2.3. Physical Damage
2.4. Microscopic Analyses and Sample Preparation
2.5. Definitions, Frequency Calculations, and Statistics
3. Results
3.1. Eyespot Focal Areas of Expanded Wings
3.2. Eyespot Focal Areas of Unexpanded Wings before Eclosion
3.3. Potential Focal Areas without Eyespots
3.4. Damaged Sites of Expanded Wings after Eclosion
3.5. Damaged Sites of Unexpanded Wings before Eclosion
3.6. Relationships among Scales, Sockets, and Wing Membrane
4. Discussion
4.1. Socket Array Irregularities and Wing Membrane Distortions
4.2. Mechanical Signals and Mechanical Organizers
4.3. Unexpanded Wings and Damage-Induced Modifications
4.4. Conventional Models and Mechanical Model
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Nakazato, Y.; Otaki, J.M. Socket Array Irregularities and Wing Membrane Distortions at the Eyespot Foci of Butterfly Wings Suggest Mechanical Signals for Color Pattern Determination. Insects 2024, 15, 535. https://doi.org/10.3390/insects15070535
Nakazato Y, Otaki JM. Socket Array Irregularities and Wing Membrane Distortions at the Eyespot Foci of Butterfly Wings Suggest Mechanical Signals for Color Pattern Determination. Insects. 2024; 15(7):535. https://doi.org/10.3390/insects15070535
Chicago/Turabian StyleNakazato, Yugo, and Joji M. Otaki. 2024. "Socket Array Irregularities and Wing Membrane Distortions at the Eyespot Foci of Butterfly Wings Suggest Mechanical Signals for Color Pattern Determination" Insects 15, no. 7: 535. https://doi.org/10.3390/insects15070535