Precise colocalization of interacting structural and pigmentary elements generates extensive color pattern variation in Phelsumalizards

Abstract

BackgroundColor traits in animals play crucial roles in thermoregulation, photoprotection, camouflage, and visual communication, and are amenable to objective quantification and modeling. However, the extensive variation in non-melanic pigments and structural colors in squamate reptiles has been largely disregarded. Here, we used an integrated approach to investigate the morphological basis and physical mechanisms generating variation in color traits in tropical day geckos of the genus Phelsuma.ResultsCombining histology, optics, mass spectrometry, and UV and Raman spectroscopy, we found that the extensive variation in color patterns within and among Phelsuma species is generated by complex interactions between, on the one hand, chromatophores containing yellow/red pteridine pigments and, on the other hand, iridophores producing structural color by constructive interference of light with guanine nanocrystals. More specifically, we show that 1) the hue of the vivid dorsolateral skin is modulated both by variation in geometry of structural, highly ordered narrowband reflectors, and by the presence of yellow pigments, and 2) that the reflectivity of the white belly and of dorsolateral pigmentary red marks, is increased by underlying structural disorganized broadband reflectors. Most importantly, these interactions require precise colocalization of yellow and red chromatophores with different types of iridophores, characterized by ordered and disordered nanocrystals, respectively. We validated these results through numerical simulations combining pigmentary components with a multilayer interferential optical model. Finally, we show that melanophores form dark lateral patterns but do not significantly contribute to variation in blue/green or red coloration, and that changes in the pH or redox state of pigments provide yet another source of color variation in squamates.ConclusionsPrecisely colocalized interacting pigmentary and structural elements generate extensive variation in lizard color patterns. Our results indicate the need to identify the developmental mechanisms responsible for the control of the size, shape, and orientation of nanocrystals, and the superposition of specific chromatophore types. This study opens up new perspectives on Phelsuma lizards as models in evolutionary developmental biology.

The ocelli of Archaeognatha (Hexapoda): Functional morphology, pigment migration and chemical nature of the reflective tapetum

“…6) encountered in the ocelli of M. hrabei is similar to the unidentified blue pigment spectra in chameleons (Teyssier et al, 2015) and the red and green pigment spectra in lizards (Saenko et al, 2013). They, in turn, resemble the Raman spectra of xanthopterin and isoxanthopterin (Saenko et al, 2013;Feng et al, 2001). There is little correspondence with the Raman spectra of melanin, carotene and the simulated spectrum of the ommochrome ommin (Hsiung et al, 2015).…”

“…Raman spectra of pigments from dark blue skin melanophores of panther chameleons (Teyssier et al, 2015) and red skin erythrophores of the lizard Phelsuma lineata (Saenko et al, 2013) exhibit two similar peaks, but the region around 1600 cm −1 is different. The spectrum of melanin from dark-brown chameleon skin melanophores (Teyssier et al, 2015) only shows a single broad peak around 1580 cm…”

Variation in Display Behavior, Ornament Morphology, Sexual Size Dimorphism, and Habitat Structure in the Fan-Throated Lizard (Sitana, Agamidae)

“…S5 for examples; K¨astle, 1998). In light of recent research on the complex physiologies underlying color production and change in lizards (Saenko et al, 2014;Teyssier et al, 2015), and comprehensive frameworks for the analysis of coloration in natural populations (Kemp et al, 2015), FanThroated Lizards offer a veritable cornucopia to biologists interested in the physiological basis of coloration.…”

Structural colors: from natural to artificial systems

“…Saenko et al found that the extensive variation in WIREs Nanomedicine and Nanobiotechnology Structural colors color patterns within and among Phelsuma lizard species is generated by complex interactions between chromatophores containing yellow/red pteridine pigments and iridophores producing structural color by constructive interference of light with guanine nanocrystals. 43 These authors showed that the color patterns of Phelsuma always require precise colocalization of different sets of interacting pigmentary and structural elements. For example, yellow and red chromatophores are associated with iridophores with ordered and disordered nanocrystals, respectively.…”