Body coloration and mechanisms of colour production in Archelosauria: the case of deirocheline turtles
Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
31417734
PubMed Central
PMC6689573
DOI
10.1098/rsos.190319
PII: rsos190319
Knihovny.cz E-zdroje
- Klíčová slova
- Chelonia, Pseudemys concinna, Trachemys scripta, chromatophores, nanostructure, pigments,
- Publikační typ
- časopisecké články MeSH
Animal body coloration is a complex trait resulting from the interplay of multiple mechanisms. While many studies address the functions of animal coloration, the mechanisms of colour production still remain unknown in most taxa. Here we compare reflectance spectra, cellular, ultra- and nano-structure of colour-producing elements, and pigment types in two freshwater turtles with contrasting courtship behaviour, Trachemys scripta and Pseudemys concinna. The two species differ in the distribution of pigment cell-types and in pigment diversity. We found xanthophores, melanocytes, abundant iridophores and dermal collagen fibres in stripes of both species. The yellow chin and forelimb stripes of both P. concinna and T. scripta contain xanthophores and iridophores, but the post-orbital regions of the two species differ in cell-type distribution. The yellow post-orbital region of P. concinna contains both xanthophores and iridophores, while T. scripta has only xanthophores in the yellow-red postorbital/zygomatic regions. Moreover, in both species, the xanthophores colouring the yellow-red skin contain carotenoids, pterins and riboflavin, but T. scripta has a higher diversity of pigments than P. concinna. Trachemys s. elegans is sexually dichromatic. Differences in the distribution of pigment cell types across body regions in the two species may be related to visual signalling but do not match predictions based on courtship position. Our results demonstrate that archelosaurs share some colour production mechanisms with amphibians and lepidosaurs (i.e. vertical layering/stacking of different pigment cell types and interplay of carotenoids and pterins), but also employ novel mechanisms (i.e. nano-organization of dermal collagen) shared with mammals.
Zobrazit více v PubMed
Kleisner K. 2010. Re-semblance and re-evolution: paramorphism and semiotic co-option may explain the re-evolution of similar phenotypes. Sign Syst. Stud. 38, 378–392. (10.12697/sss.2010.38.1-4.13) DOI
Gould SJ, Vrba ES. 1982. Exaptation—a missing term in the science of form. Paleobiology 8, 4–15. (10.1017/S0094837300004310) DOI
Badyaev AV. 2004. Developmental perspective on the evolution of sexual ornaments. Evol. Ecol. Res. 6, 975–991.
Grether GF, Kolluru GR, Nersissian K. 2004. Individual colour patches as multicomponent signals. Biol. Rev. 79, 583–610. (10.1017/S1464793103006390) PubMed DOI
Eliason CM, Maia R, Shawkey MD. 2015. Modular color evolution facilitated by a complex nanostructure in birds. Evolution 69, 357–367. (10.1111/evo.12575) PubMed DOI
Eliason CM. 2018. How do complex animal signals evolve? PLoS Biol. 16, e3000093 (10.1371/journal.pbio.3000093) PubMed DOI PMC
Cuthill IC, et al. 2017. The biology of color. Science 357, eaan0221 (10.1126/science.aan0221) PubMed DOI
Shawkey MD, D'Alba L. 2017. Interactions between colour-producing mechanisms and their effects on the integumentary colour palette. Phil. Trans. R. Soc. B 372, 20160536 (10.1098/rstb.2016.0536) PubMed DOI PMC
Hall BK. 2008. The neural crest and neural crest cells in vertebrate development and evolution, 400 pp Boston, MA: Springer.
Jeffery WR, Strickler AG, Yamamoto Y. 2004. Migratory neural crest-like cells form body pigmentation in a urochordate embryo. Nature 431, 696–699. (10.1038/nature02975) PubMed DOI
Donoghue PCJ, Graham A, Kelsh RN. 2008. The origin and evolution of the neural crest. Bioessays 30, 530–541. (10.1002/bies.20767) PubMed DOI PMC
Schartl M, Larue L, Goda M, Bosenberg MW, Hashimoto H, Kelsh RN. 2016. What is a vertebrate pigment cell? Pigment Cell Melanoma Res. 29, 8–14. (10.1111/pcmr.12409) PubMed DOI
Bagnara JT, Matsumoto J, Ferris W, Frost SK, Turner WA, Tchen TT, Taylor JD. 1979. Common origin of pigment cells. Science 203, 410–415. (10.1126/science.760198) PubMed DOI
Sherbrooke WC, Frost SKV. 1989. Integumental chromatophores of a color-change, thermoregulating lizard, Phrynosoma modestum (Iguanidae, Reptilia). American Museum novitates, 2943, 14 p.
