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Interpopulational variation in chemosensory responses to selected steroids from femoral secretions of male lizards, Podarcis hispanica, mirrors population differences in chemical signals

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Abstract

Chemical signals are important for mate and species recognition. If variation in chemical signals occurs between populations of the same species, these differences could later preclude mating between populations and lead to speciation. In the Iberian wall lizard, Podarcis hispanica, the lipophilic fraction of femoral secretions of males is mainly a mix of steroids and fatty acids. Among steroids, the most abundant compounds are cholesterol and cholesta-5,7-dien-3-ol, which are implicated in intraspecific communication and sexual selection. Interpopulational differences in chemical signals of males, and in response to these chemicals, could contribute to reproductive isolation between populations, which would explain the known genetic differences between these populations. Chemical analyses indicated that five distinct populations of this lizard from Madrid (Central Spain) differed in the proportions of two steroids (cholesterol and cholesta-5,7-dien-3-ol) in femoral secretions. Moreover, lizards discriminated and had high chemosensory responses (i.e., high tongue-flick rates) to these steroids, but showed interpopulational differences. Lizards from populations with cold temperatures and high relative humidity (i.e., northern Madrid) elicited higher responses to these steroids, whereas the converse occurred for lizards from populations occupying dry and hot habitats (i.e., southern Madrid). Interestingly, the magnitude of the chemosensory responses to cholesta-5,7-dien-3-ol in each population mirrored the abundance of this compound in secretions of males of that population. These results suggest that the importance of cholesta-5,7-dien-3-ol in males’ secretions might be lower for lizards from the southern populations. These differences in the relative importance of chemical signals could explain reproductive isolation and cryptic speciation between populations of this lizard.

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References

  • Aitchison J (1986) The statistical analysis of compositional data: Monographs in statistics and applied probability. Chapman and Hall, London

    Book  Google Scholar 

  • Alberts AC (1992) Pheromonal self-recognition in desert iguanas. Copeia 1992:229–232

    Article  Google Scholar 

  • Alberts AC (1993) Chemical and behavioral studies of femoral gland secretions in iguanid lizards. Brain Behav Evol 41:255–260

    Article  PubMed  CAS  Google Scholar 

  • Alberts AC, Pratt NC, Phillips JA (1992) Seasonal productivity of lizard femoral glands: relationships to social dominance and androgen levels. Physiol Behav 51:729–733

    Article  PubMed  CAS  Google Scholar 

  • Aragón P, López P, Martín J (2001) Chemosensory discrimination of familiar and unfamiliar conspecifics by lizards: implications of field spatial relationships between males. Behav Ecol Sociobiol 50:128–133

    Article  Google Scholar 

  • Arnold EN, Ovenden DW (2002) A field guide to the Reptiles and Amphibians of Britain and Europe. Harper Collins, London

    Google Scholar 

  • Barbosa D, Font E, Desfilis E, Carretero MA (2006) Chemically mediated species recognition in closely related Podarcis wall lizards. J Chem Ecol 32:1587–1598

    Article  PubMed  CAS  Google Scholar 

  • Boughman JW (2002) How sensory drive can promote speciation. Trends Ecol Evol 17:571–577

    Article  Google Scholar 

  • Branham MA, Wenzel JW (2003) The origin of photic behavior and the evolution of sexual communication in fireflies (Coleoptera: Lampyridae). Cladistics 19:1–22

    Article  Google Scholar 

  • Carazo P, Font E, Desfilis E (2007) Chemosensory assessment of rival competitive ability and scent mark function in a lizard (Podarcis hispanica). Anim Behav 74:895–902

    Article  Google Scholar 

  • Carazo P, Font E, Desfilis E (2008) Beyond ‘nasty neighbours’ and ‘dear enemies’? Individual recognition by scent marks in a lizard (Podarcis hispanica). Anim Behav 76:1953–1963

    Article  Google Scholar 

  • Carman EN, Ferguson GW, Gehrmann WH, Chen TC, Holick MF (2000) Photobiosynthetic opportunity and ability for UVB generated vitamin D synthesis in free living house geckos (Hemidactylus turcicus) and Texas spiny lizards (Sceloporus olivaceous). Copeia 2000:245–250

    Article  Google Scholar 

  • Carretero MA (2008) An integrated assessment of a group with complex systematics: the Iberomaghrebian lizard genus Podarcis (Squamata, Lacertidae). Integr Zool 4:247–266

    Article  Google Scholar 

  • Cooper WE (1994) Chemical discrimination by tongue-flicking in lizards: a review with hypotheses on its origin and its ecological and phylogenetic relationships. J Chem Ecol 20:439–487

