Intraspecific variations in coloration may represent a compromise between selection for intraspecific communication and selection for thermoregulation and predator avoidance. Iberian wall lizards, Podarcis hispanica, exhibit substantial levels of intraspecific variation that cannot be necessarily attributed to genetic differences. We compared variations in coloration and habitat use of three phenotypically distinct populations of P. hispanica in Central Spain. Results suggested that differences in coloration may be related to habitat characteristics and climatic conditions. Thus, lizards from populations with colder temperatures were darker and larger, which may favor thermoregulation. Lizards that lived in habitats with more vegetation and darker granite rocks showed a dark brown to black dorsal coloration. In contrast, lizards from habitats with gypsum and light sandy soil without vegetation or large rocks had a brighter yellow to green dorsal coloration. These differences may increase crypsis to predators in each habitat. There were also differences in the characteristics and relative importance of sexual visual signals (i.e., ventrolateral coloration and number of lateral blue spots) and chemical signals (i.e., number of femoral pores) that might increase efficiency of communication in each environment. Natural selection for traits that allow a better thermoregulation, predator avoidance, and communication might lead to population divergence. 1. Introduction Intraspecific variation in coloration is an intriguing phenomenon found in a widespread number of animal taxa, particularly vertebrates [1–3]. Animal coloration represents a compromise between selection for signaling functions in intraspecific communication (i.e., sexual signals) and selection for thermoregulation and defense against visually oriented predators [2, 4–10]. According to this, differences in coloration between species and populations or between sexes and age classes are the result of subtle differences in the balance between natural and sexual selection [4, 5, 9, 11]. Variation in coloration on a large geographical scale is essentially found in response to variations in climate, habitat, and predators [3, 12–14]. Correlational selection will promote that coloration will become associated genetically and developmentally with other traits [15]. In reptiles, color variations have long been studied as examples of adaptive evolution [14, 16, 17]. On the one hand, coloration impacts thermoregulation in ectotherms because darker reptiles are able to warm faster and maintain higher body
References
[1]
W. E. Cooper and N. Greenberg, “Reptilian coloration and behavior,” in Biology of the Reptilia, C. Gans and D. Crews, Eds., vol. 18, pp. 298–422, University of Chicago Press, Chicago, Ill, USA, 1992.
[2]
M. Andersson, Sexual Selection, Princeton University Press, Princeton, NJ, USA, 1994.
[3]
P. Galeotti, D. Rubolini, P. O. Dunn, and M. Fasola, “Colour polymorphism in birds: causes and functions,” Journal of Evolutionary Biology, vol. 16, no. 4, pp. 635–646, 2003.
[4]
J. A. Endler, “A predator’s view of animal colour patterns,” Evolutionary Biology, vol. 11, pp. 319–364, 1978.
[5]
J. A. Endler, “Natural and sexual selection on color patterns in poeciliid fishes,” Environmental Biology of Fishes, vol. 9, no. 2, pp. 173–190, 1983.
[6]
J. A. Endler, “On the measurement and classification of colour in studies of animal colour patterns,” Biological Journal of the Linnean Society, vol. 41, no. 4, pp. 315–352, 1990.
[7]
J. N. Lythgoe, The Ecology of Vision, Oxford University Press, Oxford, UK, 1979.
[8]
A. Forsman and R. Shine, “The adaptive significance of colour pattern polymorphism in the Australian scincid lizard Lampropholis delicata,” Biological Journal of the Linnean Society, vol. 55, no. 4, pp. 273–291, 1995.
[9]
A. E. Houde, Sex, Color, and Mate-Choice in Guppies, Princeton University Press, Princeton, NJ, USA, 1997.
[10]
Y. Espmark, T. Amundsen, and G. Rosenqvist, Animal Signals: Signalling and Signal Design in Animal Communication, Tapir Academic, Trondheim, Norway, 2000.
[11]
J. A. Endler, “Variation in the appearance of guppy color patterns to guppies and their predators under different visual conditions,” Vision Research, vol. 31, no. 3, pp. 587–608, 1991.
[12]
A. Roulin and M. Wink, “Predator-prey relationships and the evolution of colour polymorphism: a comparative analysis in diurnal raptors,” Biological Journal of the Linnean Society, vol. 81, no. 4, pp. 565–578, 2004.
[13]
J. A. Brisson, J. Wilder, and H. Hollocher, “Phylogenetic analysis of the Cardini group of Drosophila with respect to changes in pigmentation,” Evolution, vol. 60, no. 6, pp. 1228–1241, 2006.
