Lizards exploit the changing optics of developing chromatophore cells to switch defensive colors during ontogeny

Author:

Zhang Gan1ORCID,Yallapragada Venkata Jayasurya23ORCID,Halperin Topaz45ORCID,Wagner Avital1ORCID,Shemesh Michal4ORCID,Upcher Alexander6ORCID,Pinkas Iddo7ORCID,McClelland Harry L. O.8ORCID,Hawlena Dror4ORCID,Palmer Benjamin A.1ORCID

Affiliation:

1. Department of Chemistry, Ben-Gurion University of the Negev, Be’er Sheva 8410501, Israel

2. Department of Physics of Complex Systems, Weizmann Institute of Science, Rehovot 7610001, Israel

3. Department of Physics, Indian Institute of Technology Kanpur, Kanpur, Uttar Pradesh 208016, India

4. Department of Ecology, Evolution and Behavior, The Hebrew University of Jerusalem, Jerusalem 91904, Israel

5. Department of Philosophy, The Hebrew University of Jerusalem, Jerusalem 9190501, Israel

6. Ilse Katz Institute for Nanoscale Science & Technology, Ben-Gurion University of the Negev, Be’er Sheva 8410501, Israel

7. Chemical Research Support, Weizmann Institute of Science, Rehovot 7610001, Israel

8. School of Geography, Earth and Atmospheric Sciences, University of Melbourne, Parkville, VIC 3053, Australia

Abstract

Many animals undergo changes in functional colors during development, requiring the replacement of integument or pigment cells. A classic example of defensive color switching is found in hatchling lizards, which use conspicuous tail colors to deflect predator attacks away from vital organs. These tail colors usually fade to concealing colors during ontogeny. Here, we show that the ontogenetic blue-to-brown tail color change in Acanthodactylus beershebensis lizards results from the changing optical properties of single types of developing chromatophore cells. The blue tail colors of hatchlings are produced by incoherent scattering from premature guanine crystals in underdeveloped iridophore cells. Cryptic tail colors emerge during chromatophore maturation upon reorganization of the guanine crystals into a multilayer reflector concomitantly with pigment deposition in the xanthophores. Ontogenetic changes in adaptive colors can thus arise not via the exchange of different optical systems, but by harnessing the timing of natural chromatophore development. The incoherent scattering blue color here differs from the multilayer interference mechanism used in other blue-tailed lizards, indicating that a similar trait can be generated in at least two ways. This supports a phylogenetic analysis showing that conspicuous tail colors are prevalent in lizards and that they evolved convergently. Our results provide an explanation for why certain lizards lose their defensive colors during ontogeny and yield a hypothesis for the evolution of transiently functional adaptive colors.

Funder

EC | European Research Council

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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