    Article  CAS  Google Scholar 

  • Cooper WE, Burghardt GM (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 WE, Pérez-Mellado V (2002) Pheromonal discrimination of sex, reproductive condition, and species by the lacertid lizard Podarcis hispanica. J Exp Zool A 292:523–527

    Article  Google Scholar 

  • Cooper WE, Vitt LJ (1986) Interspecific odour discrimination among syntopic congeners in Scincid lizards (genus Eumeces). Behaviour 97:1–9

    Article  Google Scholar 

  • Cooper WE, Vitt LJ (1987) Ethological isolation, sexual behavior and pheromones in the fasciatus species group of the lizard genus Eumeces. Ethology 75:328–336

    Article  Google Scholar 

  • Dietemann V, Peeters C, Liebig J, Thivet V, Hölldobler B (2003) Cuticular hydrocarbons mediate discrimination of reproductives and nonreproductives in the ant Myrmecia gulosa. Proc Natl Acad Sci USA 100:10341–10346

    Article  PubMed  CAS  Google Scholar 

  • Escobar CM, Escobar CA, Labra A, Niemeyer HM (2003) Chemical composition of precloacal secretions of two Liolaemus fabiani populations: are they different? J Chem Ecol 29:629–638

    Article  PubMed  CAS  Google Scholar 

  • Fraser DR (1995) Vitamin D. Lancet 345:104–107

    Article  PubMed  CAS  Google Scholar 

  • García-Paris M, Martín C, Dorda J (1989) Los Anfibios y Reptiles de Madrid. Ministerio de Agricultura, Pesca y Alimentación, Madrid

  • Guillaume CP (1987) Les petits Lacertidés du Bassin Mediterranéen Occidental (Genera Podarcis et Archeolacerta essentiellement). PhD Thesis. Univ. Sci. Techn. Langedoc, Montpellier, France

  • Harris DJ, Sá-Sousa P (2001) Species distinction and relationships of the western Iberian Podarcis lizards (Reptilia, Lacertidae) based on morphology and mitochondrial DNA sequences. Herpetol J 11:129–136

    Google Scholar 

  • Harris DJ, Sá-Sousa P (2002) Molecular phylogenetics of Iberian wall lizards (Podarcis): is Podarcis hispanica a species complex? Mol Phyl Evol 23:75–81

    Article  CAS  Google Scholar 

  • Hayes CE, Nashold FE, Spach KM, Pedersen LB (2003) The immunological functions of the vitamin D endocrine system. Cell Mol Biol 49:277–300

    PubMed  CAS  Google Scholar 

  • Kaliontzopoulou A, Pinho C, Harris DJ, Carretero MA (2011) When cryptic diversity blurs the picture: a cautionary tale from Iberian and North African Podarcis wall lizards. Biol J Linn Soc 103:779–800

    Article  Google Scholar 

  • Laing CJ, Fraser DR (1999) The vitamin D system in iguanian lizards. Comp Biochem Physiol B 123:373–379

    Article  Google Scholar 

  • LeMaster MP, Mason RT (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 

  • López P, 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 

  • López P, Martín J (2002) Chemical rival recognition decreases aggression levels in male Iberian wall lizards, Podarcis hispanica. Behav Ecol Sociobiol 51:461–465

    Article  Google Scholar 

  • López P, Martín J (2005) Female Iberian wall lizards prefer male scents that signal a better cell-mediated immune response. Biol Lett 1:404–406

    Article  PubMed  Google Scholar 

  • López P, Martín J, Cuadrado M (2002) Pheromone mediated intrasexual aggression in male lizards, Podarcis hispanicus. Aggress Behav 28:154–163

    Article  Google Scholar 

  • López P, Gabirot M, Martín J (2009a) Immune activation affects chemical sexual ornaments of male Iberian wall lizards. Naturwiss 96:65–69

    Article  PubMed  Google Scholar 

  • López P, Gabirot M, Martín J (2009b) Immune challenge affects sexual coloration of male Iberian wall lizards. J Exp Zool A 311:96–104

    Google Scholar 

  • Martín J, López P (2000) Chemoreception, symmetry and mate choice in lizards. Proc R Soc Lond B 267:1265–1269

    Article  Google Scholar 

  • Martín J, López P (2006a) Links between male quality, male chemical signals, and female mate choice in Iberian rock lizards. Funct Ecol 20:1087–1096

    Article  Google Scholar 

  • Martín J, López P (2006b) Chemosensory responses by female Iberian wall lizards, Podarcis hispanica, to selected lipids found in femoral gland secretions of males. J Herpetol 60:556–561