Prum RO, Morrison RL, Ten Eyck GR. 1994. Structural color production by constructive reflection from ordered collagen arrays in a bird (Philepitta castanea: Eurylaimidae). J. Morphol. 222, 61–72. (10.1002/jmor.1052220107) PubMed DOI
Saenko SV, Teyssier J, Van Der Marel D, Milinkovitch MC.. 2013. Precise colocalization of interacting structural and pigmentary elements generates extensive color pattern variation in Phelsuma lizards. BMC Biol. 11, 105 (10.1186/1741-7007-11-105) PubMed DOI PMC
Prum RO, Torres RH. 2004. Structural colouration of mammalian skin: convergent evolution of coherently scattering dermal collagen arrays. J. Exp. Biol. 207, 2157–2172. (10.1242/jeb.00989) PubMed DOI
Prum RO, Torres R. 2003. Structural colouration of avian skin: convergent evolution of coherently scattering dermal collagen arrays. J. Exp. Biol. 206, 2409–2429. (10.1242/jeb.00431) PubMed DOI
Moll EO, Matson KE, Krehbiel EB. 1981. Sexual and seasonal dichromatism in the Asian river turtle Callagur borneoensis. Herpetologica 37, 181–194.
Fujii R. 1993. Cytophysiology of fish chromatophores. In International review of cytology (eds KW Jeon, M Fredlander, J Jarvik), pp. 191–255. San Diego, CA: Academic Press.
Dufresne ER, Noh H, Saranathan V, Mochrie SGJ, Cao H, Prum RO. 2009. Self-assembly of amorphous biophotonic nanostructures by phase separation. Soft Matter 5, 1792–1795. (10.1039/b902775k) DOI
Crawford NG, Parham JF, Sellas AB, Faircloth BC, Glenn TC, Papenfuss TJ, Henderson JB, Hansen MH, Simison WB. 2015. A phylogenomic analysis of turtles. Mol. Phylogenet. Evol. 83, 250–257. (10.1016/j.ympev.2014.10.021) PubMed DOI
Vetter H, van Dijk PP. 2006. Terralog: Turtles of the World Vol. 4–East and South Asia. Chimaira, Frankfurt am Main. 160 p.
Vetter H. 2004. Terralog: Turtles of the World, Vol. 2, North America. Chimaira, Frankfurt am Main. 120 p.
Vetter H. 2011. Terralog: Turtles of the world Vol. 1: Africa, Europe and Western Asia (second edition). Chimaira, Frankfurt am Main. 152 pp.
Vetter H. 2005. Terralog: Turtles of the World, Vol. 3, Central and South America. Chimaira, Frankfurt am Main. 127 p.
Alibardi L. 2013. Observations on the ultrastructure and distribution of chromatophores in the skin of chelonians. Acta Zool. 94, 222–232. (10.1111/j.1463-6395.2011.00546.x) DOI
Steffen JE, Hultberg J, Drozda S. 2019. The effect of dietary carotenoid increase on painted turtle spot and stripe color. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 229, 10–17. (10.1016/j.cbpb.2018.12.002) PubMed DOI
Gopalakrishnakone P. 1986. The structure of the pigment cells in the turtle Trionyx sinensis. Arch. Histol. Jpn. 49, 421–435. (10.1679/aohc.49.421) PubMed DOI
Steffen JE, Learn KM, Drumheller JS, Boback SM, McGraw KJ. 2015. Carotenoid composition of colorful body stripes and patches in the painted turtle (Chrysemys picta) and red-eared slider (Trachemys scripta). Chelonian Conserv. Biol. 14, 56–63. (10.2744/ccab-14-01-56-63.1) DOI
Twyman H, Valenzuela N, Literman R, Andersson S, Mundy NI. 2016. Seeing red to being red: conserved genetic mechanism for red cone oil droplets and co-option for red coloration in birds and turtles. Proc. R. Soc. B 283, 20161208 (10.1098/rspb.2016.1208) PubMed DOI PMC
Odate S, Tatebe Y, Obika M, Hama T.. 1959. Pteridine derivatives in Reptilian skin. Proc. Jpn. Acad. 35, 567–570. (10.2183/pjab1945.35.567) DOI
Legler JM. 1990. The genus Pseudemys in Mesoamerica: taxonomy, distribution, and origins. In Life history and ecology of the slider turtle (ed. Gibbons JW.), pp. 82–105. Washington, DC: Smithsonian Institution Press.
Seidel ME, Ernst CH. 2017. A systematic review of the turtle family Emydidae. Vertebr. Zool. 67, 1–122.
Dominy AE. 2015. Modeling underwater visual ability and varied color expression in the diamondback terrapin (Malaclemys terrapin) in relation to potential mate preference by females. Drexel University. 102 p.
