BMC Evolutionary Biology | |
Pigmentary and photonic coloration mechanisms reveal taxonomic relationships of the Cattlehearts (Lepidoptera: Papilionidae: Parides) | |
Doekele G Stavenga2  Natasja IJbema3  Bodo D Wilts1  | |
[1] Present address: Department of Physics, Cavendish Laboratories, University of Cambridge, 13 JJ Thomson Avenue, Cambridge, CB3 0HE, UK;Computational Physics, Zernike Institute for Advanced Materials, University of Groningen, Nijenborgh 4, Groningen, NL-9747AG, The Netherlands;Present address: Accenture Nederland B.V, Gustav Mahlerplein 90, Amsterdam, NL-1082 MA, The Netherlands | |
关键词: Wing traits; Scattering; Phylogeny; Papiliochrome; Papilionidae; Morphology; Iridescence; | |
Others : 1118101 DOI : 10.1186/s12862-014-0160-9 |
|
received in 2014-04-02, accepted in 2014-07-14, 发布年份 2014 | |
【 摘 要 】
Background
The colorful wing patterns of butterflies, a prime example of biodiversity, can change dramatically within closely related species. Wing pattern diversity is specifically present among papilionid butterflies. Whether a correlation between color and the evolution of these butterflies exists so far remained unsolved.
Results
We here investigate the Cattlehearts, Parides, a small Neotropical genus of papilionid butterflies with 36 members, the wings of which are marked by distinctly colored patches. By applying various physical techniques, we investigate the coloration toolkit of the wing scales. The wing scales contain two different, wavelength-selective absorbing pigments, causing pigmentary colorations. Scale ridges with multilayered lamellae, lumen multilayers or gyroid photonic crystals in the scale lumen create structural colors that are variously combined with these pigmentary colors.
Conclusions
The pigmentary and structural traits strongly correlate with the taxonomical distribution of Parides species. The experimental findings add crucial insight into the evolution of butterfly wing scales and show the importance of morphological parameter mapping for butterfly phylogenetics.
【 授权许可】
2014 Wilts et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150206020744320.pdf | 2262KB | download | |
Figure 6. | 62KB | Image | download |
Figure 5. | 28KB | Image | download |
Figure 4. | 38KB | Image | download |
Fig. 2. | 112KB | Image | download |
Figure 2. | 147KB | Image | download |
Figure 1. | 116KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Fig. 2.
Figure 4.
Figure 5.
Figure 6.
【 参考文献 】
- [1]Doucet SM, Meadows MG: Iridescence: a functional perspective. J R Soc Interface 2009, 6(Suppl 2):S115-S132.
- [2]Stevens M, Merilaita S: Animal camouflage: mechanisms and function. Cambridge University Press, Cambridge, UK; 2011.
- [3]Andersson M: Sexual selection. Princeton University Press, Princeton, NJ; 1994.
- [4]Condamine FL, Sperling FAH, Wahlberg N, Rasplus J, Kergoat GJ: What causes latitudinal gradients in species diversity? Evolutionary processes and ecological constraints on swallowtail biodiversity. Ecol Lett 2012, 15:267-277.
- [5]Ehrlich PR, Raven PH: Butterflies and plants: a study in coevolution. Evolution 1964, 18:586-608.
- [6]Simonsen TJ, Zakharov EV, Djernaes M, Cotton AM, Vane-Wright RI, Sperling FAH: Phylogenetics and divergence times of Papilioninae (Lepidoptera) with special reference to the enigmatic genera Teinopalpus and Meandrusa. Cladistics 2011, 27:113-137.
- [7]Silva-Brandao KL, Freitas AV, Brower AV, Solferini VN: Phylogenetic relationships of the New World Troidini swallowtails (Lepidoptera: Papilionidae) based on COI, COII, and EF-1alpha genes. Mol Phylogen Evol 2005, 36:468-483.
- [8]Silva-Brandao KL, Azeredo-Espin AM, Freitas AV: New evidence on the systematic and phylogenetic position of Parides burchellanus (Lepidoptera: Papilionidae). Mol Ecol Res 2008, 8:502-511.
