Immunocompetence and parasite infestation in a melanistic and normally-coloured population of the lacertid lizard, Podarcis siculus
In: Amphibia-ReptiliaMuseum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA
Search for other papers by Simon Baeckens in
Current site
Google Scholar
Search for other papers by Raoul Van Damme in
Current site
Google Scholar
Abstract
Melanism is the occurrence of individuals that are darker in skin pigmentation than their conspecifics, which is a common colour polymorphism among vertebrates. Due to the pleotropic effects of the POMC gene that is responsible for melanin-based colouration, dark pigmentation often co-varies with a range of other phenotypic traits. Still, not much is known on the link between melanin-based colouration and immunity in lizards. In this study, we examined and compared the immunocompetence and degree of ectoparasite infestation of Podarcis siculus lizards from a fully melanistic population on an islet in the Tyrrhenian Sea, with conspecifics from a ‘normally’-coloured population on the mainland. Our findings show that both males and females from the melanistic population were less parasitized by ectoparasites and had a greater cellular immune response to a phytohemagglutinin injection than normally-coloured conspecifics. This outcome is in line with the “genetic link hypothesis”, which predicts that melanistic individuals will be more resistant to parasites than non-melanistic individuals due to the pleiotropic POMC gene. In addition, we found correlative evidence for a link between ectoparasite load and PHA immune response, but this was only true for males from the normally-coloured population. Immunological data on additional melanistic and non-melanistic populations of Podarcis siculus in the Mediterranean basin would provide us better insight into patterns of co-variation between immunity and melanism in lizards.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
-
Amo, L., Fargallo, J.A., Martínez-Padilla, J., Millán, J., López, P., Martín, J. (2005): Prevalence and intensity of blood and intestinal parasites in a field population of a Mediterranean lizard, Lacerta lepida. Parasitol. Res. 96: 413-417.
-
Belliure, J., Smith, L., Sorci, G. (2004): Effect of testosterone on t cell-mediated immunity in two species of Mediterranean lacertid lizards. J. Exp. Zool. A. Comp. Exp. Biol. 301: 411-418.
-
Berger, S., Martin II, L.B., Wikelski, M., Romero, L.M., Kalko, E.K.V., Vitousek, M.N., Rödl, T. (2005): Corticosterone suppresses immune activity in territorial Galapagos marine iguanas during reproduction. Horm. Behav. 47: 419-429.
-
Bittner, T.D., King, R.B. (2003): Gene flow and melanism in garter snakes revisited: a comparison of molecular markers and island vs. coalescent models. Biol. J. Linn. Soc. 79: 389-399.
-
Brito, S.V., Ferreira, F.S., Ribeiro, S.C., Anjos, L.A., Almeida, W.O., Mesquita, D.O., Vasconcellos, A. (2014): Spatial-temporal variation of parasites in Cnemidophorus ocellifer (Teiidae) and Tropidurus hispidus and Tropidurus semitaeniatus (Tropiduridae) from Caatinga areas in northeastern Brazil. Parasitol. Res. 113: 1163-1169.
-
Case, T.J., Bolger, D.T. (1991): The role of interspecific competition in the biogeography of island lizards. Trends Ecol. Evol. 6: 135-139.
-
Clusella-Trullas, S., van Wyk, J.H., Spotila, J.R. (2007): Thermal melanism in ectotherms. J. Therm. Biol. 32: 235-245.
-
Clusella-Trullas, S., Terblanche, J.S., Blackburn, T.M., Chown, S.L. (2008): Testing the thermal melanism hypothesis: a macrophysiological approach. Funct. Ecol. 22: 232-238.
-
Clusella-Trullas, S., Van Wyk, J.H., Spotila, J.R. (2009): Thermal benefits of melanism in cordylid lizards: a theoretical and field test. Ecology 90: 2297-2312.
-
Cooper, W.E., Pérez-Mellado, V. (2012): Historical influence of predation pressure on escape by Podarcis lizards in the Balearic Islands. Biol. J. Linn. Soc. 107: 254-268.
-
Daniels, S.R., Mouton, P.le F.N., Toit, D.A. (2004): Molecular data suggest that melanistic ectotherms at the south-western tip of Africa are the products of Miocene climatic events: evidence from cordylid lizards. J. Zool. 263: 373-383.
-
Ducrest, A.L., Keller, L., Roulin, A. (2008): Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol. Evol. 23: 502-510.
-
Endler, J. (1984): Progressive background matching in moths, and a quantitative measure of crypsis. Biol. J. Linn. Soc. 2: 187-231.
-
Gasparini, J., Bize, P., Piault, R., Wakamatsu, K., Blount, J.D., Ducrest, A.L., Roulin, A. (2009): Strength and cost of an induced immune response are associated with a heritable melanin-based colour trait in female tawny owls. J. Anim. Ecol. 78: 608-616.
-
Gibson, A.R. (1978): The ecological significance of a colour polymorphism in the common garter snake, Thamnophis sirtalus (L.). Unpublished Ph.D. Dissertation, University of Toronto, Toronto.