Bulté G, Germain RR, O'connor CM, Blouin-Demers G. 2013. Sexual dichromatism in the northern map turtle, Graptemys geographica. Chelonian Conserv. Biol. 12, 187–192. (10.2744/ccb-0995a.1) DOI
Rowe JW, Bunce CF, Clark DL. 2014. Spectral reflectance and substrate color-induced melanization in immature and adult Midland painted turtles (Chrysemys picta marginata). Amphibia-Reptilia 35, 149–159. (10.1163/15685381-00002934) DOI
Rowe JW, Gradel JR, Bunce CF, Clark DL. 2012. Sexual dimorphism in size and shell shape, and dichromatism of spotted turtles (Clemmys guttata) in Southwestern Michigan. Amphibia-Reptilia 33, 443–450. (10.1163/15685381-00002847) DOI
Endler JA, Thery M. 1996. Interacting effects of lek placement, display behavior, ambient light, and color patterns in three neotropical forest-dwelling birds. Am. Nat. 148, 421–452. (10.1086/285934) DOI
White TE, Zeil J, Kemp DJ. 2015. Signal design and courtship presentation coincide for highly biased delivery of an iridescent butterfly mating signal. Evolution 69, 14–25. (10.1111/evo.12551) PubMed DOI PMC
Simpson RK, McGraw KJ. 2018. It's not just what you have, but how you use it: solar-positional and behavioural effects on hummingbird colour appearance during courtship. Ecol. Lett. 21, 1413–1422. (10.1111/ele.13125) PubMed DOI
Liu Y, Davy CM, Shi H-T, Murphy RW. 2013. Sex in the half-shell: a review of the functions and evolution of courtship behavior in freshwater turtles. Chelonian Conserv. Biol. 12, 84–100. (10.2744/ccb-1037.1) DOI
Kramer M, Fritz U. 1989. Courtship of the turtle, Pseudemys nelsoni. J. Herpetol. 23, 84–86. (10.2307/1564324) DOI
Cagle FR. 1950. The life history of the slider turtle, Pseudemys scripta troostii (Holbrook). Ecol. Monogr. 20, 31–54. (10.2307/1943522) DOI
Jackson CG, Davis JD. 1972. Courtship display behavior of Chrysemys concinna suwanniensis. Copeia 1972, 385–387. (10.2307/1442510) DOI
Jackson CG Jr, Davis JD. 1972. A quantitative study of the courtship display of the red-eared turtle, Chrysemys scripta elegans (Wied). Herpetologica 28, 58–64.
Fritz U, Wilhelma Z-BG. 1999. Courtship behaviour and systematics in the subtribe Nectemydina 2. A comparison above the species level and remarks on the evolution of behaviour elements. Bullefin Chicago Herpetol. Soc. 11, 225–236.
Andersson S, Prager M. 2006. Quantifying colors. In Bird coloration, volume 1: mechanisms and measurements (eds Hill GE, McGraw KJ), pp. 41–89. Boston, MA: Harvard University Press.
Lovich JE, McCoy CJ, Garstka WR. 1990. The development and significance of melanism in the slider turtle. In Life history and ecology of the slider turtle (ed. Gibbons JW.), pp. 233–254. Washington, DC: Smithsonian Institution Press.
R Core Team. 2017. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Maia R, Eliason CM, Bitton P, Doucet SM, Shawkey MD. 2013. pavo: an R package for the analysis, visualization and organization of spectral data. Methods Ecol. Evol. 4, 906–913. (10.1111/2041-210x.12069) DOI
Montgomerie R. 2006. Analyzing colors. In Bird coloration, volume 1: mechanisms and measurements (eds Hill GE, McGraw KJ), pp. 90–147. Boston, MA: Harvard University Press.
Andersson S, Andersson M. 1998. Ultraviolet sexual dimorphism and assortative mating in blue tits. Proc. R. Soc. Lond. B 265, 445–450. (10.1098/rspb.1998.0315) DOI
Oksanen J, et al. 2015. vegan: Community Ecology Package. R package version 2.0-10. https://github.com/vegandevs/vegan .
Legendre P, Gallagher ED. 2001. Ecologically meaningful transformations for ordination of species data. Oecologia 129, 271–280. (10.1007/s004420100716) PubMed DOI
Brejcha J, Bataller J-V, Bosáková Z, Geryk J, Havlíková M, Kleisner K, Maršík P, Font E. 2019. Data from: Body coloration and mechanisms of colour production in Archelosauria: the case of deirocheline turtles Dryad Digital Repository. (10.5061/dryad.b68b048) PubMed DOI PMC
Rasband WS. 1997. ImageJ. Bethesda, MD: US National Institutes of Health.
Teyssier J, Saenko SV, Van Der Marel D, Milinkovitch MC.. 2015. Photonic crystals cause active colour change in chameleons. Nat. Commun. 6, 6368 (10.1038/ncomms7368) PubMed DOI PMC
Morrison RL. 1995. A transmission electron microscopic (TEM) method for determining structural colors reflected by lizard iridophores. Pigment Cell Melanoma Res. 8, 28–36. (10.1111/j.1600-0749.1995.tb00771.x) PubMed DOI
Haisten DC, Paranjpe D, Loveridge S, Sinervo B. 2015. The cellular basis of polymorphic coloration in common side-blotched lizards, Uta stansburiana. Herpetologica 71, 125–135. (10.1655/herpetologica-d-13-00091) DOI
Denton EJ, Land MF.. 1971. Mechanism of reflexion in silvery layers of fish and cephalopods. Proc. R. Soc. Lond. B 178, 43–61. (10.1098/rspb.1971.0051) PubMed DOI
Rohrlich ST, Porter KR. 1972. Fine structural observations relating to the production of color by the iridophores of a lizard, Anolis carolinensis. J. Cell Biol. 53, 38–52. (10.1083/jcb.53.1.38) PubMed DOI PMC
Prum RO, Torres RH. 2003. A Fourier tool for the analysis of coherent light scattering by bio-optical nanostructures. Integr. Comp. Biol. 43, 591–602. (10.1093/icb/43.4.591) PubMed DOI
The MathWorks Inc. 1996. MATLAB: Application program interface guide.
