Colour Change & Thermal Protection
in Chameleons
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PUBLICATIONS
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‣NATURE COMMUNICATIONS 6: 6368 (2015)
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United Living Colours of Phelsuma
BMC BIOLOGY (2013)
Skin Cracking in Crocodiles
Science (2013)
Figure| During excitation, background skin in male panther chameleons can shift from green to yellow and red vertical bars become brighter.
Photonic Crystals Cause
Active Colour Change in Chameleons
Chameleons form a highly derived monophyletic group of iguanian lizards that originated in post-Gondwanan Africa around 90 million years ago. Many chameleons, and panther chameleons (Furcifer pardalis) in particular, have the remarkable ability to exhibit complex and rapid colour changes during social interactions such as male contests or courtship. It is generally interpreted that these changes are due to dispersion/aggregation of pigment-containing organelles within dermal chromatophores. Combining microscopy, photometric videography and photonic band-gap modelling, we show that chameleons shift colour through active tuning of a lattice of guanine nanocrystals within a superficial thick layer of dermal iridophores. In addition, we show that a deeper population of iridophores with larger crystals reflects a substantial proportion of the sunlight power, especially in the near-infrared range. The organisation of iridophores into two superposed layers constitutes an evolutionary novelty for chameleons that allows some species to combine efficient camouflage with spectacular display, while providing passive thermal protection.
Figure| Iridophore types in panther chameleons. Left panel: Cross-section of chameleon skin showing the epidermis (ep), and two thick layers of iridophores; scale= 20 μm. Right panels: TEM images of guanine nanocrystals in S-iridophores and 3D model of an FCC lattice (shown in two orientations) and TEM image of guanine nanocrystals in D-iridophores; scale= 200 nm.
Figure | In-vivo skin colour change in chameleons is reproduced ex-vivo. Left panels: TEM images of the lattice of guanine nanocrystals in S-iridophores from the same individual in a relaxed and excited state (two biopsies separated by a distance <1cm, scale: 200 nm). Right panels: This transformation and corresponding optical response is recapitulated ex-vivo by manipulation of skin osmolarity: time evolution of the colour of a single iridophore cell exhibits a strong blue shift as observed in vivo during behavioural colour change. Note that increased osmotic pressure corresponds to behavioural relaxation, hence, the reverse order of red to green to blue time evolution in comparison to in-vivo excitation (left panel above and top of page).
Figure | In-vivo skin colour change in chameleons is reproduced in-silico. Using band-gap modelling of the photonic crystal optical response, we simulated numerically the colours generated by an FCC lattice of close-packed guanine crystals for a fixed crystal size and a range of lattice parameter (distance) values measured on TEM images of various excited and un-excited male panther chameleon skin samples of different colours. The irreducible Brillouin zone was meshed and the photonic band structure was computed for each vertex. In the figure above, variation of simulated colour photonic response is shown for each vertex of the irreducible first Brillouin zone using four lattice parameter values of the modelled photonic crystal. Since no preferential orientation of crystals relative to skin surface was observed in S-iridophores, we also computed the average colour among all directions (indicated outside of the Brillouin zone). These simulated colours closely match those observed in vivo and during osmotic pressure experiments.
Photonic Crystals Cause
Thermal Protection in Chameleons
Figure | Iridophore types in lizards and function of D-iridophores in chameleons. In addition to panther chameleons, other chameleonidae (left panels) exhibit two superposed layers of (S- and D-) iridophores, whereas other lizards (right panels) such as agamids (the sister-group to chameleons) and gekkonids have a single-type iridophore layer. Scale: 500 nm. Check the original article for discovering the mechanisms by which D-iridophores provide chameleonid species with improved resistance to high sunlight exposure.
Supplementary Movies
All movies are available on the Nature Communications website as well as on the ‘EpiPhysX’ YouTube channel.
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Supplementary Movie S1 - In vivo colour change in a F. pardalis adult male under excitation upon presentation of another adult male in its vision field. The original video is stabilised and accelerated 8 times. The first frame of the movie is shown in the lower-right for a better visualisation of the extend of colour change. -
Supplementary Movie S2 - Colour change is fully reversible: in vivo colour change in a F. pardalis adult male under relaxation after a male-male combat. Males are much less mobile after than during a combat such that the movie is much more stable. The original video is accelerated 8 times. The first frame of the movie is shown in the lower-left for a better visualisation of the extend of colour change.
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Supplementary Movie S3 - In vivo colour change in a F. pardalis adult male under excitation upon presentation of another adult male in its vision field. The original video is stabilised and accelerated 3 times. The first frame of the movie is shown in the upper-right for a better visualisation of the extend of colour change. Note that this male is dominated by the male in its vision field, hence, colour change is mild.
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Supplementary Movie S4 - Ex vivo colour change of an adult male F. pardalis white skin sample induced by increasing osmolarity of the medium from 236 mOsm to 944 mOsm. The original video is accelerated 30x. The inset shows a 10x magnification of a single cell. This experiment indicates that individual S-iridophores experience a gradual shift in colour across the whole visible spectrum.
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Supplementary Movie S5 - Simulation of RGB colour shift at the surface of the first Brillouin zone of the FCC lattice of S-iridophores when gradually reducing the crystal lattice parameter (a) from 480 to 233 nm. The simulated colours closely match those observed in vivo (Figure 1b in main text, Supplementary Movies 1-3) and during osmotic shock experiments (Figure 2c in main text, Supplementary Movie 4).
Publications
Please, consult the full publication below for references & much additional information.
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✓Teyssier J., Saenko S.V., van der Marel D. & M.C. Milinkovitch.
Photonic Crystals Cause Active Colour Change in Chameleons
Nature Communications 6: 6368 (2015) -
Supporting Information (Suppl Figs 1-4, Suppl Table 1, Suppl Text and Refs) -
Coverage
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Contact: michel.milinkovitch@unige.ch
Other related publications
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✓Saenko S., Teyssier J., van der Marel D. & M. C. Milinkovitch
Precise colocalization of interacting structural and pigmentary elements generates extensive color pattern variation in Phelsuma lizards
BMC Biology 2013, 11: 105 -
✓Grbic D., Saenko S.V., Randriamoria T.M., Debry A., Raselimanana A.P. & M.C. Milinkovitch.
Phylogeography and Support Vector Machine Classification of Colour Variation in Panther Chameleons
Molecular Ecology (2015) 24, 3455–3466 -
Additional File 1 (Additional Discussion, Tables S1-S4, Figs. S1-S6).
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Crocodile Head Scales Are Not Developmental Units But Emerge from Physical Cracking
Science 339, 78 (2013) -- DOI: 10.1126/science.1226265
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✓Tzika A.C., Helaers R., Schramm G. & M. C. Milinkovitch
Reptilian-transcriptome v1.0, a glimpse in the brain transcriptome
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