Precise colocalization of interacting structural and pigmentary elements generates extensive color pattern variation in Phelsumalizards
© Saenko et al.; licensee BioMed Central Ltd. 2013
Received: 16 August 2013
Accepted: 2 October 2013
Published: 7 October 2013
Color 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.
Combining 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.
Precisely 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.
KeywordsPhysics of biology Structural colors Pigmentary colors Color patterns Iridophores Chromatophores Reptiles Lizards Phelsuma
Vertebrate skin coloration provides a promising model system for exploring the link between genotypes and phenotypes in an ecological and phylogenetic framework. Indeed, color traits play crucial roles in thermoregulation, photoprotection, camouflage, and visual communication [1–4], and can vary extensively among and within species and populations. Moreover, colors and color patterns are amenable to objective quantification and modeling, providing an opportunity for integrated analyses of phenotypic variation. In particular, non-mammalian vertebrates, for example, squamates (lizards and snakes), exhibit a broad range of pigmentary and structural colors, generated by different types of chromatophores. In addition to melanophores, which produce black/brown melanins, squamates develop xanthophores and erythrophores, containing yellow and red pigments, respectively. These pigments are typically either pteridines, which are synthesized in situ from guanosine triphosphate, or carotenoids, which are metabolized from food in the liver and transported to skin via the circulatory system [5, 6]. Squamates additionally possess iridophores, which do not contain any pigment but generate structural coloration through interference of light waves with transparent guanine nanocrystals [7–9]. The spatial arrangement of all these cell types generates a broad range of colors and color patterns.
Despite such a high potential for complexity and diversity, lizards and snakes remain relatively under-represented in evolutionary developmental studies in general , and in analyses of color-pattern evolution in particular (for example, in comparison with other vertebrates or insects) [3, 4, 11, 12]. Although chromatophores have been described in some squamates [8, 9, 13–16], and their melanin pathway has been associated with adaptive color variation [17, 18], few data are available on the mechanisms that generate extensive variation in non-melanic pigments and structural colors in this lineage. The presence of such a variety of colors in squamates makes them appropriate models for investigating the essentially unknown genetic, developmental, and physical mechanisms generating a diversity of phenotypes through interactions between different types of chromatophores.
Here, we used an integrated approach that combines histology, Raman and UV spectroscopy, mass spectrometry (MS), optics, and numerical simulations to investigate the morphological basis and the physical mechanisms generating variation in color traits in five representative tropical day gecko species of the genus Phelsuma. More specifically, we show that 1) the reflectivity of the white belly, and of the dorsal pigmentary red spots and stripes, is increased by underlying, structurally disorganized broadband reflectors, whereas 2) the hue of the vivid dorsolateral background coloration is generated by structural, highly ordered narrowband reflectors, and is modulated both by the photonic crystal geometry and by a layer of yellow pigments. Most importantly, we show that these interactions require precise colocalization of red and yellow pigment cells with iridophores characterized by different organizations of nanocrystals.
Results and discussion
Melanophores generate dark lateral spots and stripes
The skin of all geckos studied here, regardless of color, contains two types of melanophores (Figure 2a): small light-brown cells that, when associated with iridophores, form ‘dermal chromatophore units’ , and large dark-brown cells at the base of the dermis. The former are dendritic cells with processes extending through the layer of iridophores for translocation of melanin granules in response to hormones, resulting in darkening of the skin [9, 22]. For example, the melanophore processes cover the iridophores in the dorsal skin of P. klemmeri, giving it a light-brown appearance. Moreover, in dark-brown lateral spots and stripes of P. klemmeri, P. quadriocellata, and P. lineata, small melanophores are abundant on top of iridophores, that is, in the layer typically occupied by xanthophores or erythrophores in other parts of the body (Figure 2a). In P. lineata, melanophores are found in combination with red erythrophores in the red-brown regions of the lateral stripes. Hence, in addition to their likely involvement in darkening of the skin, the small melanophores form dark lateral spots/stripes in some Phelsuma geckos, whereas the larger and darker melanophores might protect the deeper layers from harmful UV radiation . However, the homogeneous distribution of these two types of chromatophores in the skin of any color suggests that neither of them substantially contribute to color variation in Phelsuma geckos.
