A butterfly’s wing is covered in hundreds of thousands of tiny scales, like miniature shingles on a paper-thin roof. A single shell is as small as a speck of dust yet surprisingly complex, with a corrugated surface of ridges that help drain water, manage heat and reflect light to give a butterfly its signature glow.
MIT researchers have now captured the first moments during a butterfly’s metamorphosis as an individual shell 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 its chrysalis.
The team continuously imaged individual scales as they grew from the wing’s membrane. These images reveal for the first time how the initially smooth surface of a scale begins to wrinkle to form microscopic, parallel undulations. The wrinkle-like structures eventually grow into finely patterned ridges, which define the features of a mature scale.
The researchers found that the transition from shell to corrugated surface likely results from ‘buckling’ – a general mechanism that describes how a smooth surface wrinkles as it grows in a confined space.
“Buckling is an instability, which is something we as engineers generally don’t want,” 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 intricate, functional structures.”
The team is working to visualize more stages in butterfly wing growth, hoping this will provide clues for designing advanced functional materials in the future.
“Given the multifunctionality of butterfly scales, we hope to understand and mimic these processes, with the goal of sustainably designing and fabricating new functional materials. These materials would exhibit tailored optical, thermal, chemical, and mechanical properties for textiles, building surfaces, vehicles — basically any surface that needs to exhibit features dependent on micro- and nanoscale structure,” Kolle adds.
The team published their results in a study appearing today in the journal Cell reports natural sciencesThe study’s co-authors include first author and former MIT postdoc Jan Totz, joint first author and postdoc Anthony McDougal, doctoral student Leonie Wagner, former postdoc Sungsam Kang, professor of mechanical and biomedical engineering Peter So, professor of mathematics Jörn Dunkel, and professor of materials science and chemistry Bodo Wilts of the University of Salzburg.
A living transformation
In 2021, McDougal, Kolle and their colleagues developed an approach to continuously capture microscopic details of a butterfly’s wing growth during metamorphosis. Their method involved carefully cutting through the insect’s paper-thin pupa and peeling away a small square of cuticle to expose the growing wing membrane. They placed a small glass slide over the exposed area and then used a microscope technique developed by team member Peter So to capture continuous images of scales as they grew from the wing membrane.
They applied the method of observing Vanessa cardui, a butterfly commonly known as a Painted Lady, which the team chose because of its shell architecture, which is common to most lepidopteran species. They observed the Painted Lady’s scales growing along a wing membrane in precise, overlapping rows, like shingles on a roof. Those images provided scientists with the most continuous visualization of living butterfly wing scale growth on a microscale to date.
Image: Courtesy of the researchers
In their new study, the team used the same approach to target a specific time window 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 in a piece of corduroy, enable many of the functions of the wing scales.
Because little is known about how these ridges form, the MIT team wanted to capture the continuous formation of ridges in a living, developing butterfly and unravel the mechanisms behind ridge formation in the organism.
“We followed the development of the wing over 10 days and took thousands of measurements of how the surfaces of the scales of a single butterfly changed,” McDougal says. “We could see early on that the surface is quite flat. As the butterfly grows, the surface starts to rise up a little bit and then, around 41 percent of the way through development, we see this very regular pattern of fully popped up protoridges. This whole process happens over about five hours and lays the structural foundation for the subsequent expression of patterned ridges.”
Pinned down
What could be the cause of the first ridges emerging in a precisely aligned manner? The researchers suspected that buckling might play a role. Buckling is a mechanical process in which a material bends in on itself when subjected to compressive forces. For example, an empty soda can buckles when it is pressed down from above. A material can also buckle when it grows, is clamped or is fixed in place.
Scientists have noticed that as the cell membrane of a butterfly’s scale grows, it is effectively pinned down in certain places by actin bundles – long filaments that run beneath the growing membrane and act as a scaffold to support the scale as it takes shape. Scientists have hypothesized that actin bundles constrain a growing membrane, similar to ropes around an inflating hot air balloon. As the butterfly’s wing scale grows, they proposed, it would bulge between the underlying actin filaments, buckling in a way that forms the first, parallel ridges of a scale.
To test this idea, the MIT team looked at a theoretical model describing the general mechanics of buckling. They fed the model imagery, such as measurements of the height of a shell membrane at different early stages of development, and different spacings of actin bundles across a growing membrane. They then ran the model forward in time to see if the underlying principles of mechanical buckling would produce the same ridge patterns the team observed in the real butterfly.
“With this modeling we have shown that we can go from a flat surface to a more wavy surface,” says Kolle. “In terms of mechanics, this indicates that buckling of the membrane is most likely the cause of the formation of these amazingly ordered ridges.”
“We want to learn from nature, not only how these materials function, but also how they are formed,” says McDougal. “For example, if you want to create a wrinkled surface, which is useful for different applications, then this gives you two very simple knobs to adjust, to adjust how those surfaces are wrinkled. You can change the distance where that material is pinned , or you can change the amount of material you grow between the pinned parts. And we saw that the butterfly uses both 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.