- [9]Pinheiro CEG: Palatability and escaping ability in Neotropical butterflies: tests with wild kingbirds (Tyrannus melancholicus, Tyrannidae). Biol J Linn Soc 1996, 59:351-365.
- [10]Ruxton GD, Sherratt TN, Speed MP: Avoiding Attack: The Evolutionary Ecology of Crypsis, Warning Signals and Mimicry. Oxford University Press; 2004. ISBN 0-19-852859-0.
- [11]Pinheiro CEG: Asynchrony in daily activity patterns of butterfly models and mimics. J Trop Ecol 2007, 23:119-123.
- [12]Kinoshita S: Structural colors in the realm of nature. World Scientific, Singapore; 2008.
- [13]Ghiradella H: Light and color on the wing: structural colors in butterflies and moths. Appl Opt 1991, 30:3492-3500.
- [14]Vukusic P, Sambles JR: Photonic structures in biology. Nature 2003, 424:852-855.
- [15]Michielsen K, Stavenga DG: Gyroid cuticular structures in butterfly wing scales: biological photonic crystals. J R Soc Interface 2008, 5:85-94.
- [16]Vukusic P: Advanced photonic systems on the wing-scales of Lepidoptera. In Functional surfaces in biology - Little structures with big effects, Volume 1. Edited by Gorb SN. Springer, New York; 2009:237-258.
- [17]Poladian L, Wickham S, Lee K, Large MC: Iridescence from photonic crystals and its suppression in butterfly scales. J R Soc Interface 2009, 6(Suppl 2):S233-S242.
- [18]Saranathan V, Osuji CO, Mochrie SG, Noh H, Narayanan S, Sandy A, Dufresne ER, Prum RO: Structure, function, and self-assembly of single network gyroid (I4132) photonic crystals in butterfly wing scales. Proc Natl Acad Sci U S A 2010, 107:11676-11681.
- [19]Wilts BD, Michielsen K, De Raedt H, Stavenga DG: Iridescence and spectral filtering of the gyroid-type photonic crystals in Parides sesostris wing scales. Interface Focus 2012, 2:681-687.
- [20]Yoshioka S, Fujita H, Kinoshita S, Matsuhana B: Alignment of crystal orientations of the multi-domain photonic crystals in Parides sesostris wing scales. J R Soc Interface 2014, 11:20131029.
- [21]Vukusic P, Stavenga DG: Physical methods for investigating structural colours in biological systems. J R Soc Interface 2009, 6(Suppl 2):S133-S148.
- [22]Vukusic P, Sambles JR, Lawrence CR: Structurally assisted blackness in butterfly scales. Proc R Soc B 2004, 271(Suppl 4):S237-S239.
- [23]Ghiradella H: Insect cuticular surface modifications: scales and other structural formations. Adv Insect Physiol 2010, 38:135-180.
- [24]Ghiradella H: Structure and development of iridescent butterfly scales: lattices and laminae. J Morphol 1989, 202:69-88.
- [25]Dechkrong P, Jiwajinda S, Dokchan P, Kongtungmon M, Chomsaeng N, Chairuangsri T, Yu C, Hsiao C, Shiojiri M: Fine structure of wing scales of butterflies, Euploea mulciber and Troides aeacus. J Struct Biol 2011, 176:75-82.
- [26]Vukusic P, Sambles JR, Lawrence CR, Wootton RJ: Structural colour: now you see it—now you don't. Nature 2001, 4:36.
- [27]Giraldo MA, Yoshioka S, Stavenga DG: Far field scattering pattern of differently structured butterfly scales. J Comp Physiol A 2008, 194:201-207.
- [28]Wilts BD, Pirih P, Stavenga DG: Spectral reflectance properties of iridescent pierid butterfly wings. J Comp Physiol A 2011, 197:693-702.
- [29]Stavenga DG, Leertouwer HL, Pirih P, Wehling MF: Imaging scatterometry of butterfly wing scales. Opt Express 2009, 17:193-202.
- [30]Yeh P: Optical waves in layered media. Wiley-Interscience, Hoboken NJ; 2005.
- [31]Stavenga DG, Wilts BD, Leertouwer HL, Hariyama T: Polarized iridescence of the multilayered elytra of the Japanese jewel beetle, Chrysochroa fulgidissima. Phil Trans Roy Soc B 2011, 366:709-723.