[14]
A. Forsman and V. ？berg, “Associations of variable coloration with niche breadth and conservation status among Australian reptiles,” Ecology, vol. 89, no. 5, pp. 1201–1207, 2008.
[15]
A. Forsman, J. Ahnesj？, S. Caesar, and M. Karlsson, “A model of ecological and evolutionary consequences of color polymorphism,” Ecology, vol. 89, no. 1, pp. 34–40, 2008.
[16]
H. B. Cott, Adaptive Coloration in Animals, Methuen, London, UK, 1940.
[17]
K. S. Norris and C. H. Lowe, “Analysis of background color-matching in amphibians and reptiles,” Ecology, vol. 45, no. 3, pp. 565–580, 1964.
[18]
T. D. Bittner, R. B. King, and J. M. Kerfin, “Effects of body size and melanism on the thermal biology of garter snakes (Thamnophis sirtalis),” Copeia, vol. 2002, no. 2, pp. 477–482, 2002.
[19]
S. Clusella Trullas, J. H. van Wyk, and J. R. Spotila, “Thermal melanism in ectotherms,” Journal of Thermal Biology, vol. 32, no. 5, pp. 235–245, 2007.
[20]
S. Clusella-Trullas, J. H. van Wyk, and J. R. Spotila, “Thermal benefits of melanism in cordylid lizards: a theoretical and field test,” Ecology, vol. 90, no. 8, pp. 2297–2312, 2009.
[21]
K. S. Norris, “Color adaptation in desert reptiles and its thermal relationships,” in Lizard Ecology: A Symposium, W. W. Milstead, Ed., pp. 162–226, University of Missouri Press, Columbia, Mo, USA, 1965.
[22]
J. M. Macedonia, J. F. Husak, Y. M. Brandt, A. K. Lappin, and T. A. Baird, “Sexual dichromatism and color conspicuousness in three populations of collared lizards (Crotaphytus collaris) from Oklahoma,” Journal of Herpetology, vol. 38, no. 3, pp. 340–354, 2004.
[23]
E. B. Rosenblum, “Convergent evolution and divergent selection: lizards at the white sands ecotone,” The American Naturalist, vol. 167, no. 1, pp. 1–15, 2006.
[24]
E. B. Rosenblum, H. R？mpler, T. Sch？neberg, and H. E. Hoekstra, “Molecular and functional basis of phenotypic convergence in white lizards at White Sands,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 5, pp. 2113–2117, 2010.
[25]
A. C. Alberts, “Constraints on the design of chemical communication systems in terrestrial vertebrates,” The American Naturalist, vol. 139, pp. S62–S89, 1992.
[26]
J. A. Endler, “Signals, signal conditions, and the direction of evolution,” The American Naturalist, vol. 139, pp. S125–S153, 1992.
[27]
T. A. Baird, S. F. Fox, and J. K. McCoy, “Population differences in the roles of size and coloration in intra- and intersexual selection in the collared lizard, Crotaphytus collaris: influence of habitat and social organization,” Behavioral Ecology, vol. 8, no. 5, pp. 506–517, 1997.
[28]
S. F. Fox and P. A. Shipman, “Social behavior at high and low elevations: environmental release and phylogenetic effects in Liolaemus,” in Lizard Social Behavior, S. F. Fox, J. K. McCoy, and T. A. Baird, Eds., pp. 310–355, John Hopkins University Press, Baltimore, Md, USA, 2003.
[29]
J. Martín and P. López, “Effects of global warming on sensory ecology of rock lizards: increased temperatures alter the efficacy of sexual chemical signals,” Functional Ecology, vol. 27, no. 6, pp. 1332–1340, 2013.
[30]
D. J. Harris and P. Sá-Sousa, “Species distinction and relationships of the western Iberian Podarcis lizards (Reptilia, Lacertidae) based on morphology and mitochondrial DNA sequences,” Herpetological Journal, vol. 11, no. 4, pp. 129–136, 2001.
[31]
P. Sáa -Sousa, “Molecular phylogenetics of Iberian wall lizards (Podarcis): is Podarcis hispanica a species complex?” Molecular Phylogenetics and Evolution, vol. 23, no. 1, pp. 75–81, 2002.
[32]
C. Pinho, D. J. Harris, and N. Ferrand, “Comparing patterns of nuclear and mitochondrial divergence in a cryptic species complex: the case of Iberian and North African wall lizards (Podarcis, Lacertidae),” Biological Journal of the Linnean Society, vol. 91, no. 1, pp. 121–133, 2007.
