Intraspecific colour variation among lizards in distinct island environments enhances local camouflage

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Marshall, Kate L A ^a   Philpot, Kate E ^b   Damas Moreira, Isabel ^c   Stevens, Martin ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF EXETER   (United Kingdom)

^c CENTRO DE INVESTIGAÇÃO EM BIODIVERSIDADE E RECURSOS GENÉTICOS   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

BIRD; ECOLOGY; EVOLUTIONARY ADAPTATION; HUMAN; LIZARD; LUMINANCE; PREDATOR; REPRODUCTIVE ISOLATION; ANIMAL; BIOLOGICAL MIMICRY; ECOSYSTEM; EVOLUTION; PHYSIOLOGY; SKIN PIGMENTATION;

ANIMALS; BIOLOGICAL EVOLUTION; BIOLOGICAL MIMICRY; ECOSYSTEM; LIZARDS; SKIN PIGMENTATION;

EID: 84945968051     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0135241     Document Type: Article

References (92)

1. Clarke B. Natural selection in mixed populations of two polymorphic snails. Heredity. 1962; 17: 319-45.
2. Kettlewell HBD. A resume of investigations on the evolution of melanism in the Lepidoptera. P Roy Soc B. 1956; 145(920): 297-303.
3. Kettlewell HBD. The phenomenon of industrial melanism in Lepidoptera. Annu Rev Entomol. 1961; 6: 245-62.
4. Rundle HD, Nosil P. Ecological speciation. Ecol Lett. 2005; 8: 336-52.
5. Schluter D. Ecology and the origin of species. Trends Ecol Evol. 2001; 16: 372-80. PMID: 11403870
6. Stevens M. Sensory Ecology, Behaviour and Evolution. Oxford: Oxford University Press; 2013.
7. Hoekstra HE, Hirschmann RJ, Bundey RA, Insel PA, Crossland JP. A single amino acid mutation contributes to adaptive beach mouse color pattern. Science. 2006; 313: 101-4. PMID: 16825572
8. Manceau M, Domingues VS, Mallarino R, Hoekstra HE. The developmental role of agouti in color pattern evolution. Science. 2011; 331: 1062-5. doi: 10.1126/science.1200684 PMID: 21350176
9. Nachman MW, Hoekstra HE, D'Agostino SL. The genetic basis of adaptive melanism in pocket mice. P Natl Acad Sci USA. 2003; 100(9): 5268-73.
10. Rosenblum EB, Römpler H, Schöneberg T, Hoekstra HE. Molecular and functional basis of phenotypic convergence in white lizards at White Sands. P Natl Acad Sci USA. 2010; 107: 2113-7.
11. Steiner CC, Weber JN, Hoekstra HE. Adaptive variation in beach mice produced by two interacting pigmentation genes. PloS Biol. 2007; 6: e36.
12. McLean CA, Moussalli A, Stuart-Fox DM. Local adaptation and divergence in colour signal conspicuousness between monomorphic and polymorphic lineages in a lizard. J Evol Biol. 2014; 27: 2654-64. doi: 10.1111/jeb.12521 PMID: 25330209
13. Stuart-Fox DM, Moussalli A, Johnston GR, Owens IPF. Evolution of color variation in dragon lizards: Quantitative tests of the role of crypsis and local adaptation. Evolution. 2004; 58: 1549-59. PMID: 15341157
14. Hart NS. Vision in the peafol (Aves: Pavo cristatus). J Exp Biol. 2002; 205: 3925-35. PMID: 12432014
15. Lind O, Mitkus M, Olsson P, Kelber A. Ultraviolet sensitivity and colour vision in raptor foraging. J Exp Biol. 2013; 216: 1819-26. doi: 10.1242/jeb.082834 PMID: 23785106
16. Endler JA, Mielke PW. Comparing entire colour patterns as birds see them. Biol J Linn Soc Lond. 2005; 86(4): 405-31.
17. Stevens M. Predator perception and the interrelation between different forms of protective coloration. P Roy Soc B. 2007; 274(1617): 1457-64.
