Skip to main content
SpringerLink
Log in

Chemical polymorphism in male femoral gland secretions matches polymorphic coloration in common wall lizards (Podarcis muralis)

  • Research Paper
  • Published:
Chemoecology Aims and scope Submit manuscript

Abstract

Previous studies showed that common wall lizards (Podarcis muralis) are polymorphic in colour, both sexes showing three main ventral morphs (white, yellow and red) within the same population and that the three morphs correlate with many life-history traits, including a positive assortative mating according to colour. Chemical communication plays a key role in intra-specific recognition and in social organization of lizards; thus chemical cues might be involved in morph recognition and mate choice. We used gas chromatography–mass spectrometry (GC–MS) to investigate possible differences in the lipophilic fraction of femoral gland secretions between size/age classes and to explore whether chemical secretions match male colour morphs. As expected, most males shared the same compounds, but smaller males showed significantly higher proportions of aldehydes, alcohols and ketones and significantly lower proportions of tocopherols than larger males. Interestingly, inter-morph differences in the proportion of some compounds (especially tocopherols and furanones) matched ventral colour polymorphism. Pairwise comparisons showed that white lizards had significantly different chemical profiles than both the yellow and red ones, whereas differences between yellow and red males were only marginal. A further canonical analysis of principal coordinates correctly classified 67.2 % on average of the chemical profiles according to colour morph (white 85.0 %, red 60.9 %, yellow 57.1 %). We hypothesized that chemical differences associated with colour polymorphism may play a central role in intra-specific communication and even in sexual selection, allowing individuals to choose their partners according to their age, and more interestingly according to their colour morph, in a non-random mating population system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Aebischer NJ, Robertson PA, Kenward RE (1993) Compositional analysis of habitat use from animal radio-tracking data. Ecology 74:1313–1325

    Article  Google Scholar 

  • Ahnesjö J, Forsman A (2006) Correlated evolution of colour pattern and body size in polymorphic pygmy grasshoppers, Tetrix undulata. J Evol Biol 16:1308–1318

    Article  Google Scholar 

  • Alberts AC (1990) Chemical properties of femoral gland secretions in the desert iguana, Dipsosaurus dorsalis. J Chem Ecol 16:13–25

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Alberts AC, Sharp TR, Werner DI, Weldon PJ (1992) Seasonal variation of lipids in femoral gland secretions of male green iguanas, Iguana iguana. J Chem Ecol 18:703–712

    Article  CAS  PubMed  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525

    Article  Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E Ltd, Plymouth

    Google Scholar 

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

    Article  Google Scholar 

  • Bellati A (2012) Intra- and inter-population analysis of colour polymorphism in Podarcis muralis (Sauria: Lacertidae) using mitochondrial and nuclear markers. PhD thesis, University of Pavia, Pavia

  • Bellati A, Pellitteri-Rosa D, Sacchi R, Nistri AM, Galimberti A, Casiraghi M, Fasola M, Galeotti P (2011) Molecular survey of morphological subspecies reveals new mitochondrial lineages in Podarcis muralis (Squamata: Lacertidae) from the Tuscan Archipelago (Italy). J Zool Syst Evol Res 49:240–250

    Article  Google Scholar 

  • Biaggini M, Bombi P, Capula M, Corti C (2011) Lucertola muraiola Podarcis muralis. In: Corti C, Capula M, Luiselli L, Razzetti E, Sindaco R (eds) Fauna d’Italia—Reptilia. Calderini, Bologna, pp 391–401

    Google Scholar 

  • Calsbeek B, Hasselquist D, Clobert J (2010) Multivariate phenotypes and the potential for alternative phenotypic optima in wall lizard (Podarcis muralis) ventral colour morphs. J Evol Biol 23:1138–1147

    Article  PubMed  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 

  • Carpenter GC (1995) The ontogeny of a variable social badge: throat color development in tree lizards. J Herpetol 29:7–13

    Article  Google Scholar 

  • Cheylan M (1988) Variabilité phénotypique du Lézard des murailles Podarcis muralis sur les isle de la côte provençale, France. Rev Ecol 43:287–321

    Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E Ltd, Plymouth

    Google Scholar 

  • Colin SJ (1999) The naturally occurring furanones: formation and function from pheromone to food. Biol Rev Camb Philos Soc 74:259–276

    Article  Google Scholar 

  • Cooper WE Jr (1994) Prey chemical discrimination, foraging mode, and phylogeny. In: Pianka ER, Vitt LJ (eds) Lizard ecology: historical and experimental perspectives. Princeton University Press, Princeton, pp 95–116

    Google Scholar 

  • Cooper WE, Burns N Jr (1987) Social significance of ventrolateral coloration in the fence lizard, Sceloporus undulatus. Anim Behav 35:526–532

    Article  Google Scholar 

  • Cooper WE, Perez-Mellado V, Vitt LJ (2002) Responses to major categories of food chemicals by the lizard Podarcis lilfordi. J Chem Ecol 28:709–720