[33]
M. A. Carretero, “An integrated assessment of a group with complex systematics: the Iberomaghrebian lizard genus Podarcis (Squamata, Lacertidae),” Integrative Zooloogy, vol. 3, no. 4, pp. 247–266, 2008.
[34]
A. Kaliontzopoulou, C. Pinho, D. J. Harris, and M. A. Carretero, “When cryptic diversity blurs the picture: a cautionary tale from Iberian and North African Podarcis wall lizards,” Biological Journal of the Linnean Society, vol. 103, no. 4, pp. 779–800, 2011.
[35]
E. N. Arnold and J. A. Burton, A Field Guide to the Reptiles and Amphibians of Britain and Europe, Collins, London, UK, 2nd edition, 2002.
[36]
P. Sá-Sousa, L. Vicente, and E. G. Crespo, “Morphological variability of Podarcis hispanica (Sauria: Lacertidae) in Portugal,” Amphibia Reptilia, vol. 23, no. 1, pp. 55–69, 2002.
[37]
M. García-Paris, C. Martín, and J. Dorda, Los Anfibios y Reptiles de Madrid, Ministerio de Agricultura, Pesca y Alimentación, Madrid, Spain, 1989.
[38]
J. Martín and P. López, “Interpopulational differences in chemical composition and chemosensory recognition of femoral gland secretions of male lizards Podarcis hispanica: implications for sexual isolation in a species complex,” Chemoecology, vol. 16, no. 1, pp. 31–38, 2006.
[39]
J. Martín and P. López, “Pre-mating mechanisms favouring or precluding speciation in a species complex: chemical recognition and sexual selection between types in the lizard Podarcis hispanica,” Evolutionary Ecology Research, vol. 8, no. 4, pp. 643–658, 2006.
[40]
M. Gabirot, P. López, and J. Martín, “Differences in chemical sexual signals may promote reproductive isolation and cryptic speciation between Iberian wall lizard populations,” International Journal of Evolutionary Biology, vol. 2012, Article ID 698520, 13 pages, 2012.
[41]
M. Gabirot, P. López, and J. Martín, “Female mate choice based on pheromone content may inhibit reproductive isolation between distinct populations of Iberian wall lizards,” Current Zoology, vol. 59, no. 2, pp. 210–220, 2013.
[42]
P. López and J. Martín, “Pheromonal recognition of females takes precedence over the chromatic cue in male Iberian wall lizards Podarcis hispanica,” Ethology, vol. 107, no. 10, pp. 901–912, 2001.
[43]
P. López, J. Martín, and M. Cuadrado, “Pheromone-mediated intrasexual aggression in male lizards,” Aggressive Behavior, vol. 28, no. 2, pp. 154–163, 2002.
[44]
P. López and J. Martín, “Chemical rival recognition decreases aggression levels in male Iberian wall lizards, Podarcis hispanica,” Behavioral Ecology and Sociobiology, vol. 51, no. 5, pp. 461–465, 2002.
[45]
P. López and J. Martín, “Female Iberian wall lizards prefer male scents that signal a better cell-mediated immune response,” Biology Letters, vol. 1, no. 4, pp. 404–406, 2005.
[46]
P. Carazo, E. Font, and E. Desfilis, “Chemosensory assessment of rival competitive ability and scent-mark function in a lizard, Podarcis hispanica,” Animal Behaviour, vol. 74, no. 4, pp. 895–902, 2007.
[47]
R. Montgomerie, “Analyzing colors,” in Bird Coloration: Volume 1. Mechanisms and Measurements, G. E. Hill and K. J. McGraw, Eds., pp. 90–147, Harvard University Press, Cambridge, Mass, USA, 2006.
[48]
C. P. Grill and V. N. Rush, “Analysing spectral data: comparison and application of two techniques,” Biological Journal of the Linnean Society, vol. 69, no. 2, pp. 121–138, 2000.
[49]
I. C. Cuthill, A. T. D. Bennett, J. C. Partridge, and E. J. Maier, “Plumage reflectance and the objective assessment of avian sexual dichromatism,” The American Naturalist, vol. 153, no. 2, pp. 183–200, 1999.
[50]
R. R. Sokal, F. J. Rohlf, and W. H. Biometry, Biometry, W. H. Freeman, New York, NY, USA, 3rd edition, 1995.
[51]
P. López, J. Martín, and M. Cuadrado, “The role of lateral blue spots in intrasexual relationships between male Iberian rock-lizards, Lacerta monticola,” Ethology, vol. 110, no. 7, pp. 543–561, 2004.
