A butterfly’s wing is covered in hundreds of thousands of tiny scales, like miniature shingles on a paper-thin roof. A single scale is as small as a speck of dust, but surprisingly complex, with a wavy surface of ridges that help shed water, manage heat, and reflect light to give the butterfly its characteristic glow.
MIT researchers have now captured the first moments of a butterfly’s metamorphosis, as an individual scale begins to develop this ridged pattern. The researchers used advanced imaging techniques to observe the microscopic features of a developing wing as the butterfly transformed into a chrysalis.
The team continuously photographed individual scales as they grew from the wing membrane. These images reveal for the first time how the initially smooth surface of a scale begins to wrinkle to form microscopic, parallel ripples. These ripple-like structures eventually transform into finely drawn ridges, which define the functions of an adult scale.
The researchers found that the scale’s transition to a wavy surface is likely the result of “buckling” – a general mechanism that describes how a smooth surface wrinkles as it expands in a confined space.
“Buckling is an instability, something we don’t typically want as engineers,” says Mathias Kolle, an associate professor of mechanical engineering at MIT. “But in this context, the organism uses buckling to initiate the growth of these complex functional structures.”
The team is working to visualize more stages of butterfly wing growth in hopes of revealing clues about how they might design advanced functional materials in the future.
“Given the multifunctionality of butterfly scales, we hope to understand and mimic these processes, with the goal of designing and manufacturing new functional materials in a sustainable manner.” These materials would exhibit optical, thermal, chemical and mechanical properties suitable for textiles, building surfaces, vehicles – in fact, any surface that must exhibit characteristics that depend on its micro and nanometric structure,” adds Kolle.
The team published their findings in a study published today in the journal Cell Reports Physical Sciences. Study co-authors include first author and former MIT postdoctoral fellow Jan Totz, co-first author and postdoctoral fellow Anthony McDougal, graduate student Leonie Wagner, former postdoctoral fellow Sungsam Kang, professor of mechanical engineering and engineering biomedical Peter So, Professor of Mathematics Jörn Dunkel and Professor of Physics and Materials Chemistry Bodo Wilts of the University of Salzburg.
A live transformation
In 2021, McDougal, Kolle and their colleagues developed an approach to continuously capture the microscopic details of a butterfly’s wing growth during metamorphosis. Their method involved carefully cutting away the insect’s paper-thin chrysalis and removing a small square of cuticle to reveal the growing wing membrane. They placed a small glass slide over the exposed area, then used a microscope technique developed by team member Peter So to capture continuous images of the scales as they grew out of the membrane of the l ‘wing.
They applied the method to observe Vanessa Cardui, a butterfly commonly known as the Painted Lady, which the team chose for its scale architecture common to most Lepidoptera species. They observed that the Painted Lady’s scales grew along the wing membrane in precise, overlapping rows, like shingles on a roof. These images provided scientists with the most continuous visualization of butterfly wing scale growth at the microscopic level to date.
Image: Courtesy of the researchers
In their new study, the team used the same approach to focus on a specific window of time during scale development, to capture the initial formation of the finely structured ridges that run along a single scale in a living butterfly. Scientists know that these ridges, which run parallel to each other along the length of a single scale, like stripes on a piece of corduroy, enable many of the functions of wing scales.
Since little is known about how these crests form, the MIT team sought to record continued crest formation in a developing living butterfly and decipher the organism’s crest formation mechanisms.
“We watched the wing develop over 10 days and got thousands of measurements of the evolution of the scale surface of a single butterfly,” McDougal says. “We could see very early on that the surface is quite flat. As the butterfly grows, the surface starts to show a little bit, and then at about 41 percent of its development, we see this very regular pattern of completely broken protoridges. This whole process takes place over about five hours and lays the structural foundation for the later expression of patterned ridges.”
Pin
What could be causing the initial ridges to appear in a precise alignment? The researchers suspected that buckling might be at play. Buckling is a mechanical process by which a material bends on itself when subjected to compressive forces. For example, an empty soda can bends when squeezed from top to bottom. A material can also bend as it grows, if it is constrained or immobilized.
Scientists have noted that as the cell membrane of a butterfly’s scales grows, it is actually attached in certain places by actin bundles – long filaments that pass under the growing membrane and act as a scaffold to support the scale as it takes shape. The scientists hypothesized that the actin bundles constrain a growing membrane, similar to the ropes surrounding an inflating hot air balloon. As the butterfly’s wing scale grew, they proposed, it would bulge between the underlying actin filaments, deforming so as to form the initial parallel ridges of a scale.
To test this idea, the MIT team studied a theoretical model that describes the general mechanics of buckling. They incorporated image data into the model, such as measurements of the height of a scale membrane at different early stages of development and various spacings of actin bundles on a growing membrane. They then ran the model forward in time to see if its underlying principles of mechanical buckling would produce the same ridge patterns that the team observed in the real butterfly.
“With this modeling, we showed that we could go from a flat surface to a more wavy surface,” Kolle says. “In terms of mechanics, this indicates that membrane buckling is most likely the cause of the formation of these surprisingly ordered ridges.”
“We want to learn from nature, not only how these materials work, but also how they form,” says McDougal. “If you want to, for example, create a crinkled surface, which is useful for various applications, this gives you two very easy to adjust knobs, to tailor the way those surfaces are crinkled. You can either change the spacing of where this material is pinned, or you can change the amount of material you crop between pinned sections. And we saw that the butterfly uses these two strategies.
This research was supported in part by the International Human Frontier Science Program Organization, the National Science Foundation, the Humboldt Foundation, and the Alfred P. Sloan Foundation.