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

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 ta...

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Autores principales: Zhang, Gan, Yallapragada, Venkata Jayasurya, Halperin, Topaz, Wagner, Avital, Shemesh, Michal, Upcher, Alexander, Pinkas, Iddo, McClelland, Harry L. O., Hawlena, Dror, Palmer, Benjamin A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10161005/
https://www.ncbi.nlm.nih.gov/pubmed/37104475
http://dx.doi.org/10.1073/pnas.2215193120
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author Zhang, Gan
Yallapragada, Venkata Jayasurya
Halperin, Topaz
Wagner, Avital
Shemesh, Michal
Upcher, Alexander
Pinkas, Iddo
McClelland, Harry L. O.
Hawlena, Dror
Palmer, Benjamin A.
author_facet Zhang, Gan
Yallapragada, Venkata Jayasurya
Halperin, Topaz
Wagner, Avital
Shemesh, Michal
Upcher, Alexander
Pinkas, Iddo
McClelland, Harry L. O.
Hawlena, Dror
Palmer, Benjamin A.
author_sort Zhang, Gan
collection PubMed
description 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.
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spelling pubmed-101610052023-05-06 Lizards exploit the changing optics of developing chromatophore cells to switch defensive colors during ontogeny Zhang, Gan Yallapragada, Venkata Jayasurya Halperin, Topaz Wagner, Avital Shemesh, Michal Upcher, Alexander Pinkas, Iddo McClelland, Harry L. O. Hawlena, Dror Palmer, Benjamin A. Proc Natl Acad Sci U S A Physical Sciences 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. National Academy of Sciences 2023-04-27 2023-05-02 /pmc/articles/PMC10161005/ /pubmed/37104475 http://dx.doi.org/10.1073/pnas.2215193120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Physical Sciences
Zhang, Gan
Yallapragada, Venkata Jayasurya
Halperin, Topaz
Wagner, Avital
Shemesh, Michal
Upcher, Alexander
Pinkas, Iddo
McClelland, Harry L. O.
Hawlena, Dror
Palmer, Benjamin A.
Lizards exploit the changing optics of developing chromatophore cells to switch defensive colors during ontogeny
title Lizards exploit the changing optics of developing chromatophore cells to switch defensive colors during ontogeny
title_full Lizards exploit the changing optics of developing chromatophore cells to switch defensive colors during ontogeny
title_fullStr Lizards exploit the changing optics of developing chromatophore cells to switch defensive colors during ontogeny
title_full_unstemmed Lizards exploit the changing optics of developing chromatophore cells to switch defensive colors during ontogeny
title_short Lizards exploit the changing optics of developing chromatophore cells to switch defensive colors during ontogeny
title_sort lizards exploit the changing optics of developing chromatophore cells to switch defensive colors during ontogeny
topic Physical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10161005/
https://www.ncbi.nlm.nih.gov/pubmed/37104475
http://dx.doi.org/10.1073/pnas.2215193120
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