Pteridins contribute to red and green colors of dorsolateral skin
We could dissolve in NH4OH (but not in acetone) both the red and yellow pigments, found respectively in red-skin erythrophores and green-skin xanthophores (Figure 2b). This indicates that both pigments belong to the pteridine class rather than to the carotenoid class [23, 24]. We confirmed these findings by Raman spectroscopy and UV spectroscopy/MS (see Additional file 1). The Raman spectra (see Additional file 1: Figure S1) of both yellow xanthophores and red erythrophores in P. quadriocellata, P. lineata, and P. laticauda are similar to that of xanthopterin , a known pigment in squamates . Conversely, although the Raman spectrum of yellow xanthophores in P. grandis also indicates xanthopterin, the spectrum obtained for the red erythrophores in this species is significantly different, suggesting the presence of other molecules.
We then performed UV chromatography/MS on pigments extracted from the red and green skin of P. quadriocellata, P. lineata, and P. grandis, and compared their spectra with those of available pteridin standards. We confirmed the presence of xanthopterin in the yellow chromatophores of P. grandis, and in both the yellow and red chromatophores of P. lineata. We also identified biopterin in the yellow and red chromatophores of P. quadriocellata and in the red chromatophores of P. grandis, and identified sepiapterin in the yellow chromatophores of P. grandis. Finally, we found three unidentified molecules (probably pterins, based on their UV absorption spectra (see Additional file 1: Figure S2)) in all three species. It is, however, unclear which components contribute most substantially to the final pigmentary colors of the skin.
Remarkably, although pigment compositions differ substantially between P. lineata and P. quadriocellata, the pigment compositions of xanthophores and erythrophores are identical within a species (see Additional file 1: Figure S2a), strongly suggesting that the actual in vivo colors of these chromatophores (red or yellow) are determined by some other factors, such as the pH of the cellular environment of the pigment (as is the case for plant anthocyanins ) or the redox state of the pigment molecules (as has been shown for ommochromes in dragonflies ). Supporting this hypothesis, the red color of dorsal skin changed to yellow when we lowered the pH of, or added an oxidant (NaNO2) to, the skin of P. quadriocellata or P. lineata, respectively (Figure 2c). Even though the exact in vivo processes generating variation in the pH or redox states are unknown, these results indicate that these mechanisms provide an additional source of color variation in squamates.
Ordered multilayer interference reflectors generate structural blue or green
Geometric parameters of guanine crystals in Phelsuma species
Orientation A/y 0 (FWHM)a
Crystal height, nmb
Crystal spacing, nmb
Orientation A/y 0 (FWHM)
Crystal height, nm
Crystal length, nm
Orientation A/y 0 (FWHM)
Crystal height, nm
Crystal length, nm
P. grandis (1)
80.8 ± 12.2/ 78.5 ± 10.9c
96.0 ± 20.8/ 104.7 ± 25.5c
84 ± 44
173 ± 84
68 ± 34
128 ± 70
P. grandis (2)
81.0 ± 12.9
84.9 ± 22.7
78 ± 39
169 ± 96
67 ± 33
124 ± 82
P. grandis (3)
79.4 ± 10.7
99.2 ± 10.6
75 ± 36
171 ± 91
71 ± 37
130 ± 73
82.5 ± 11.4
97.3 ± 12.6
71 ± 41
194 ± 140
75 ± 42
154 ± 87
70.0 ± 22.7
37.9 ± 13.8
84 ± 42
209 ± 126
69 ± 41
171 ± 103
68.0 ± 10.8
93.2 ± 26.3
72 ± 47
265 ± 209
74.0 ± 11.1
109.6 ± 21.8
94 ± 57
226 ± 137
68 ± 43
170 ± 107
To further test experimentally if the multilayer is responsible for the structural color component of blue/green skin in Phelsuma, we applied mechanical or osmotic pressure to modify the distance between the guanine nanocrystal layers and therefore induce changes in structural coloration . We found that mechanical pressure or dehydration applied to de-pigmented green skin (hence, exhibiting structural green) resulted in a shift to structural dark blue (Figure 2e; see Additional files 3 and 4: supplementary movies). Note that complete dehydration made the layer of iridophores transparent, revealing the underlying melanophores (Figure 2e), because a severe decrease in crystal spacing either obliterates coherent interferences (that is, the entire stack of crystals behaves as a single block of guanine), or causes a shift in the reflectivity peak beyond the optical visible range, that is, below 390 nm.