Adobe Systems Inc. 2005. Adobe Photoshop CS3.
Leonard DW, Meek KM. 1997. Refractive indices of the collagen fibrils and extrafibrillar material of the corneal stroma. Biophys. J. 72, 1382–1387. (10.1016/s0006-3495(97)78784-8) PubMed DOI PMC
Briggs WL, Henson VE. 1995. The DFT. An owner's manual. Philadelphia, PA: SIAM.
Benedek GB. 1971. Theory of transparency of the eye. Appl. Opt. 10, 459–473. (10.1364/ao.10.000459) PubMed DOI
Krajíček J, Kozlík P, Exnerová A, Štys P, Bursová M, Čabala R, Bosáková Z. 2014. Capillary electrophoresis of pterin derivatives responsible for the warning coloration of Heteroptera. J. Chromatogr. A 1336, 94–100. (10.1016/j.chroma.2014.02.019) PubMed DOI
Ferré J, Silva FJ, Real MD, Ménsua JL. 1986. Pigment patterns in mutants affecting the biosynthesis of pteridines and xanthommatin in Drosophila melanogaster. Biochem. Genet. 24, 545–569. (10.1007/bf00504334) PubMed DOI
Kozlík P, Krajíček J, Kalíková K, Tesařová E, Čabala R, Exnerová A, Štys P, Bosáková Z. 2013. Hydrophilic interaction liquid chromatography with tandem mass spectrometric detection applied for analysis of pteridines in two Graphosoma species (Insecta: Heteroptera). J. Chromatogr. B 930, 82–89. (10.1016/j.jchromb.2013.05.004) PubMed DOI
Andrade P, et al. 2019. Regulatory changes in pterin and carotenoid genes underlie balanced color polymorphisms in the wall lizard. Proc. Natl Acad. Sci. USA 116, 5633–5642. (10.1101/481895) PubMed DOI PMC
Matsumoto J. 1965. Studies on fine structure and cytochemical properties of erythrophores in swordtail, Xiphophorus helleri, with special reference to their pigment granules (pterinosomes). J. Cell Biol. 27, 493–504. (10.1083/jcb.27.3.493) PubMed DOI PMC
Obika M. 1993. Formation of pterinosomes and carotenoid granules in xanthophores of the teleost Oryzias latipes as revealed by the rapid-freezing and freeze-substitution method. Cell Tissue Res. 271, 81–86. (10.1007/bf00297544) DOI
Ernst CH, Barbour RW. 1989. Turtles of the world, 416 pp Washington, DC: Smithsonian Institution Press.
Lindgren J, et al. 2015. Molecular composition and ultrastructure of Jurassic paravian feathers. Sci. Rep. 5, 13520 (10.1038/srep13520) PubMed DOI PMC
Manning PL, et al. 2013. Synchrotron-based chemical imaging reveals plumage patterns in a 150 million year old early bird. J. Anal. At. Spectrom. 28, 1024–1030. (10.1039/c3ja50077b) DOI
Li Q, Gao KQ, Vinther J, Shawkey MD, Clarke JA, D'Alba L, Meng Q, Briggs DE, Prum RO. 2010. Plumage color patterns of an extinct dinosaur. Science 327, 1369 (10.1126/science.1186290) PubMed DOI
Li Q, et al. 2012. Reconstruction of Microraptor and the evolution of iridescent plumage. Science 335, 1215–1219. (10.1126/science.1213780) PubMed DOI
Lingham-Soliar T, Plodowski G. 2010. The integument of Psittacosaurus from Liaoning Province, China: taphonomy, epidermal patterns and color of a ceratopsian dinosaur. Naturwissenschaften 97, 479–486. (10.1007/s00114-010-0661-3) PubMed DOI
Vinther J, Nicholls R, Lautenschlager S, Pittman M, Kaye TG, Rayfield E, Mayr G, Cuthill IC. 2016. 3D camouflage in an ornithischian dinosaur. Curr. Biol. 26, 2456–2462. (10.1016/j.cub.2016.06.065) PubMed DOI PMC
Hu D, et al. 2018. A bony-crested Jurassic dinosaur with evidence of iridescent plumage highlights complexity in early paravian evolution. Nat. Commun. 9, 217 (10.1038/s41467-017-02515-y) PubMed DOI PMC
Wang Z, et al. 2013. The draft genomes of soft-shell turtle and green sea turtle yield insights into the development and evolution of the turtle-specific body plan. Nat. Genet. 45, 701 (10.1038/ng.2615) PubMed DOI PMC
Shaffer HB, et al. 2013. The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biol. 14, R28 (10.1186/gb-2013-14-3-r28) PubMed DOI PMC
Tollis M, DeNardo DF, Cornelius JA, Dolby GA, Edwards T, Henen BT, Karl AE, Murphy RW, Kusumi K. 2017. The Agassiz's desert tortoise genome provides a resource for the conservation of a threatened species. PLoS ONE 12, e0177708 (10.1371/journal.pone.0177708) PubMed DOI PMC
