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Diverse set of Turing nanopatterns coat corneae across insect lineages

  1. Vladimir L. Katanaevc,e,1
  1. aInstitute of Protein Research, Russian Academy of Sciences, 142290 Pushchino, Russian Federation;
  2. bInstitute of Mathematical Problems of Biology, Russian Academy of Sciences, 142290 Pushchino, Russian Federation;
  3. cDepartment of Pharmacology and Toxicology, Faculty of Biology and Medicine, University of Lausanne, 1005 Lausanne, Switzerland;
  4. dDepartment of Entomology, Faculty of Biology, Lomonosov Moscow State University, 119234 Moscow, Russian Federation;
  5. eSchool of Biomedicine, Far Eastern Federal University, Vladivostok, Russian Federation
  1. Edited by Jeremy Nathans, Johns Hopkins University, Baltimore, MD, and approved July 17, 2015 (received for review March 23, 2015)

Significance

Corneal surfaces of some insects are coated with nipple-like nanostructures reducing the light reflection. Here we provide an extensive analysis of corneae across insect groups. Using atomic force microscopy, we discover a striking diversity of corneal nanocoatings, omnipresent in arthropods. These fascinating bionanostructures replicate the complete set of the Turing patterns—shapes resulting from the reaction−diffusion modeling underlying many examples of patterning in biological and physicochemical systems. Our work, verging on the interface of nanotechnology and zoology, evolution and biophysics, and ecology and genetics, sheds light on the molecular origin and evolutionary diversification of a beautiful diversity of insect corneal nanostructures. It also describes, to our knowledge, the first-ever biological example of Turing nanopatterns.

Abstract

Nipple-like nanostructures covering the corneal surfaces of moths, butterflies, and Drosophila have been studied by electron and atomic force microscopy, and their antireflective properties have been described. In contrast, corneal nanostructures of the majority of other insect orders have either been unexamined or examined by methods that did not allow precise morphological characterization. Here we provide a comprehensive analysis of corneal surfaces in 23 insect orders, revealing a rich diversity of insect corneal nanocoatings. These nanocoatings are categorized into four major morphological patterns and various transitions between them, many, to our knowledge, never described before. Remarkably, this unexpectedly diverse range of the corneal nanostructures replicates the complete set of Turing patterns, thus likely being a result of processes similar to those modeled by Alan Turing in his famous reaction−diffusion system. These findings reveal a beautiful diversity of insect corneal nanostructures and shed light on their molecular origin and evolutionary diversification. They may also be the first-ever biological example of Turing nanopatterns.

Footnotes

  • 1To whom correspondence may be addressed. Email: vladimir.katanaev{at}unil.ch or bswin2000{at}gmail.com.
  • Author contributions: V.L.K. designed research; A.B., A.S., and M.K. performed research; A.S. and Y.L. contributed new reagents/analytic tools; A.B., A.S., M.K., and V.L.K. analyzed data; and A.B. and V.L.K. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1505748112/-/DCSupplemental.

Freely available online through the PNAS open access option.

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