18. Fan M, Stuart-Fox DM, Cadena V. Cyclic colour change in the bearded dragon Pogona vitticeps under different photoperiods. PloS One. 2014; 9: e111504. doi: 10.1371/journal.pone.0111504 PMID: 25354192
19. Hawlena D, Boochnik R, Abramsky Z, Bouskila A. Blue tail and striped body: why do lizards change their infant costume when growing up? Beh Ecol. 2006; 17: 889-96.
20. Hemmi JM, Marshall J, Pix W, Vorobyev M, Zeil J. The variable colours of the fiddler crab Uca vomeris and their relation to background and predation. J Exp Biol. 2006; 209: 4140-53. PMID: 17023607
21. Stevens M, Rong CP, Todd P. Colour change and camouflage in the horned ghost crab Ocypode ceratophthalmus. Biol J Linn Soc Lond. 2013; 109: 257-70.
22. Jv Bedriaga. Die Amphibien und Reptilien Griechenlands. Bull Soc Imp Nat Moscou 1882; 56: 43-103, 278-344.
23. Chondropoulos BP. A checklist of the Greek reptiles. I. The lizards. Amphibia-Reptilia. 1986; 7(3): 217-35.
24. Poulakakis N, Goulielmos G, Antoniou A, Zouros E, Mylonas M. Isolation and characterization of polymorphic microsatellite markers in the wall lizard Podarcis erhardii (Squamata: Lacertidae). Mol Ecol Notes. 2005; 5: 549-51.
25. Poulakakis N, Lymberakis P, Antoniou A, Chalkia D, Zouros E, Mylonas M, et al. Molecular phylogeny and biogeography of the wall-lizard Podarcis erhardii (Squamata: Lacertidae). Mol Phylogenet Evol. 2003; 28(1): 38-46. PMID: 12801470
26. Hurston H, Voith L, Bonanno J, Foufopoulos J, Pafilis P, Valakos E, et al. Effects of fragmentation on genetic diversity in island populations of the Aegean wall lizard Podarcis erhardii (Lacertidae, Reptilia). Mol Phylogenet Evol. 2009; 52: 395-405. doi: 10.1016/j.ympev.2009.03.028 PMID: 19348955
27. Foufopoulos J, Ives AR. Reptile extinctions on land-bridge islands: Life-history attributes and vulnerability to extinction. Am Nat. 1999; 153: 1-25.
28. Poulakakis N, Kapli P, Lymberakis P, Trichas A, Vardinoyiannis K, Sfenthourakis S, et al. A review of phylogeographic analyses of animal taxa from the Aegean and surrounding regions. J Zool Syst Evol Res. 2014; 53: 18-32.
29. Rosenblum EB. Convergent evolution and divergent selection: Lizards at the White Sands ecotone. Am Nat. 2006; 167: 1-15. PMID: 16475095
30. Brock KM, Bednekoff PA, Pafilis P, Foufopoulos J. Evolution of antipredator behavior in an island lizard species, Podarcis erhardii (Reptilia: Lacertidae): The sum of all fears? Evolution. 2014; 69: 216-31. doi: 10.1111/evo.12555 PMID: 25346210
31. Handrinos G, Akriotis T. The Birds of Greece. London: Christopher Helm Ltd.; 1997.
32. Perissoratis C, Conispoliatis N. The impacts of sea-level changes during latest Pleistocene and Holocene times on the morphology of the Ionian and Aegean seas (SE Alpine Europe). Mar Geol. 2003; 196: 145-56.
33. Kalogeropoulos S, Paritsis S. Geological and geochemical evolution of the Santorini Volcano: a review. In: Hardy DA, editor. Proceedings of the Third International Congress; Santorini, Greece. London: The Thera Foundation; 1990. p. 164-71.