Alibardi L. 2011. Histology, ultrastructure, and pigmentation in the horny scales of growing crocodilians. Acta Zool. 92, 187–200. (10.1111/j.1463-6395.2010.00469.x) DOI
Spearman RIC, Riley PA. 1969. A comparison of the epidermis and pigment cells of the crocodile with those in two lizard species. Zool. J. Linn. Soc. 48, 453–466. (10.1111/j.1096-3642.1969.tb00723.x) DOI
Herring PJ. 1994. Reflective systems in aquatic animals. Comp. Biochem. Physiol. A Physiol. 109, 513–546. (10.1016/0300-9629(94)90192-9) DOI
Thayer AH. 1896. The law which underlies protective coloration. Auk 13, 124–129. (10.2307/4068693) DOI
Bustard HR. 1970. The adaptive significance of coloration in hatchling green sea turtles. Herpetologica 26, 224–227.
Ruxton GD, Speed MP, Kelly DJ. 2004. What, if anything, is the adaptive function of countershading? Anim. Behav. 68, 445–451. (10.1016/j.anbehav.2003.12.009) DOI
Rowe JW, Clark DL, Mortensen RA, Commissaris CV, Wittle LW, Tucker JK. 2016. Thermal and substrate color-induced melanization in laboratory reared red-eared sliders (Trachemys scripta elegans). J. Therm. Biol. 61, 125–132. (10.1016/j.jtherbio.2016.09.005) PubMed DOI
Rowe JW, Martin CE, Kamp KR, Clark DL. 2017. Spectral reflectance of Blanding's turtle (Emydoidea blandingii) and substrate color-induced melanization in laboratory-reared turtles. Herpetol. Conserv. Biol. 12, 576–584.
Rowe JW, Clark DL, Ryan C, Tucker JK. 2006. Effect of substrate color on pigmentation in midland painted turtles (Chrysemys picta marginata) and red-eared slider turtles (Trachemys scripta elegans). J. Herpetol. 40, 358.–. (10.1670/0022-1511(2006)40[358:eoscop]2.0.co;2) DOI
Polo-Cavia N, López P, Martín J. 2013. Head coloration reflects health state in the red-eared slider Trachemys scripta elegans. Behav. Ecol. Sociobiol. 67, 153–162. (10.1007/s00265-012-1435-z) DOI
Wang JC, Yang CC, Liang W, Shi HT. 2013. Spectra analysis reveals the sexual dichromatism of red-eared slider turtle (Trachemys scripta). Zool. Res. 34, 475–478. PubMed
Arnold K, Neumeyer C. 1987. Wavelength discrimination in the turtle Pseudemys scripta elegans. Vision Res. 27, 1501–1511. (10.1016/0042-6989(87)90159-3) PubMed DOI
Loew ER, Govardovskii VI. 2001. Photoreceptors and visual pigments in the red-eared turtle, Trachemys scripta elegans. Vis. Neurosci. 18, 753–757. (10.1017/s0952523801185081) PubMed DOI
Ibáñez A, Martín J, Marzal A, Bertolero A. 2017. The effect of growth rate and ageing on colour variation of European pond turtles. Sci. Nat. 104, 49 (10.1007/s00114-017-1469-1) PubMed DOI
Smith HM, Kritsky DC, Holland RL. 1969. Reticulate melanism in the painted turtle. J. Herpetol. 3, 173–176. (10.2307/1562961) DOI
Djurdjevič I, Kreft ME, Sušnik Bajec S. 2015. Comparison of pigment cell ultrastructure and organisation in the dermis of marble trout and brown trout, and first description of erythrophore ultrastructure in salmonids. J. Anat. 227, 583–595. (10.1111/joa.12373) PubMed DOI PMC
Montoyo YG, García M, Segovia Y. 2018. Light and electron microscopic studies on the retina of the booted eagle (Aquila pennata). Zoomorphology 137, 177–190. (10.1007/s00435-017-0373-8) DOI
Lipetz LE. 1984. Pigment types, densities and concentrations in cone oil droplets of Emydoidea blandingii. Vision Res. 24, 605–612. (10.1016/0042-6989(84)90115-9) PubMed DOI
Goldsmith TH, Collins JS, Licht S. 1984. The cone oil droplets of avian retinas. Vision Res. 24, 1661–1671. (10.1016/0042-6989(84)90324-9) PubMed DOI
Manukyan L, Montandon SA, Fofonjka A, Smirnov S, Milinkovitch MC. 2017. A living mesoscopic cellular automaton made of skin scales. Nature 544, 173–179. (10.1038/nature22031) PubMed DOI
van de Hulst HC. 1981. Light scattering by small particles, 470 p New York, NY: Courier Corporation.