- [32]Wilts BD, Trzeciak TM, Vukusic P, Stavenga DG: Papiliochrome II pigment reduces the angle-dependency of structural wing colouration in nireus group papilionids. J Exp Biol 2012, 215:796-805.
- [33]Möhn E, Bauer E, Frankenbach T: Butterflies of the world: Papilionidae XIII: Parides. Goecke & Evers, Canterbury; 2007.
- [34]Simonsen TJ, de Jong R, Heikkilä M, Kaila L: Butterfly morphology in a molecular age – does it still matter in butterfly systematics? Arthropod Struct Dev 2012, 41:307-322.
- [35]Wilts BD, Leertouwer HL, Stavenga DG: Imaging scatterometry and microspectrophotometry of lycaenid butterfly wing scales with perforated multilayers. J R Soc Interface 2009, 6(Suppl 2):S185-S192.
- [36]Bálint Z, Kertész K, Piszter G, Vértesy Z, Biró LP: The well-tuned blues: the role of structural colours as optical signals in the species recognition of a local butterfly fauna (Lepidoptera: Lycaenidae: Polyommatinae). J R Soc Interface 2012, 9:1745-1756.
- [37]Michielsen K, De Raedt H, Stavenga DG: Reflectivity of the gyroid biophotonic crystals in the ventral wing scales of the Green Hairstreak butterfly, Callophrys rubi. J R Soc Interface 2010, 7:765-771.
- [38]Stavenga DG, Leertouwer HL, Hariyama T, De Raedt H, Wilts BD: Sexual dichromatism of the damselfly Calopteryx japonica caused by a melanin-chitin multilayer in the male wing veins. PLoS One 2012, 7:e49743.
- [39]Umebachi Y: Yellow pigments in the wings of Papilio xuthus (papilionid butterfly). Acta Vitaminologica et Enzymologica 1975, 29:219-222.
- [40]Umebachi Y: Papiliochrome, a new pigment group of butterfly. Zool Sci 1985, 2:163-174.
- [41]Pirih P, Wilts BD, Stavenga DG: Spatial reflection patterns of iridescent wings of male pierid butterflies: curved scales reflect at a wider angle than flat scales. J Comp Phys A 2011, 197:987-997.
- [42]Ghiradella H: Structure and development of iridescent lepidopteran scales - the Papilionidae as a showcase family. Ann Entomol Soc 1985, 78:252-264.
- [43]Hamley IW, Castelletto V, Mykhaylyk OO, Yang Z, May RP, Lyakhova KS, Sevink GJ, Zvelindovsky AV: Mechanism of the transition between lamellar and gyroid phases formed by a diblock copolymer in aqueous solution. Langmuir 2004, 20:10785-10790.
- [44]Cochran EW, Garcia-Cervera CJ, Fredrickson GH: Stability of the gyroid phase in diblock copolymers at strong segregation. Macromolecules 2006, 39:2449-2451.
- [45]Reed RD, Papa R, Martin A, Hines HM, Counterman BA, Pardo-Diaz C, Jiggins CD, Chamberlain NL, Kronforst MR, Chen R, Halder G, Nijhout HF, McMillan WO: Optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 2011, 333:1137-1141.
- [46]Beutel RG, Kristensen NP: Morphology and insect systematics in the era of phylogenomics. Arth Struct Devel 2012, 41:303-305.
- [47]Wilts BD, Michielsen K, De Raedt H, Stavenga DG: Hemispherical Brillouin zone imaging of a diamond-type biological photonic crystal. J R Soc Interface 2012, 9:1609-1614.
- [48]Leertouwer HL, Wilts BD, Stavenga DG: Refractive index and dispersion of butterfly chitin and bird keratin measured by polarizing interference microscopy. Opt Express 2011, 19:24061-24066.
- [49]Land MF: The physics and biology of animal reflectors. Prog Biophys Mol Biol 1972, 24:77-105.
- [50]Kinoshita S, Yoshioka S, Miyazaki J: Physics of structural colors. Rep Prog Phys 2008, 71:076401.