[52]
A. C. Cameron and P. K. Trivedi, Regression Analysis of Count Data, vol. 53 of Econometric Society Monographs, Cambridge University Press, Cambridge, UK, 2nd edition, 2013.
[53]
N. H. Nie, C. H. Hull, J. G. Jenkins, K. Steinberger, and D. H. Bent, Statistical Package for the Social Sciences (SPSS), McGraw-Hill, New York, NY, USA, 1975.
[54]
M. Gabirot, A. Balleri, P. López, and J. Martín, “Differences in thermal biology between two morphologically distinct populations of iberian wall lizards inhabiting different environments,” Annales Zoologici Fennici, vol. 50, no. 4, pp. 225–236, 2013.
[55]
L. M. Carrascal, P. López, J. Martín, and A. Salvador, “Basking and antipredator behaviour in a high altitude lizard: implications of heat-exchange rate,” Ethology, vol. 92, no. 2, pp. 143–154, 1992.
[56]
Y. Yom-Tov and H. Nix, “Climatological correlates for body size of five species of Australian mammals,” Biological Journal of the Linnean Society, vol. 29, no. 4, pp. 245–262, 1986.
[57]
M. á. Olalla-Tárraga, M. á. Rodríguez, and B. A. Hawkins, “Broad-scale patterns of body size in squamate reptiles of Europe and North America,” Journal of Biogeography, vol. 33, no. 5, pp. 781–793, 2006.
[58]
A. D. Leaché, D.-S. Helmer, and C. Moritz, “Phenotypic evolution in high-elevation populations of western fence lizards (Sceloporus occidentalis) in the Sierra Nevada Mountains,” Biological Journal of the Linnean Society, vol. 100, no. 3, pp. 630–641, 2010.
[59]
K. G. Ashton and C. R. Feldman, “Bergmann's rule in nonavian reptiles: turtles follow it, lizards and snakes reverse it,” Evolution, vol. 57, no. 5, pp. 1151–1163, 2003.
[60]
D. Pincheira-Donoso, D. J. Hodgson, and T. Tregenza, “The evolution of body size under environmental gradients in ectotherms: why should Bergmann's rule apply to lizards?” BMC Evolutionary Biology, vol. 8, no. 1, article 68, 2008.
[61]
E. B. Rosenblum and L. J. Harmon, “‘Same same but different’: replicated ecological speciation at white sands,” Evolution, vol. 65, no. 4, pp. 946–960, 2011.
[62]
P. López, M. Gabirot, and J. Martín, “Immune challenge affects sexual coloration of male iberian wall lizards,” Journal of Experimental Zoology A: Ecological Genetics and Physiology, vol. 311, no. 2, pp. 96–104, 2009.
[63]
J. M. Macedonia, S. James, L. W. Wittle, and D. L. Clark, “Skin pigments and coloration in the Jamaican radiation of Anolis lizards,” Journal of Herpetology, vol. 34, no. 1, pp. 99–109, 2000.
[64]
G. F. Grether, G. R. Kolluru, and K. Nersissian, “Individual colour patches as multicomponent signals,” Biological Reviews of the Cambridge Philosophical Society, vol. 79, no. 3, pp. 583–610, 2004.
[65]
L. M. San-Jose, F. Granado-Lorencio, B. Sinervo, and P. S. Fitze, “Iridophores and not carotenoids account for chromatic variation of carotenoid-based coloration in common lizards (Lacerta vivipara),” American Naturalist, vol. 181, no. 3, pp. 396–409, 2013.
[66]
G. F. Grether, J. Hudon, and D. F. Millie, “Carotenoid limitation of sexual coloration along an environmental gradient in guppies,” Proceedings of the Royal Society B: Biological Sciences, vol. 266, no. 1426, pp. 1317–1322, 1999.
[67]
J. A. Endler, “The color of light in forests and its implications,” Ecological Monographs, vol. 63, no. 1, pp. 1–27, 1993.
[68]
C. M. Escobar, C. A. Escobar, A. Labra, and H. M. Niemeyer, “Chemical composition of precloacal secretions of two Liolaemus fabiani populations: are they different?” Journal of Chemical Ecology, vol. 29, no. 3, pp. 629–638, 2003.
[69]
M. Gabirot, P. López, and J. Martín, “Interpopulational variation in chemosensory responses to selected steroids from femoral secretions of male lizards, Podarcis hispanica, mirrors population differences in chemical signals,” Chemoecology, vol. 22, no. 1, pp. 65–73, 2012.