34. Higgins MD, Higgins R. A geological companion to Greece and the Aegean. Ithaca, NY/London: Cornell University Press/Duckworth Publishers; 1996.
35. Photiades A, Keay S. Geological and geochronological data for Sikinos and Folegandros metamorphic units (Cyclades, Greece): Their tectono-stratigraphic significance. Bulletin of the Geological Society of Greece. 2003; 35: 35-45.
36. Marshall KLA, Stevens M. Wall lizards display conspicuous signals to conspecifics and reduce detection by avian predators. Beh Ecol. 2014; 25(6): 1325-37.
37. Castilla AM, Gosá A, Galán P, Pérez-Mellado V. Green tails in lizards of the Genus Podarcis: Do they influence the intensity of predation? Herpetologica. 1999; 55: 530-7.
38. Huyghe K, Vanhooydonck B, Herrel A, Tadić Z, Van Damme R. Morphology, performance, behavior and ecology of three color morphs in males of the lizard Podarcis melisellensis. Integr Comp Biol. 2007; 47: 211-20. doi: 10.1093/icb/icm043 PMID: 21672832
39. Van Damme R, Bauwens D, Castilla AM, Verheyen RP. Comparative thermal ecology of the sympatric lizards Podarcis tiliguerta and Podarcis sicula. Acta Oecol. 1990; 11: 503-12.
40. Macedonia JM, Brandt Y, Clark DL. Sexual dichromatism and differential conspicuousness in two populations of the common collared lizard (Crotaphytus collaris) from Utah and New Mexico, USA. Biol J Linn Soc. 2002; 77: 67-85.
41. Valakos E, Maragou P, Mylonas M. Geographical distribution: Podarcis erhardii. Herp Rev. 1999; 30: 52-3.
42. Jordan MA, Snell HL. Historical fragmentation of islands and genetic drift in populations of Galápagos lava lizards (Microlophus albemarlensis complex). Mol Ecol. 2008; 17: 1224-37. doi: 10.1111/j.1365- 294X.2007.03658.x PMID: 18302685
43. Arnold N, Ovenden D. Field Guide to Reptiles and Amphibians of Britain and Europe. London: Harper Collins; 2002.
44. Valakos E. The feeding ecology of Podarcis erhardii (Reptilia: Lacertidae) in a main insular ecosystem. J Herpetol. 1986; 1: 118-21.
45. Grimm A, Ramírez AMP, Moulherat S, Reynaud J, Henle K. Life-history trait database of European reptile species. Nat Cons. 2014; 9: 45-67.
46. Podarcis erhardii [database on the Internet]. IUCN Red List of Threatened Species Version 2013.2. 2009 [cited 25 November 2013].
47. García-Muñoz E, Sillero N. Two new types of noose for capturing herps. Acta Herpetologica. 2010; 5, 259-263.
48. Stevens M, Párraga CA, Cuthill IC, Partridge JC, Troscianko TS. Using digital photography to study animal coloration. Biol J Linn Soc Lond. 2007; 90(2): 211-37.
49. Bergman TJ, Beehner JC. A simple method for measuring colour in wild animals: validation and use on chest patch colour in geladas (Theropithecus gelada). Biol J Linnean Soc. 2008; 94(2): 231-40.
50. Stevens M, Stoddard MC, Higham JP. Studying primate color: towards visual system-dependent methods. Int J Primatol. 2009; 30: 893-917.
51. Verwaijen D, Van Damme R. Wide home ranges for widely foraging lizards. Zoology. 2008; 111(1): 37-47. PMID: 17997294
52. Cooper WE, Greenberg N. Reptilian Coloration and Behavior. In: Crews D, Gans C, editors. Biology of the Reptilian: Hormones, Brain, and Behaviour. New York: Academic Press; 1992. p. 298-422.
