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Chemically Mediated Species Recognition in Closely Related Podarcis Wall Lizards

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Abstract

In many animals, chemical signals play an important role in species recognition and may contribute to reproductive isolation and speciation. The Iberian lizards of the genus Podarcis, with up to nine currently recognized lineages that are often sympatric, are highly chemosensory and provide an excellent model for the study of chemically mediated species recognition in closely related taxa. In this study, we tested the ability of male and female lizards of two sister species with widely overlapping distribution ranges (Podarcis bocagei and P. hispanica type 1) to discriminate between conspecific and heterospecific mates by using only substrate-borne chemical cues. We scored the number of tongue flicks directed at the paper substrate by each individual in a terrarium previously occupied by a conspecific or a heterospecific lizard of the opposite sex. Results show that males of P. bocagei and P. hispanica type 1 are capable of discriminating chemically between conspecifics and heterospecifics of the opposite sex, but females are not. These results suggest that differences in female, but not male, chemical cues may underlie species recognition and contribute to reproductive isolation in these species. The apparent inability of females to discriminate conspecific from heterospecific males, which is not because of reduced baseline exploration rates, is discussed in the context of sexual selection theory and species discrimination.

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References

  • Alberts, A. C. 1991. Phylogenetic and adaptative variation in lizard femoral gland secretions. Copeia 1991:69–79.

    Article  Google Scholar 

  • Barbosa, D., Desfilis, E., Carretero, M. A., and Font, E. 2005. Chemical stimuli mediate species recognition in Podarcis wall lizards. Amphib-Reptil. 26:257–263.

    Article  Google Scholar 

  • Bininda-Emonds, O. R. P., Decker-Flum, D. M., and Gittleman, J. L. 2001. The utility of chemical signals as phylogenetic characters: an example from Felidae. Biol. J. Linn. Soc. 72:1–15.

    Article  Google Scholar 

  • Blumstein, D. T., Evans, C. S., and Daniel, J. C. 2000. JWatcher version 0.9. Animal Behaviour Lab., Macquarie University, Sydney.

    Google Scholar 

  • Butlin, R. K. and Ritchie, M. G. 1994. Behaviour and speciation, pp 43–79, in P. J. B. Slater and T. R. Halliday (eds.). Behaviour and Evolution. Cambridge University Press, Cambridge.

    Google Scholar 

  • Cooper, W. E., Jr. 1998. Evaluation of swab and related tests as a bioassay for assessing responses by squamate reptiles to chemical stimuli. J. Chem. Ecol. 24:841–866.

    Article  CAS  Google Scholar 

  • Cooper, W. E., Jr. and Burghardt, G. M. 1990. A comparative analysis of scoring methods for chemical discrimination of prey by squamate reptiles. J. Chem. Ecol. 16:45–65.

    Article  Google Scholar 

  • Cooper, W. E., Jr. and Garstka, W. R. 1987. Lingual responses to chemical fractions of urodaeal glandular pheromone of the skink Eumeces laticeps. J. Exp. Zool. 242:249–253.

    Article  CAS  Google Scholar 

  • Cooper, W. E., Jr. and Pérez-Mellado, V. 2002. Pheromonal discrimination of sex, reproductive condition, and species by the lacertid lizard Podarcis hispanica. J. Exp. Zool. 292:523–527.

    Article  PubMed  Google Scholar 

  • Cooper, W. E., Jr. and Vitt, L. J. 1984. Detection of conspecific odors by the female broad-headed skink, Eumeces laticeps. J. Exp. Zool. 229:49–54.

    Article  Google Scholar 

  • Cooper, W. E., Jr. and Vitt, L. J. 1986a. Thermal dependence of tongue-flicking and comments on the use of tongue-flicking as an index of squamate behavior. Ethology 71:177–186.

    Article  Google Scholar 

  • Cooper, W. E., Jr. and Vitt, L. J. 1986b. Tracking female conspecific odor by trails by male broad-headed skinks (Eumeces laticeps). Ethology 71:242–248.

    Google Scholar 

  • Cooper, W. E., Jr. and Vitt, L. J. 1987. Ethological isolation, sexual behavior and pheromones in the Fasciatus species group of the lizard genus Eumeces. Ethology 75:328–336.