Optical simulations of ordered multilayer interference match the reflectivities and colors produced by iridophores
The collaborative interplay between the structural and pigment components is illustrated (Figure 3b); we measured the reflectivity of green skin before and after yellow pigment removal (green and blue solid lines, respectively). The modeled reflectivity for an arbitrarily chosen crystal size (70 nm) and spacing (mean = 30 nm, SD = 13 nm), shown as dashed blue line, closely resembles the measured reflectivity of green skin after pigment removal. When a 3 μm yellow pigment layer is included in the model, the resultant reflectivity (Figure 3b, dashed green line) is a good match to the measured reflectivity of green skin before pigment removal. A similar reflectivity distribution (red line) was obtained as the direct product of the blue line with the measured normalized transmittance of the yellow pigment (orange dashed line). Hence, the green color of the skin is due to the structure-based blue reflection filtered by the yellow-transmitting pigment.
Optical systems based on multilayer interference usually show a spectral shift in reflectivity as the angle of the incident light changes . This angular dependence is determined by the refractive indices of the alternating layers, and the ratio between the optical paths at different angles (that is, path length × the refractive index of the medium) [31, 32]. Under very particular combinations of the refractive indices and thicknesses of its two components, a multilayer reflector can exhibit greatly reduced angular dependence . Only one of these conditions is met in Phelsuma geckos: the optical paths in low (n c d c ) and high (n g d g ) index layers are close, making the multilayer a narrowband optimal reflector as a result of the collaborative effects of crystal and spacing interferences. However, the iridescence in Phelsuma skin is much weaker than that predicted by the model (see Additional file 5: Figure S5a) because of another reason, namely, the variable orientation of iridophores in the skin reduces or annihilates iridescence by averaging the contributions from different cells (see Additional file 5: Figure S5b).
Incoherent scattering by disorganized crystals enhances the reflectivity of red dorsal and white ventral skin
Guanine crystals in iridophores of green and blue skin are well-organized, and therefore contribute extensively to the final background color of Phelsuma lizards. Remarkably, iridophores are also abundant in both the white ventral skin and red dorsal markings, but these cells are characterized by crystals with mostly random orientations and broad size distribution (Figure 2d; Table 1). This gives rise, as in some insects and fish [34–39], to incoherent scattering. In other words, in contrast to iridophores in blue/green skin, which generate a narrowband distribution of reflected frequencies, iridophores in white and red skin form broadband reflectors with overall reflectivity of similar intensity to that measured on coherently scattering structures (Figure 3c). Hence, these cells with disorganized guanine crystals not only produce the white color of the belly, but also significantly enhance the reflectivity, and therefore the visibility, of the red pigmentary patterns on the back. In the absence of iridophores, the red spots would appear less bright because much of the incident light would be absorbed by the underlying tissues. The mechanisms responsible for the distribution of ordered versus disordered crystals and for this spectacular colocalization of pigment cells with a particular type of iridophores are unknown.
Variation in skin coloration is explained by both structural and pigmentary components
Extensive variation in background coloration, and in dorsal and lateral color patterns, is present within and among species of the genus Phelsuma (Figure 1). Our analyses indicate that this variation is generated by a combination of features associated with pigmentary and structural color chromatophores (as previously reported in birds [40, 41]). The black lateral spots and stripes found in some species, and the light-brown background coloration of P. klemmeri, are due to melanophores occupying the upper layers of the dermis. Blue skin color is solely due to iridophores with well-organized guanine nanocrystals (that is, narrowband multilayer interference reflectors), whereas green skin is produced, depending on the species and the individual, either by structural green or by the interaction of structural blue with yellow pigments (xanthophores). Dorsal marks are formed by red erythrophores, the reflectivity of which is enhanced by iridophores with disorganized crystals (that is, broadband reflectors producing incoherent scattering). In addition, the hue produced by erythrophore and xanthophore pigments is pH-dependent or redox-dependent in some species. Most importantly, we show 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. This indicates the need to identify the developmental mechanisms responsible for the superposition of specific chromatophore types, opening up new perspectives for Phelsuma lizards as model organisms in evolutionary developmental biology.