53. Fitze PS, Cote J, San-Jose LM, Meylan S, Isaksson C, Andersson S, et al. Carotenoid-based colours reflect the stress response in the common lizard. PloS One. 2009; 4: e5111. doi: 10.1371/journal.pone. 0005111 PMID: 19352507
54. Pike TW. Using digital cameras to investigate animal colouration: estimating sensor sensitivity functions. Behav Ecol Sociobiol. 2011; 65: 849-58.
55. Stevens M, Cuthill IC. Hidden messages: are ultraviolet signals a special channel in avian communication? BioScience. 2007; 57(6): 501-7.
56. Stevens M, Lown AE, Wood LE. Color change and camouflage in juvenile shore crabs Carcinus maenas. Front Ecol Evol. 2014; 2: 14.
57. Hart NS, Partridge JC, Cuthill IC, Bennett ATD. Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L.) and the blackbird (Turdus merula L.). Journal of Comparative Physiology. 2000; 186: 375-87. PMID: 10798725
58. Jones CD, Osorio D. Discrimination of oriented visual textures by poultry chicks. Vision Research. 2004; 44: 83-9. PMID: 14599573
59. Osorio D, Vorobyev M. Photoreceptor spectral sensitivities in terrestrial animals: adaptations for luminance and colour vision. Proc R Soc B. 2005; 272: 1745-52. PMID: 16096084
60. Cuthill IC. Color Perception. In: Hill GE, McGraw KJ, editors. Bird Coloration. Cambridge, MA: Harvard University Press; 2006. p. 3-40.
61. Hart NS, Hunt DM. Avian visual pigments: characteristics, spectral tuning, and evolution. Am Nat. 2007; 169(S1): S7-S26.
62. Martín J, López P. Avian predation on a large lizard (Lacerta lepida) found at low population densities in Mediterranean habitats: An analysis of bird diets. Copeia 1996; 1996: 722-6.
63. Ödeen A, Håstad O. 2013. The phylogenetic distribution of ultraviolet sensitivity in birds. BMC Evol Biol. 13:36. doi: 10.1186/1471-2148-13-36 PMID: 23394614
64. Castilla AM, Labra A. Predation and spatial distribution of the lizard Podarcis hispanica atrata: an experimental approach. Acta Oecologica. 1997; 19: 107-114.
65. Collar NJ. Family Turdidae (thrushes). In: del Hoyo J, Elliot A, Sargatal J, editors. Handbook of the Birds of the World Vol. 10.Cuckoo-shrikes to thrushes. Barcelona: Lynx Edicions; 2005. p. 514-807.
66. Sazima I, D'Angelo GB. The pale-breasted thrush (Turdud leucomelas) preys on a gekkonid lizard and an anomalepidid snake. Revista Brasileira de Ornitologia. 2011; 19: 450-452.
67. Martín J, López P. Amphibians and reptiles as prey of birds in southwestern Europe. Washington: Smithsonian Herpetological Information Service; 1990.
68. Castilla AM, Bauwens D. Thermal biology, microhabitat selection, and conservation of the insular lizard Podarcis hispanica astrata. Oecologia. 1990; 85: 366-74.
69. Stevens M, Merilaita S. Defining disruptive coloration and distinguishing its functions. Phil Trans B. 2009; 364: 481-488.
70. Komdeur J, Oorebeek M, Overveld Tv, Cuthill IC. Mutual ornamentation, age, and reproductive performance in the European starling. Beh Ecol. 2005; 16: 805-17.
71. Spottiswoode CN, Stevens M. How to evade a coevolving brood parasite: egg discrimination versus egg variability as host defences. Proc R Soc B. 2011; 278: 3566-73. doi: 10.1098/rspb.2011.0401 PMID: 21490019
72. Stevens M, Lown AE, Denton AM. Rockpool gobies change colour for camouflage. PloS One. 2014; 9: e110325. doi: 10.1371/journal.pone.0110325 PMID: 25333382
73. Osorio D, Smith AC, Vorobyev M, Buchanan-Smith HM. Detection of fruit and the selection of primate visual pigments for color vision. Am Nat. 2004; 164: 696-708.