    Google Scholar 

  • de Queiroz, A. and Wimberger, P. H. 1993. The usefulness of behavior for phylogeny estimation: levels of homoplasy in behavioral and morphological characters. Evolution 47:46–60.

    Article  Google Scholar 

  • Desfilis, E., Font, E., and Guillén-Salazar, F. 2003. Stimulus control of predatory behavior by the Iberian wall lizard (Podarcis hispanica, Sauria, Lacertidae): effects of familiarity with prey. J. Comp. Psychol. 117:309–316.

    Article  PubMed  Google Scholar 

  • Dial, B. E. and Schwenk, K. 1996. Olfaction and predator detection in Coleonyx brevis (Squamata: Eublepharidae), with comments on the functional significance of buccal pulsing in geckos. J. Exp. Zool. 276:415–424.

    Article  Google Scholar 

  • Eady, P. E. 2001. Postcopulatory, prezygotic reproductive isolation. J. Zool. 253:47–52.

    Article  Google Scholar 

  • Font, E. and Desfilis, E. 2002. Chemosensory recognition of familiar and unfamiliar conspecifics by juveniles of the Iberian wall lizard Podarcis hispanica. Ethology 108:319–330.

    Article  Google Scholar 

  • Gabe, M. and Saint-Girons, H. 1976. Contribution a la morphologie compareé des fosses nasales et de leur annexes chez les Lépidosauriens. Mem. Mus. Natl. Hist. Nat., Ser. A Zool. 98:1–87.

    Google Scholar 

  • Galán, P. 1986. Morfología y distribución del género Podarcis Wagler, 1830 (Sauria, Lacertidae) en el noroeste de la Península Ibérica. Rev. Esp. Herpetol. 1:87–142.

    Google Scholar 

  • Gittleman, J. L. and Decker, M. 1994. The phylogeny of behaviour, pp. 80–105, in P. J. B. Slater and T. R. Halliday (eds.). Behaviour and Evolution. Cambridge University Press, Cambridge.

    Google Scholar 

  • Gómez, A., Font, E., and Desfilis, E. 1993. Chemoreception in the Lacertidae: exploration and conspecific discrimination in the Spanish wall lizard, Podarcis hispanica, pp. 213–230, in E. D. Valakos, V. Pérez-Mellado, and P. Maragou (eds.). Lacertids of the Mediterranean Region: A Biological Approach. Hellenic Zoological Society, Athens.

    Google Scholar 

  • Greenberg, N. 1985. Exploratory behavior and stress in the lizard, Anolis carolinensis. Z. Tierpsychol. 70:89–102.

    Google Scholar 

  • Halpern, M. 1992. Nasal chemical senses in reptiles: structure and function, pp. 423–523, in C. Gans and D. Crews (eds.). Hormones, Brain, and Behavior. Biology of Reptilia, Vol. 18 E. The University of Chicago Press, Chicago.

    Google Scholar 

  • Hamilton, P. S. and Sullivan, B. K. 2005. Female mate attraction in ornate tree lizards (Urosaurus ornatus): a multivariate analysis. Anim. Behav. 69:219–224.

    Article  Google Scholar 

  • Harris, D. J. and Sá-Sousa, P. 2002. Molecular phylogenetics of Iberian wall lizard (Podarcis): is Podarcis hispanica a species complex? Mol. Phylogenet. Evol. 23:75–81.

    Article  PubMed  CAS  Google Scholar 

  • Heth, G., Todrank, J., Busquet, N., and Baudoin, C. 2001. Odour-genes covariance and differential investigation of individual odours in the Mus species complex. Biol. J. Linn. Soc. 73:213–220.

    Article  Google Scholar 

  • Kaliontzopoulou, A., Carretero, M. A., and Llorente, G. A. 2005. Differences in pholidotic patterns of Podarcis bocagei and P. carbonelli and its implications for species determination. Rev. Esp. Herpetol. (in press).

  • Labra, A., Escobar, C. A., and Niemeyer, H. M. 2001. Chemical discrimination in Liolaemus lizards: A comparison of behavioral and chemical data, pp. 437–444, in A. Marchelewska-Koj, F. Lepri and D. Müller-Schwarze (eds.). Chemical Signals in Vertebrates 9. Kluwer Academic/Plenum Publishers, New York.