We also show that the exact combination of parameters producing a given color is difficult to predict without experimental estimation of parameter values (such as, through electron-microscopy and spectroscopy analyses). Hence, exploring the genetic and developmental bases of phenotypic variation in ecologically important color traits in squamate reptiles will require integration of the structural and pigmentary color components and their interactions. The fact that red/yellow coloration in Phelsuma is based on pteridines, the synthesis of which is controlled by enzymes that have been well studied in model organisms , readily suggests candidate genes for this pigmentary aspect of color variation. Furthermore, although guanine crystal formation in iridophores is poorly understood, and the genetic determinants of variation in size, shape, and orientation of nanocrystals are virtually unknown, several enzymes associated with aberrant iridophore phenotypes [43, 44] are candidates for variation in structural coloration in Phelsuma.
Maintenance of, and experiments on, animals were approved by the Geneva Canton ethical regulation authority (authorization 1008/3421/1R) and performed in accordance with Swiss law.
Animals and phylogenetic mapping
Adult P. klemmeri (n = 1), P. quadriocellata (n = 1), P. lineata (n = 2), P. laticauda (n = 1), and P. grandis (n = 5) were obtained from the pet market or bred in our laboratory. On the phylogenetic tree of the genus Phelsuma[19, 20], we mapped (Figure 1a) the presence or absence of the following phenotypic characters (based on previous reports and our own observations [20, 45–50]): 1) dorsolateral background coloration; 2) red/brown dorsal pattern; and 3) black/brown lateral pattern. Most Phelsuma geckos exhibit a vivid dorsolateral coloration, with a background typically of one or more colors (for example, bright green, yellow, or turquoise-blue, but sometimes dull gray or brown). Almost all species have distinct dorsal marks consisting of red to brown spots and stripes of various shapes. In addition, some species have black/brown lateral stripes or spots.
Skin histology and TEM
Skin samples were placed in Ringer’s solution for microscopy observation. Cross-sections of 14 to 16 μm were prepared from skin embedded in optimum cutting temperature compound on a Leica (Wetzlar, Germany) CM1850 cryostat. For TEM, skin pieces of approximately 1 cm2 in size were fixed overnight at 4°C in 2% glutaraldehyde and 4% paraformaldehyde in 0.05 mol/L sodium cacodylate buffer (pH 7.4), rinsed with 0.1 mol/L cold sodium cacodylate, and fixed for 1.5 hours on ice in the same buffer with the addition of 1% osmium tetraoxide. Samples were then rinsed in water, stained with 1% uranyl acetate for 2 hours, gradually dehydrated in ethanol, rinsed three times in propylene oxide, incubated overnight in 1:1 propylene oxide/resin, and finally embedded in epoxy resin (Epon). Semi-thin (1 to 2 μm) and ultra-thin (80 to 90 nm) cross-sections were cut with a diamond knife on a Leica UCT microtome. Semi-thin sections were examined under a light microscope. Ultra-thin sections were placed on formavar-coated grids, and viewed with a Tecnai™ G2 Sphera (FEI) TEM at 120 kV to visualize intact guanine crystals, because post-staining inevitably results in loss of crystals . The grids were then post-stained with uranyl acetate and lead citrate, and viewed with the TEM again (in this case, spaces that were occupied by crystals appear white).
Optical modeling of skin reflectivity and color
For each individual, 10 to 20 TEM images of stained sections of iridophores of white, red, and green skin were collected at low (×1,500) magnification, and 20 to 30 images of unstained sections were collected at high (×25,000) magnification for green/blue skin. To analyze the size and orientation of crystals relative to skin surface, white ‘holes’ (corresponding to guanine crystals dissolved by uranyl acetate/lead citrate during post-staining) on low magnification images were fitted with ellipses (in JMicroVision ), whose geometric parameters (length, height, and orientation of major axis) were computed subsequently.
The A/y 0 ratio varies from zero (when A = 0 in a purely random system) to infinity (when A is high and y0 is close to zero in a perfectly ordered system) as schematically illustrated (see Additional file 2: Figure S3d).