Gur D, Palmer BA, Weiner S, Addadi L. 2017. Light manipulation by guanine crystals in organisms: biogenic scatterers, mirrors, multilayer reflectors and photonic crystals. Adv. Funct. Mater. 27, 1603514 (10.1002/adfm.201603514) DOI
Levy-Lior A, Shimoni E, Schwartz O, Gavish-Regev E, Oron D, Oxford G, Weiner S, Addadi L. 2010. Guanine-based biogenic photonic-crystal arrays in fish and spiders. Adv. Funct. Mater. 20, 320–329. (10.1002/adfm.200901437) DOI
Shawkey MD, Hill GE. 2005. Carotenoids need structural colours to shine. Biol. Lett. 1, 121–124. (10.1098/rsbl.2004.0289) PubMed DOI PMC
Steffen JE, McGraw KJ. 2007. Contributions of pterin and carotenoid pigments to dewlap coloration in two anole species. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 146, 42–46. (10.1016/j.cbpb.2006.08.017)) PubMed DOI
Saks L, McGraw K, Hõrak P. 2003. How feather colour reflects its carotenoid content. Funct. Ecol. 17, 555–561. (10.1046/j.1365-2435.2003.00765.x) DOI
Weaver RJ, Santos ESA, Tucker AM, Wilson AE, Hill GE. 2018. Carotenoid metabolism strengthens the link between feather coloration and individual quality. Nat. Commun. 9, 73 (10.1038/s41467-017-02649-z) PubMed DOI PMC
Beltran JCM, Stange C.. 2016. Apocarotenoids: a new carotenoid-derived pathway. In Carotenoids in nature (ed. Stange C.), pp. 239–272. Cham, Switzerland: Springer. PubMed
Giuliano G, Al-Babili S, Von Lintig J.. 2003. Carotenoid oxygenases: cleave it or leave it. Trends Plant Sci. 8, 145–149. (10.1016/s1360-1385(03)00053-0) PubMed DOI
Von Lintig J. 2010. Colors with functions: elucidating the biochemical and molecular basis of carotenoid metabolism. Annu. Rev. Nutr. 30, 35–56. (10.1146/annurev-nutr-080508-141027) PubMed DOI
Toomey MB, Collins AM, Frederiksen R, Cornwall MC, Timlin JA, Corbo JC. 2015. A complex carotenoid palette tunes avian colour vision. J. R. Soc. Interface 12, 20150563 (10.1098/rsif.2015.0563) PubMed DOI PMC
Li B, et al. 2014. Inactivity of human β, β-carotene-9′, 10′-dioxygenase (BCO2) underlies retinal accumulation of the human macular carotenoid pigment. Proc. Natl Acad. Sci. USA 111, 10 173–10 178. (10.1073/pnas.1402526111) PubMed DOI PMC
Cuervo JJ, Belliure J, Negro JJ. 2016. Coloration reflects skin pterin concentration in a red-tailed lizard. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 193, 17–24. (10.1016/j.cbpb.2015.11.011) PubMed DOI
Weiss SL, Foerster K, Hudon J. 2012. Pteridine, not carotenoid, pigments underlie the female-specific orange ornament of striped plateau lizards (Sceloporus virgatus). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 161, 117–123. (10.1016/j.cbpb.2011.10.004) PubMed DOI
Braasch I, Schartl M, Volff J-N. 2007. Evolution of pigment synthesis pathways by gene and genome duplication in fish. BMC Evol. Biol. 7, 74 (10.1186/1471-2148-7-74) PubMed DOI PMC
Steffen JE, McGraw KJ. 2009. How dewlap color reflects its carotenoid and pterin content in male and female brown anoles (Norops sagrei). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 154, 334–340. (10.1016/j.cbpb.2009.07.009) PubMed DOI
Ibáñez A, Polo-Cavia N, López P, Martín J. 2014. Honest sexual signaling in turtles: experimental evidence of a trade-off between immune response and coloration in red-eared sliders Trachemys scripta elegans. Naturwissenschaften 101, 803–811. (10.1007/s00114-014-1219-6) PubMed DOI
Grether GF, Hudon J, Endler JA. 2001. Carotenoid scarcity, synthetic pteridine pigments and the evolution of sexual coloration in guppies (Poecilia reticulata). Proc. R. Soc. Lond. B 268, 1245–1253. PubMed PMC
McGraw KJ. 2005. The antioxidant function of many animal pigments: are there consistent health benefits of sexually selected colourants? Anim. Behav. 69, 757–764 (10.1016/j.anbehav.2004.06.022.) DOI
McGraw KJ, Ardia DR. 2003. Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am. Nat. 162, 704–712. (10.1086/378904) PubMed DOI
Andersson M, Simmons LW. 2006. Sexual selection and mate choice. Trends Ecol. Evol. 21, 296–302. (10.1016/j.tree.2006.03.015) PubMed DOI
Stevens M, Merilaita S. 2008. Defining disruptive coloration and distinguishing its functions. Phil. Trans. R. Soc. B 364, 481–488. (10.1098/rstb.2008.0216) PubMed DOI PMC
Kondo S, Miura T. 2010. Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329, 1616–1620. PubMed
Patterson LB, Bain EJ, Parichy DM. 2014. Pigment cell interactions and differential xanthophore recruitment underlying zebrafish stripe reiteration and Danio pattern evolution. Nat. Commun. 5, 5299 (10.1038/ncomms6299) PubMed DOI PMC
Murray JD. 2003. Mathematical biology II—spatial models and biomedical applications, 814 pp New York, NY: Springer.