    Article  Google Scholar 

  • Martín J, López P (2006c) 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. Chemoecol 16:31–38

    Article  Google Scholar 

  • Martín J, López P (2006d) Pre-mating mechanisms favoring or precluding speciation in a species complex: chemical recognition and sexual selection between types in the lizard Podarcis hispanica. Evol Ecol Res 8:643–658

    Google Scholar 

  • Martín J, López P (2007) Scent may signal fighting ability in male Iberian rock lizards. Biol Lett 3:125–127

    Article  PubMed  Google Scholar 

  • Martín J, López P (2011) Pheromones and reproduction in Reptiles. In: Norris DO, Lopez KK (eds) Hormones and reproduction of vertebrates, vol 3. Reptiles. Academic Press, San Diego, pp 141–167

    Chapter  Google Scholar 

  • Martín J, Moreira PL, López P (2007) Status-signaling chemical badges in male Iberian rock lizards. Funct Ecol 21:568–576

    Article  Google Scholar 

  • Mas F, Jallon JM (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 RT (1992) Reptilian pheromones. In: Gans C (ed) Biology of reptilia: hormones, brain, and behavior. Physiology, vol 18. The University of Chicago Press, Chicago and London, pp 114–228

    Google Scholar 

  • Mason RT, Parker MR (2010) Social behavior and pheromonal communication in reptiles. J Comp Phys A 196:729–749

    Article  CAS  Google Scholar 

  • Mellado J, Olmedo G (1981) Sobre las poblaciones de Podarcis en el Macizo de Guadarrama. Doñana Acta Vertebr 8:299–300

    Google Scholar 

  • Olsson M, Madsen T, Nordby J, Wapstra E, Ujvari B, Wittsell H (2003) Major histocompatibility complex and mate choice in sand lizards. Proc R Soc Lond B, Suppl 270:254–256

    Article  Google Scholar 

  • Pinho C, Harris DJ, Ferrand N (2007) Comparing patterns of nuclear and mitochondrial divergence in a cryptic species complex: the case of Iberian and North African wall lizards (Podarcis, Lacertidae). Biol J Linn Soc 91:121–133

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Shine R, Reed RN, Shetty S, Lemaster M, Mason RT (2002) Reproductive isolating mechanisms between two sympatric sibling species of sea snakes. Evolution 56:1655–1662

    PubMed  Google Scholar 

  • Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral sciences, 2nd edn. McGraw-Hill, New York

    Google Scholar 

  • Smadja C, Butlin RK (2009) On the scent of speciation: the chemosensory system and its role in premating isolation. Heredity 102:77–97

    Article  PubMed  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. Freeman, New York

    Google Scholar 

  • Symonds MRE, Elgar MA (2009) The evolution of pheromone diversity. Trends Ecol Evol 23:220–228

    Article  Google Scholar 

  • Weldon PJ, Flachsbarth B, Schulz S (2008) Natural products from the integument of nonavian reptiles. Nat Prod Rep 25:738–756

    Article  PubMed  CAS  Google Scholar 

  • Wyatt TD (2003) Pheromones and animal behaviour: communication by smell and taste. Cambridge University Press, New York

    Book  Google Scholar 

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Acknowledgments

We thank two anonymous reviewers for helpful comments, and “El Ventorrillo” MNCN Field Station for use of their facilities. Financial support was provided by the projects MCI-CGL2008-02119/BOS and MICIIN-CGL2011-24150/BOS, and by an “El Ventorrillo” CSIC grant to MG. The Spanish Meteorological Agency ‘Agencia Estatal de Metereología (AEMET)’ kindly provided climatic data. Captures and experiments enforced all the present Spanish laws and were performed under license from the Environmental Agency of Madrid Government (“Consejería del Medio Ambiente de la Comunidad de Madrid”, Spain).

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  1. Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, C.S.I.C., José Gutiérrez Abascal 2, 28006, Madrid, Spain

    Marianne Gabirot, Pilar López & José Martín

  2. Department Ecologie Comportementale, (U.M.R. 5175), CEFE-CNRS, 1919 Route de Mende, 34293, Montpellier, Cedex 5, France

    Marianne Gabirot

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  1. Marianne Gabirot
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Correspondence to José Martín.

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Gabirot, M., López, P. & Martín, J. Interpopulational variation in chemosensory responses to selected steroids from femoral secretions of male lizards, Podarcis hispanica, mirrors population differences in chemical signals. Chemoecology 22, 65–73 (2012). https://doi.org/10.1007/s00049-011-0100-8

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