74. Osorio D, Vorobyev M. Colour vision as an adaptation to frugivory in primates. Proc R Soc B. 1996; 263: 593-9. PMID: 8677259
75. Rowe MH. Trichromatic color vision in primates. Physiology. 2002; 17: 93-8.
76. Vorobyev M, Osorio D. Receptor noise as a determinant of colour thresholds. Proc R Soc B. 1998; 265 (1394): 351-8. PMID: 9523436
77. Siddiqi A, Cronin TW, Loew ER, Vorobyev M, Summers K. Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio. J Exp Biol. 2004; 207: 2471-85. PMID: 15184519
78. Vorobyev M, Osorio D, Bennett ATD, Marshall NJ, Cuthill IC. Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol A. 1998; 183: 621-33. PMID: 9839454
79. Ruxton GD, Beauchamp G. Time for some a priori thinking about post hoc testing. Behav Ecol. 2008; 19(3): 690-3.
80. Rosenblum EB, Hoekstra HE, Nachman MW. Adaptive reptile color variation and the evolution of the MC1R gene. Evolution. 2004; 58(8): 1794-808. PMID: 15446431
81. Vignieri SN, Larson JG, Hoekstra HE. The selective advantage of crypsis in mice. Evolution. 2010; 64 (7): 2153-8. doi: 10.1111/j.1558-5646.2010.00976.x PMID: 20163447
82. Garcia JE, Rohr D, Dyer AG. Trade-off between camouflage and sexual dimorphism revealed by UV digital imaging: the case of Australian Mallee dragons (Ctenophorus fordi). J Exp Biol. 2013; 216: 4290-8. doi: 10.1242/jeb.094045 PMID: 23997198
83. Osorio D, Miklosi A, Gonda Z. Visual ecology and perception of coloration patterns by domestic chicks. Evol Ecol. 1999; 13: 673-89.
84. Stuart-Fox DM, Whiting MJ, Moussalli A. Camouflage and colour change: responses to bird and snake predators across multiple populations in a dwarf chameleon. Biol J Linn Soc Lond. 2006; 88: 437-46.
85. Kelber A, Vorobyev M, Osorio D. Animal colour vision-behavioural tests and physiological concepts. Biological Reviews. 2003; 78: 81-118. PMID: 12620062
86. Husak JF, Macedonia JM, Fox SF, Sauceda RC. Predation cost of conspicuous male coloration in collared lizards (Crotaphytus collaris): An experimental test using clay-covered model lizards. Ethology. 2006; 112(6): 572-80.
87. Stuart-Fox DM, Moussalli A, Marshall NJ, Owens IPF. Conspicuous males suffer higher predation risk: visual modelling and experimental evidence from lizards. Anim Behav. 2003; 66(3): 541-50.
88. Hamilton PS, Gaalema DE, Sullivan BK. Short-term changes in dorsal reflectance for background matching in Ornate Tree lizards (Urosaurus ornatus). Amphibia-Reptilia. 2008; 29: 473-7.
89. Hernández-Gallegos O, Domínguez-Vega H. Seasonal changes in the dorsal coloration in the lizard Aspidoscelis costata costata (Squamata: Teiidae). Rev Biol Trop. 2012; 60: 405-12. PMID: 22458234
90. Houston AI, Stevens M, Cuthill IC. Animal camouflage: compromise of specialize in a 2 patch-type envrionment? Beh Ecol. 2007; 18: 769-75.
91. Merilaita S, Tuomi J, Jormalainen V. Optimization of cryptic coloration in heterogeneous habitats. Biol J Linn Soc Lond. 1999; 67: 151-61.
92. Jordan MA, Snell HL, Snell HM, Jordan WC. Phenotypic divergence despite high levels of gene flow in Galápagos lava lizards (Microlophus albemarlensis). Mol Ecol. 2005; 14: 859-67. PMID: 15723677