For optical modeling in blue/green skin, the thickness of crystals and the spacing between well-aligned crystal layers were measured on images of unstained sections taken at ×25,000 magnification (Table 1; see Additional file 2: Table S3). These values were used in a multilayer model (see Additional file 2) that simulates the reflectivity and color produced by alternating layers of guanine crystals and cytoplasm, each with a different thickness and refractive index [14, 52, 53].
To account for the contribution of pigments to skin reflectivity and hue, a top layer of pigment with variable thickness and wavelength-dependent absorption was included in the model. The optical transmission of the pigments measured on skin cryosections was fitted to a Drude-Lorentz model and included in the multilayer (see Additional file 2). As the intensity of light reflected coherently by organized photonic structures is much more intense (reflectivity can be close to 1) than that reflected by incoherent scattering, the latter was not taken into account.
Pigment chemical analysis
To determine pigment composition in xanthophores and erythrophores, skin samples were treated with 100% acetone and 30% NH4OH, known to dissolve carotenoids and pteridins, respectively [23, 24]. MS was performed on pteridin standards (neopterin, isoxanthopterin, xanthopterin, pterin, 6-biopterin and sepiapterin) and on extracted pigments by UHPLC/DAD/ESI-QTOF (Agilent Technologies 1290 Infinity, ESI-QTOF model G6530A). A Poroshell C8 analytical column (100 × 3.0 mm internal diameter; particle size 2.7 μm) was used for the separation. The column oven temperature was set at 40°C. The binary mobile phase consisted of 0.4% acetic acid in water (solvent A) and acetonitrile (solvent B), and the flow rate was set to 0.5 ml/min. UV/visible spectra were recorded between 190 to 600 nm, and the injection volume was 1 μl. Mass spectra were acquired in positive and negative mode using electrospray ionization with nitrogen as the nebulizing gas, and recorded for the range of m/z 50 to 1700. Drying gas flow was 10 l/min, with a fragmentation voltage of 120 V, drying gas temperature of 300°C, nebulizer pressure of 40 psi, and capillary voltage of 3500 V. Compounds were identified with MassHunter Qualitative Analysis Software (Agilent Technologies) by analysis of their UV and high-resolution MS spectra (see Additional file 1).
Raman spectroscopy was performed on cryosections of red and green/yellow skin. This non-invasive technique  determines the chemical structure of a target molecule by measuring the energy shift of an incident laser light after its interaction with the molecule. The bespoke micro-Raman system was composed of a half-meter focal length spectrometer coupled to a nitrogen-cooled Princeton CCD detector. The excitation source was an argon laser with a wavelength of 514.5 nm. The full collection of Raman spectra on different pigments is shown (see Additional file 1).
For extended UV reflectivity measurements (300 to 800 nm), a probe (QR400-7-VIS/BX; Ocean Optics) was connected to the scanning Xenon source of a spectroscopic Woollam ellipsometer with silicon diode as detector. Lock-in detection was used for ambient light noise reduction. For monitoring color change in real time (see Additional files 3 and 4, movies) and for imaging of the skin samples (see Additional file 2: Table S3), a Thorlab color CCD camera was mounted on a Leica M125 stereo microscope with a high field depth. With CCD, a systematic underestimate of RGB numbers of about 5% (that is, darker colors) was seen, but the color balance was rendered correctly. During the mechanical pressure and dehydration experiments, skin color was measured in situ, and compared with simulations in which the distance between the crystals was the only adjusted parameter.
We thank Adrien Debry for technical assistance in captive breeding/animal handling; Elise Schubert for assistance in micro-colorimetry setup and color analyses; and Floriant Bellvert and Anne-Emmanuelle Hay-de Bettignies for assistance in mass spectrometry. Comments from two anonymous reviewers allowed us to improve the manuscript significantly. This work was supported by grants from the University of Geneva (Switzerland), the Swiss National Science Foundation (FNSNF, Sinergia grant CRSII3_132430 and grant 31003A_125060), the SystemsX.ch initiative (project EpiPhysX), the Georges and Antoine Claraz Foundation, and the Ernst and Lucie Schmidheiny Foundation.
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