-
Gunn, A. (1998): The determination of larval phase coloration in the African armyworm, Spodoptera exempta and its consequences for thermoregulation and protection from UV light. Entomol. Exp. Appl. 86: 125-133.
-
Hoekstra, H.E. (2006): Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity 97: 222-234.
-
Huyghe, K., Husak, J.F., Herrel, A., Tadić, Z., Moore, I.T., Van Damme, R., Vanhooydonck, B. (2009): Relationships between hormones, physiological performance and immunocompetence in a color-polymorphic lizard species, Podarcis melisellensis. Horm. Behav. 55: 488-494.
-
Jacquin, L., Lenouvel, P., Haussy, C., Ducatez, S., Gasparini, J. (2011): Melanin-based coloration is related to parasite intensity and cellular immune response in an urban free living bird: the feral pigeon Columba livia. J. Avian Biol. 42: 11-15.
-
Kennedy, M.W., Nager, R.G. (2006): The perils and prospects of using phytohaemagglutinin in evolutionary ecology. Trends Ecol. Evol. 21: 653-655.
-
Kettlewell, H.B.D. (1973): The Evolution of Melanism: the Study of a Recurring Necessity, With Special Reference to Industrial Melanism in the Lepidoptera. Clarendon Press, Oxford.
-
Korsos, Z., Nagy, Z.T. (2006): Short report on a completely melanistic specimen of the East European green lizard Lacerta viridis (Laurenti, 1768), in Hungary. Eidechse 17: 42-46.
-
Martin, L.B., Han, P., Lewittes, J., Kuhlman, J.R., Klasing, K.C., Wikelski, M. (2006): Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct. Ecol. 20: 290-299.
-
Monti, D.M., Raia, P., Vroonen, J., Maselli, V., Van Damme, R., Fulgione, D. (2013): Physiological change in an insular lizard population confirms the reversed island syndrome. Biol. J. Linn. Soc. 108: 144-150.
-
Nevo, E. (1978): Genetic variation in natural populations: patterns and theory. Theor. Popul. Biol. 13: 121-177.
-
Nieberding, C., Morand, S., Libois, R., Michaux, J.R. (2006): Parasites and the island syndrome: the colonization of the western Mediterranean islands by Heligmosomoides polygyrus (Dujardin, 1845). J. Biogeogr. 33: 1212-1222.
-
Oppliger, A., Clobert, J., Lecomte, J., Boudjemadi, K. (1998): Environmental stress increases the prevalence and intensity of blood parasite infection in the common lizard Lacerta vivipara. Ecol. Lett. 1: 129-138.
-
Oppliger, A., Giorgi, M.S., Conelli, A., Nembrini, M., John-Alder, H.B. (2004): Effect of testosterone on immunocompetence, parasite load, and metabolism in the common wall lizard (Podarcis muralis). Can. J. Zool. 82: 1713-1719.
-
Ortega, Z., Pérez-Mellado, V. (2017): The effect of thermal requirements on microhabitat selection and activity of Podarcis lilfordi (Squamata: Lacertidae). Salamandra 53: 351-358.
-
Pereira, L.K.J., Galdino, C.A.B., Nascimento, L.B. (2014): Tropidophorus torquatus melanism. Herp. Rev. 45: 334.
-
Pérez-Mellado, V. (1984): Sobre un ejemplar melánico de Podarcis hispanica (Steindachner 1870). Doñana, Acta Vert. 11: 320-321.
-
Pérez-Mellado, V., Corti, C., Lo Cascio, P. (1997): Tail autotomy and extinction in Mediterranean lizards: a preliminary study of continental and insular populations. J. Zool. 243: 533-541.
-
Poulin, R. (2006): Variation in infection parameters among populations within parasite species: intrinsic properties versus local factors. Int. J. Parasitol. 36: 877-885.
-
Raia, P., Guarino, F.M., Turano, M., Polese, G., Rippa, D., Carotenuto, F., Monti, D.M., Cardi, M., Fulgione, D. (2010): The blue lizard spandrel and the island syndrome. BMC Evol. Biol. 10: 289.
-
Rosenblum, E.B. (2006): Convergent evolution and divergent selection: lizards at the White Sands Ecotone. Am. Nat. 167: 1-15.
-
Roulin, A., Ducrest, A.L. (2011): Association between melanism, physiology and behaviour: a role for the melanocortin system. Eur. J. Pharmacol. 660: 226-233.
-
Roulin, A., Jungi, T.W., Pfister, H., Dijkstra, C. (2000): Female barn owls (Tyto alba) advertise good genes. Proc. R. Soc. Lond. 267: 937-941.
-
Roulin, A., Riols, C., Dijkstra, C., Ducrest, A.L. (2001): Female plumage spottiness and parasite resistance in the barn owl (Tyto alba). Behav. Ecol. 12: 103-110.