    Google Scholar 

  • LeBas, N. R. and Marshall, N. J. 2001. No evidence of female choice for a condition-dependent trait in the agamid lizard, Ctenophorus ornatus. Behaviour 138:965–980.

    Article  Google Scholar 

  • LeMaster, M. P. and Mason, R. T. 2003. Pheromonally mediated sexual isolation among denning populations of red-sided garter snakes, Thamnophis sirtalis parietalis. J. Chem. Ecol. 29:1027–1043.

    Article  PubMed  CAS  Google Scholar 

  • LeMaster, M. P., Moore, I. T., and Mason, R. T. 2001. Conspecific trailing behaviour of red-sided garter snakes, Thamnophis sirtalis parietalis, in the natural environment. Anim. Behav. 61:827–833.

    Article  Google Scholar 

  • López, P. and Martín, J. 2001. Pheromonal recognition of females takes precedence over the chromatic cue in male Iberian wall lizards Podarcis hispanica. Ethology 107:901–912.

    Article  Google Scholar 

  • Mas, F. and Jallon, J.-M. 2005. Sexual isolation and cuticular hydrocarbon differences between Drosophila santomea and Drosophila yakuba. J. Chem. Ecol. 31:2747–2752.

    Article  PubMed  CAS  Google Scholar 

  • Mason, R. T. 1992. Reptilian pheromones, pp. 114–228, in C. Gans and D. Crews (eds.). Hormones, Brain, and Behavior. Biology of Reptilia, Vol. 18 E. The University of Chicago Press, Chicago.

    Google Scholar 

  • Mason, R. T. 1993. Chemical ecology of the red-sided garter-snake, Thamnophis sirtalis parietalis. Brain Behav. Evol. 41:261–268.

    CAS  Google Scholar 

  • Olsson, M. and Madsen, T. 1998. Sexual selection and sperm competition in reptiles, pp. 503–577, in T. R. Birkhead and A. P. Møller (eds.). Sperm Competition and Sexual Selection. Academic Press, San Diego.

    Chapter  Google Scholar 

  • Phelan, P. L. and Baker, T. C. 1987. Evolution of male pheromones in moths: reproductive isolation through sexual selection? Science 235:205–207.

    Article  PubMed  CAS  Google Scholar 

  • Pinho, C., Harris, D. J., and Ferrand, N. 2003. Genetic polymorphism of 11 allozyme loci in populations of wall lizards (Podarcis sp.) from the Iberian Peninsula and North Africa. Biochem. Genet. 41:343–359.

    Article  PubMed  CAS  Google Scholar 

  • Pinho, C., Ferrand, N., and Harris, D. J. 2006. Reexamination of the Iberian and North African Podarcis (Squamata: Lacertidae) phylogeny based on increased mitochondrial DNA sequencing. Mol. Phylogenet. Evol. 38:266–273.

    Article  PubMed  CAS  Google Scholar 

  • Ptacek, M. B. 2000. The role of mating preferences in shaping interspecific divergence in mating signals in vertebrates. Behav. Processes 51:111–134.

    Article  PubMed  Google Scholar 

  • Quinn, G. P. and Keough, M. J. 2002. Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge.

    Google Scholar 

  • Roberts, J. A. and Uetz, G. W. 2004. Chemical signaling in a wolf spider: a test of ethospecies discrimination. J. Chem. Ecol. 30:1271–1284.

    Article  PubMed  CAS  Google Scholar 

  • Rypstra, A. L., Wieg, C., Walker, S. E., and Persons, M. H. 2003. Mutual mate assessment in wolf spiders: differences in the cues used by males and females. Ethology 109:315–325.

    Article  Google Scholar 

  • Sá-Sousa, P. 2000. A predictive distribution model for the Iberian wall lizard (Podarcis hispanicus) in Portugal. Herpetol. J. 10:1–11.

    Google Scholar 

  • Sá-Sousa, P. 2001. A controversa sistemática das lagartixas do género Podarcis Wagler, 1830 (Sauria, Lacertidae) em Portugal. Ph.D. dissertation. University of Lisbon, Lisbon.

  • Sá-Sousa, P., Vicente, L., and Crespo, E. G. 2002. Morphological variability of Podarcis hispanica (Sauria: Lacertidae) in Portugal. Amphib-Reptil. 23:55–69.