Turing AM. 1952. The chemical basis of morphogenesis. Phil. Trans. R. Soc. Lond. B 237, 37–72. (10.1098/rstb.1952.0012) PubMed DOI PMC
Rice R, Cebra-Thomas J, Haugas M, Partanen J, Rice DPC, Gilbert SF. 2017. Melanoblast development coincides with the late emerging cells from the dorsal neural tube in turtle Trachemys scripta. Sci. Rep. 7, 12063 (10.1038/s41598-017-12352-0) PubMed DOI PMC
Hou L, Takeuchi T. 1991. Differentiation of extracutaneous melanocytes in embryos of the turtle, Trionyx sinensis japonicus. Pigment Cell Melanoma Res. 4, 158–162. (10.1111/j.1600-0749.1991.tb00433.x) PubMed DOI
Macedonia JM, James S, Wittle LW, Clark DL. 2000. Skin pigments and coloration in the Jamaican radiation of Anolis lizards. J. Herpetol. 34, 99–109. (10.2307/1565245) DOI
Hirata M, Nakamura K, Kanemaru T, Shibata Y, Kondo S. 2003. Pigment cell organization in the hypodermis of zebrafish. Dev. Dyn. 227, 497–503. (10.1002/dvdy.10334) PubMed DOI
Yasutomi M, Yamada S. 1998. Formation of the dermal chromatophore unit (DCU) in the tree frog Hyla arborea. Pigment Cell Res. 11, 198–205. (10.1111/j.1600-0749.1998.tb00730.x) PubMed DOI
Nielsen HI, Dyck J. 1978. Adaptation of the tree frog, Hyla cinerea, to colored backgrounds, and the role of the three chromatophore types. J. Exp. Zool. 205, 79–94. (10.1002/jez.1402050111) DOI
Kuriyama T, Miyaji K, Sugimoto M, Hasegawa M. 2006. Ultrastructure of the dermal chromatophores in a lizard (Scincidae: Plestiodon latiscutatus) with conspicuous body and tail coloration. Zoolog. Sci. 23, 793–799. (10.2108/zsj.23.793) PubMed DOI
Ernst CH. 1972. Temperature-activity relationship in the painted turtle, Chrysemys picta. Copeia 1972, 217–222. (10.2307/1442479) DOI
Bury RB, Wolfheim JH. 1973. Aggression in free-living pond turtles (Clemmys marmorata). Bioscience 23, 659–662. (10.2307/1296781) DOI
Kobelt F, Linsenmair KE. 1992. Adaptations of the reed frog Hyperolius viridiflavus (Amphibia: Anura: Hyperoliidae) to its arid environment. J. Comp. Physiol. B 162, 314–326. (10.1007/bf00301475) PubMed DOI
Medina I, Newton E, Kearney MR, Mulder RA, Porter WP, Stuart-Fox D. 2018. Reflection of near-infrared light confers thermal protection in birds. Nat. Commun. 9, 3610 (10.1038/s41467-018-05898-8) PubMed DOI PMC
Stuart-Fox D, Newton E, Mulder RA, D'Alba L, Shawkey MD, Igic B. 2018. The microstructure of white feathers predicts their visible and near-infrared reflectance properties. PLoS ONE 13, e0199129 (10.1371/journal.pone.0199129) PubMed DOI PMC
Pinkert S, Zeuss D. 2018. Thermal biology: melanin-based energy harvesting across the tree of life. Curr. Biol. 28, R887–R889. (10.1016/j.cub.2018.07.026) PubMed DOI
Kelsh RN, Harris ML, Colanesi S, Erickson CA. 2009. Stripes and belly-spots—a review of pigment cell morphogenesis in vertebrates. Semin. Cell Dev. Biol. 20, 90–104. (10.1016/j.semcdb.2008.10.001) PubMed DOI PMC
Quevedo WC., Jr 1972. Epidermal melanin units melanocyte-keratinocyte interactions. Am. Zool. 12, 35–41. (10.1093/icb/12.1.35) DOI
Li Q, Clarke JA, Gao K-Q, Zhou C-F, Meng Q, Li D, D'Alba L, Shawkey MD. 2014. Melanosome evolution indicates a key physiological shift within feathered dinosaurs. Nature 507, 350–353. (10.1038/nature12973) PubMed DOI
Eliason CM, Clarke JA.. 2018. Metabolic physiology explains macroevolutionary trends in the melanic colour system across amniotes. Proc. R. Soc. B 285, 20182014 (10.1098/rspb.2018.2014) PubMed DOI PMC
Stettenheim PR. 2000. The integumentary morphology of modern birds—an overview. Am. Zool. 40, 461–477. (10.1093/icb/40.4.461) DOI
Biedermann W. 1928. Vergleichende Physiologie des Integuments der Wirbeltiere. In Ergebnisse der Biologie (eds von Frisch K, Goldschmidt R, Ruhland W, Winterstein H), pp. 360–680. Berlin, Germany: Springer.