-
Runemark, A., Hansson, B., Pafilis, P., Valakos, E.D., Svensson, E.I. (2010): Island biology and morphological divergence of the Skyros wall lizard Podarcis gaigeae: a combined role for local selection and genetic drift on color morph frequency divergence? BMC Evol. Biol. 10: 269.
-
San-Jose, L.M., Gonzalez-Jimena, V. (2008): Frequency and phenotypic differences of melanistic and normally colored common lizards, Lacerta (Zootoca) vivipara of the southern Pyrenees (Spain). Herpetol. Rev. 39: 422-425.
-
Santiago-Alarcon, D., Whiteman, N.K., Parker, P.G., Ricklefs, R.E., Valkiu, G. (2008): Patterns of parasite abundance and distribution in island populations of Galápagos endemic birds. J. Parasitol. 94: 584-590.
-
Seddon, R.J., Hews, D.K. (2016): Phenotypic correlates of melanization in two Sceloporus occidentalis (Phrynosomatidae) populations: behavior, androgens, stress reactivity, and ectoparasites. Physiol. Behav. 163: 70-80.
-
Tanaka, K. (2007): Thermal biology of a colour-dimorphic snake, Elaphe quadrivirgata, in a montane forest: do melanistic snakes enjoy thermal advantages? Biol. J. Linn. Soc. 92: 309-322.
-
Trapanese, M., Buglione, M., Maselli, V., Petrelli, S., Aceto, S., Fulgione, D. (2017): The first transcriptome of Italian wall lizard, a new tool to infer about the Island Syndrome. PLOS One 12: e0185227.
-
Trocsanyi, B., Korsos, Z. (2004): Recurring melanism in a population of the common wall lizard: numbers and phenotypes. Salamandra 40: 81-90.
-
True, J.R. (2003): Insect melanism: the molecules matter. Trends Ecol. Evol. 18: 640-647.
-
Turner, J.R.G. (1977): Butterfly mimicry: the genetical evolution of an adaptation. Evol. Biol. 10: 163-206.
-
Vervust, B., Grbac, I., Van Damme, R. (2007): Differences in morphology, performance and behaviour between recently diverged populations of Podarcis sicula mirror differences in predation pressure. Oikos 116: 1343-1352.
-
Vroonen, J., Vervust, B., Van Damme, R. (2013): Melanin-based colouration as a potential indicator of male quality in the lizard Zootoca vivipara (Squamata: Lacertidae). Amphibia-Reptilia 34: 539-549.
-
Wiernasz, D.C. (1989): Female choice and sexual selection of male wing melanin pattern in Pieris occidentalis (Lepidoptera). Evolution 43: 1672-1682.
-
Wilson, K., Lotter, S.C., Reeson, A.F., Pell, J.K. (2001): Melanism and disease resistance in insects. Ecol. Lett. 4: 637-649.
-
Zuffi, M. (1986): Su Podarcis muralis maculiventris (Werner, 1891) melanica in risaia a Bereguardo (Pavia) (Reptilia Lacertidae). Atti. Soc. Ital. Sci. Nat. Mus. Civ. Stor. Nat. Milano 127: 293-296.
| All Time | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 942 | 119 | 10 |
| Full Text Views | 229 | 7 | 2 |
| PDF Views & Downloads | 100 | 10 | 4 |
Immunocompetence and parasite infestation in a melanistic and normally-coloured population of the lacertid lizard, Podarcis siculus
In: Amphibia-ReptiliaMuseum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA
Search for other papers by Simon Baeckens in
Current site
Google Scholar
PubMed
Search for other papers by Raoul Van Damme in
Current site
Google Scholar
PubMed
Abstract
Melanism is the occurrence of individuals that are darker in skin pigmentation than their conspecifics, which is a common colour polymorphism among vertebrates. Due to the pleotropic effects of the POMC gene that is responsible for melanin-based colouration, dark pigmentation often co-varies with a range of other phenotypic traits. Still, not much is known on the link between melanin-based colouration and immunity in lizards. In this study, we examined and compared the immunocompetence and degree of ectoparasite infestation of Podarcis siculus lizards from a fully melanistic population on an islet in the Tyrrhenian Sea, with conspecifics from a ‘normally’-coloured population on the mainland. Our findings show that both males and females from the melanistic population were less parasitized by ectoparasites and had a greater cellular immune response to a phytohemagglutinin injection than normally-coloured conspecifics. This outcome is in line with the “genetic link hypothesis”, which predicts that melanistic individuals will be more resistant to parasites than non-melanistic individuals due to the pleiotropic POMC gene. In addition, we found correlative evidence for a link between ectoparasite load and PHA immune response, but this was only true for males from the normally-coloured population. Immunological data on additional melanistic and non-melanistic populations of Podarcis siculus in the Mediterranean basin would provide us better insight into patterns of co-variation between immunity and melanism in lizards.
| All Time | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 942 | 119 | 10 |
| Full Text Views | 229 | 7 | 2 |
| PDF Views & Downloads | 100 | 10 | 4 |