    Article  Google Scholar 

  • Schwenk, K. 1995. Of tongue and noses: chemoreception in lizards and snakes. Trends Ecol. Evol. 10:7–12.

    Article  Google Scholar 

  • Shine, R., Olsson, M. M., and Mason, R. T. 2000. Chastity belts in gartersnakes: the functional significance of mating plugs. Biol. J. Linn. Soc. 70:377–390.

    Article  Google Scholar 

  • Shine, R., Reed, R. N., Shetty, S., LeMaster, M., and Mason, R. T. 2002. Reproductive isolating mechanisms between two sympatric sibling species of sea snakes. Evolution 56:1655–1662.

    PubMed  Google Scholar 

  • Shine, R., Phillips, B., Waye, H., LeMaster, M., and Mason, R. T. 2003. Chemosensory cues allow courting male garter snakes to assess body length and body condition of potential mates. Behav. Ecol. Sociobiol. 54:162–166.

    Google Scholar 

  • Siegel, S. and Castellan, N. J. 1988. Nonparametric Statistics for the Behavioral Sciences. McGraw-Hill Book Company, New York.

    Google Scholar 

  • Steele, L. J. and Cooper, W. E., Jr. 1997. Investigations of pheromonal discrimination between conspecific individuals by male and female leopard geckos (Eublepharis macularius). Herpetologica 53:475–484.

    Google Scholar 

  • Sutton, R., Bolton, E., Bartels-Hardege, H. D., Eswards, M., Reish, D. J., and Hardege, J. D. 2005. Chemical signal mediated premating reproductive isolation in a marine polychaete, Neanthes acuminata (arenaceodentata). J. Chem. Ecol. 31:1865–1876.

    Article  PubMed  CAS  Google Scholar 

  • Symonds, M. R. E. and Elgar, M. A. 2004. The mode of pheromone evolution: evidence from bark beetles. Proc. R. Soc. Lond. B 271:839–846.

    Article  Google Scholar 

  • Tokarz, R. R. 1995. Mate choice in lizards: A review. Herpetol. Monogr. 9:17–40.

    Article  Google Scholar 

  • Verbeek, B. 1972. Ethologische Untersuchungen an einigen europäischen Eidechsen. Bonn. Zool. Beitr. 23:122–151.

    Google Scholar 

  • Verrell, P. 2003. Population and species divergence of chemical cues that influence male recognition of female in desmognathine salamanders. Ethology 109:577–586.

    Article  Google Scholar 

  • Wyatt, T. D. 2003. Pheromones and Animal Behaviour: Communication by Smell and Taste. Cambridge University Press, Cambridge.

    Google Scholar 

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Acknowledgments

This work was financially supported by project POCTI/BSE/45664/2002 of Fundação para a Ciência e a Tecnologia (FCT, Portugal). D.B. was funded by a Ph.D. grant (SFRH/BD/14084/2003) and M.A.C. by a postdoctoral grant (SFRH/BPD/3596/2000), both also from FCT. We thank two anonymous reviewers for helpful advice and comments and R. Ribeiro, R. Vasconcelos, and D. J. Harris for helping in fieldwork. Animals were collected under permits provided by the Instituto da Conservação da Natureza (ICN, Portugal) and were maintained and treated in accordance with Spanish Law (Real Decreto 223/1988) and Animal Behavior Society Guidelines for the Treatment of Animals in Behavioral Research and Teaching.

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  1. Instituto Cavanilles de Biodiversidad y Biología Evolutiva, Universidad de Valencia, Apartado 22085, 46071, Valencia, Spain

    Diana Barbosa, Enrique Font & Ester Desfilis

  2. CIBIO Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus Agrário de Vairão, 4485-661, Vairão, Portugal

    Diana Barbosa & Miguel A. Carretero

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  1. Diana Barbosa
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  2. Enrique Font
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Correspondence to Diana Barbosa.

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Barbosa, D., Font, E., Desfilis, E. et al. Chemically Mediated Species Recognition in Closely Related Podarcis Wall Lizards. J Chem Ecol 32, 1587–1598 (2006). https://doi.org/10.1007/s10886-006-9072-5

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