Oliphant LW, Hudon J, Bagnara JT. 1992. Pigment cell refugia in homeotherms—the unique evolutionary position of the iris. Pigment Cell Melanoma Res. 5, 367–371. (10.1111/j.1600-0749.1992.tb00564.x) PubMed DOI
Menon GK, Menon J. 2000. Avian epidermal lipids: functional considerations and relationship to feathering. Am. Zool. 40, 540–552. (10.1093/icb/40.4.540) DOI
Sköld HN, Aspengren S, Cheney KL, Wallin M. 2016. Fish chromatophores—from molecular motors to animal behavior. Int. Rev. Cell Mol. Biol. 321, 171–219. (10.1016/bs.ircmb.2015.09.005) PubMed DOI
Cal L, Suarez-Bregua P, Moran P, Cerdá-Reverter JM, Rotllant J. 2018. Fish pigmentation. A key issue for the sustainable development of fish farming. In Emerging issues in fish larvae research (ed. Yúfera M.), pp. 229–252. Cham, Switzerland: Springer.
Bagnara JT. 1976. Color change. In Physiology of Amphibia (ed. Lofts B.), pp. 1–52. New York, NY: Academic; Press.
DuShane GP. 1943. The embryology of vertebrate pigment cells. Part I. Amphibia. Q. Rev. Biol. 18, 109–127. (10.1086/394671) DOI
Cooper WE, Greenberg N. 1992. Reptilian coloration and behavior. In Biology of Reptilia, Volume 18, Physiology E, Hormones, Brain and Behaviour (eds Gans C, Crews D), pp. 298–422. Chicago, IL: The University of Chicago Press.
Alibardi L. 2012. Cytology and localization of chromatophores in the skin of the Tuatara (Sphenodon punctaus). Acta Zool. 93, 330–337. (10.1111/j.1463-6395.2011.00506.x) DOI
Eriksson J, et al. 2008. Identification of the yellow skin gene reveals a hybrid origin of the domestic chicken. PLoS Genet. 4, e1000010 (10.1371/journal.pgen.1000010.eor) PubMed DOI PMC
McGraw KJ, Toomey MB, Nolan PM, Morehouse NI, Massaro M, Jouventin P. 2007. A description of unique fluorescent yellow pigments in penguin feathers. Pigment Cell Melanoma Res. 20, 301–304. (10.1111/j.1600-0749.2007.00386.x) PubMed DOI
McGraw KJ, et al. 2004. You can't judge a pigment by its color: carotenoid and melanin content of yellow and brown feathers in swallows, bluebirds, penguins, and domestic chickens. Condor 106, 390–395. (10.1650/7384) DOI
Oliphant LW. 1987. Pteridines and purines as major pigments of the avian iris. Pigment Cell Res. 1, 129–131. (10.1111/j.1600-0749.1987.tb00401.x) PubMed DOI
Obika M, Bagnara JT. 1964. Pteridines as pigments in amphibians. Science 143, 485–487. (10.1126/science.143.3605.485) PubMed DOI
Oliphant LW. 1988. Cytology and pigments of non-melanophore chromatophores in the avian iris. Prog. Clin. Biol. Res. 256, 65–82. PubMed
Oliphant LW. 1981. Crystalline pteridines in the stromal pigment cells of the iris of the great horned owl. Cell Tissue Res. 217, 387–395. (10.1007/bf00233588) PubMed DOI
Kumar S, Stecher G, Suleski M, Hedges SB. 2017. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34, 1812–1819. (10.1093/molbev/msx116) PubMed DOI
Vinther J. 2015. A guide to the field of palaeo colour: melanin and other pigments can fossilise: reconstructing colour patterns from ancient organisms can give new insights to ecology and behaviour. Bioessays 37, 643–656. (10.1002/bies.201500018) PubMed DOI
Lindgren J, et al. 2018. Soft-tissue evidence for homeothermy and crypsis in a Jurassic ichthyosaur. Nature 564, 359–365. (10.1038/s41586-018-0775-x) PubMed DOI
Lindgren J, et al. 2014. Skin pigmentation provides evidence of convergent melanism in extinct marine reptiles. Nature 506, 484–488. (10.1038/nature12899) PubMed DOI