It’s more of superpower than we thought

Marine Biological Laboratory

Like invisibility in legends, transparency in nature is a powerful tool. Most transparent animals live in the ocean, where a close visual match with the water renders them almost invisible to predators.

On land, transparency is rare and difficult to achieve, but some butterflies and moths (Lepidoptera) do have transparent wings. And a new study indicates transparency can serve not only to camouflage them, but in other cases to signal and warn predators, “Don’t eat me! I’m toxic.”

This flexible weapon for self-defense is one of many findings from a multiyear study spanning the physics, biology, ecology, and evolution of transparency in Lepidoptera conducted by several groups, including the lab of Nipam Patel, director of the Marine Biological Laboratory (MBL).

“This is one of those interdisciplinary studies you dream about, where you want to understand [a biological structure] from its physics to its development and ecology,” says Patel of the international study, which began as a project in the MBL Embryology course and ended up being funded by the Human Frontier Science Program. Ph.D. candidate Aaron Pomerantz in Patel’s lab is also on the team.

Mimicry for Self-Defense

The group’s latest paper adds a unique perspective on Lepidoptera self-defense. In some species, vivid wing coloration indicates the presence of chemical defenses that make the butterfly unpalatable or toxic, and predators learn to avoid them. Accordingly, palatable species can evolve to mimic the toxic ones, so predators leave them alone, too. In addition, multiple unpalatable species may converge in their warning colorations, thereby sharing in the benefits of the warning coloration process. Large “mimicry rings” can even form containing both toxic and nontoxic species, all displaying strikingly similar patterns and color combinations.

“The most amazing place to see this is the Amazon,” Patel says. “You’ll find a group of species that are distantly related to each other, yet they’ve all converged on a similar wing pattern.”

Surprisingly, mimicry rings have also been found among clear-wing species in the Amazon. “So we asked, ‘Wait, why would a species be transparent and unpalatable at the same time?'” Patel says. And, structurally, how would a clear-wing species accomplish that trick?

The team looked at the optical and structural properties of transparent butterfly wings within mimicry rings to see if they were convergent, and found in some rings, they were.

“In one transparency ring we studied (see photo 1, middle row), the key unpalatable butterfly doesn’t have an anti-glare coating on its transparent wing, so in sunlight, it’s really easy to see,” Patel says. “It may be signaling a warning pattern to predators when it’s in bright sun, and it’s camouflaged when in shadows. So it kind of cheats: it has the best of both worlds.”

Previously, the team reported on the developmental origins of transparency in a clear-wing species, Greta oto. They also compared wing transparency across 123 Lepidoptera species for its structural basis, optical properties, and biological relevance in relation to concealment, thermoregulation, and protection against UV. Those results showed a wide diversity of solutions to achieve transparency, suggesting that transparency has likely evolved multiple times independently.

Approaching transparency from multiple disciplines brought emergent knowledge and interesting new questions, Patel said. “Now that we’ve identified different Lepidoptera groups that have found different ways to achieve transparency, we can ask, how did they actually do this? Or, alternatively, if two very distant lineages have come up with the same solution for transparency, did they solve the problem in the same way?”

In addition to the MBL, collaborators in the initiative include scientists from the University of California, Berkeley; University of Chicago; California Institute of Technology; CNRS, France; Muséum National d’Histoire Naturelle, France; Sorbonne Université, Paris, France; Université des Antilles, France; Ecole Pratique des Hautes Etudes, France; Ministère de la Culture, France; and Université de Montpellier, France.

References:

  1. Charline Sophie Pinna, Maëlle Vilbert, Stephan Borensztajn, Willy Daney de Marcillac, Florence Piron-Prunier, Aaron Pomerantz, Nipam H Patel, Serge Berthier, Christine Andraud, Doris Gomez, Marianne Elias. Mimicry can drive convergence in structural and light transmission features of transparent wings in Lepidoptera. eLife, 2021; 10 DOI: 10.7554/eLife.69080
  2. Doris Gomez, Charline Pinna, Jonathan Pairraire, Mónica Arias, Jérôme Barbut, Aaron Pomerantz, Willy Daney de Marcillac, Serge Berthier, Nipam Patel, Christine Andraud, Marianne Elias. Wing transparency in butterflies and moths: structural diversity, optical properties, and ecological relevance. Ecological Monographs, 2021; 91 (4) DOI: 10.1002/ecm.1475
  3. Aaron F. Pomerantz, Radwanul H. Siddique, Elizabeth I. Cash, Yuriko Kishi, Charline Pinna, Kasia Hammar, Doris Gomez, Marianne Elias, Nipam H. Patel. Developmental, cellular, and biochemical basis of transparency in clearwing butterflies. Journal of Experimental Biology, 2021; DOI: 10.1242/jeb.237917

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