    Article  CAS  PubMed  Google Scholar 

  • Cote J, Meylan S, Clobert J, Voituron Y (2010) Carotenoid based coloration, oxidative stress and corticosterone in common lizards. J Exp Biol 213:2116–2124

    Google Scholar 

  • Dawkins R, Krebs JR (1978) Animal signals: information or manipulation. In: Krebs JR, Davies NB (eds) Behavioural ecology. Sinauer Associates, Sunderland, pp 282–309

    Google Scholar 

  • Díaz JA, Alonso-Gómez AL, Delgado MJ (1994) Seasonal variation of gonadal development, sexual steroids, and lipid reserves in a population of the lizard Psammodromus algirus. J Herpetol 28:199–205

    Article  Google Scholar 

  • Elmer KR, Lehtonen TK, Meyer A (2009) Color assortative mating contributes to sympatric divergence of neotropical cichlid fish. Evolution 63:2750–2757

    Article  PubMed  Google Scholar 

  • Escobar CA, Labra A, Niemeyer HM (2001) Chemical composition of precloacal secretions of Liolaemus lizards. J Chem Ecol 27:1677–1690

    Article  CAS  PubMed  Google Scholar 

  • Fitze PS, Cote J, San-Jose LM, Meylan S, Isaksson C, Andersson S, Rossi J-M, Clobert J (2009) Carotenoid-based colours reflect the stress response in the common lizard. PLoS One 4:e5111

    Google Scholar 

  • Gabirot M, López P, Martín J, de Fraipont M, Heulin B, Sinervo B, Clobert J (2008) Chemical composition of femoral secretions of oviparous and viviparous types of male common lizards Lacerta vivipara. Biochem Syst Ecol 36:539–544

    Article  CAS  Google Scholar 

  • Gabirot M, Castilla AM, López P, Martín J (2010) Differences in chemical signals may explain species recognition between an island lizard, Podarcis atrata, and related mainland lizards, P hispanica. Biochem Syst Ecol 38:521–528

    Article  CAS  Google Scholar 

  • Gabirot M, López P, Martín J (2012) 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

    Article  CAS  Google Scholar 

  • Galeotti P, Pellitteri-Rosa D, Sacchi R, Gentilli A, Pupin F, Rubolini D, Fasola M (2010) Sex-, morph- and size-specific susceptibility to stress measured by haematological variables in captive common wall lizard Podarcis muralis. Comp Biochem Physiol A 157:354–363

    Article  Google Scholar 

  • Galeotti P, Sacchi R, Pellitteri-Rosa D, Bellati A, Cocca W, Gentilli A, Scali S, Fasola M (2013) Colour polymorphism and alternative breeding strategies: effects of parent’s colour morph on fitness traits in the common wall lizard. Evol Biol 40:385–394

    Article  Google Scholar 

  • Halpern M (1992) Nasal chemical senses in reptiles: structure and function. In: Gans C, Crews D (eds) Biology of the Reptilia, vol 18., PhysiologyUniversity of Chicago Press, Chicago, pp 424–532

    Google Scholar 

  • Huyghe K, Vanhooydonck B, Herrel A, Tadić Z, Van Damme R (2007) Morphology, performance, behavior and ecology of three color morphs in male of the lizard Podarcis melisellensis. Integr Comp Biol 47:211–220

    Article  PubMed  Google Scholar 

  • Huyghe K, Husak JF, Herrel A, Tadic Z, Moore IT, 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

    Article  CAS  PubMed  Google Scholar 

  • Kopena R, López P, Martín J (2009) Lipophilic compounds from the femoral gland secretions of male Hungarian green lizards, Lacerta viridis. Z Naturforsch C 64:434–440

    CAS  PubMed  Google Scholar 

  • Kopena R, Martín J, López P, Herczeg G (2011) Vitamin E supplementation increases the attractiveness of males’ scent for female European green lizards. PLoS ONE 6(4):e19410

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kopena R, López P, Martín J (2014) Relative contribution of dietary carotenoids and vitamin E to visual and chemical sexual signals of male Iberian green lizards: an experimental test. Behav Ecol Sociobiol. doi:10.1007/s00265-013-1672-9

    Google Scholar 

  • Lepetz V, Massot M, Chaine AS, Clobert J (2009) Climate warming and the evolution of morphotypes in a reptile. Glob Change Biol 15:454–466

    Article  Google Scholar 

  • López P, Martín J (2005a) Chemical compounds from femoral gland secretions of male Iberian rock lizards, Lacerta monticola cyreni. Z Naturforsch C 60:632–636

    PubMed  Google Scholar 

  • López P, Martín J (2005b) Age related differences in lipophilic compounds found in femoral gland secretions of male spiny-footed lizards, Acanthodactylus erythrurus. Z Naturforsch C 61:915–920

    Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • López P, Martín J (2006) Lipids in the femoral gland secretions of male Schreiber’s green lizards, Lacerta schreiberi. Z Naturforsch C 61:763–768

    PubMed  Google Scholar 

  • López P, Muñoz A, Martín J (2002) Symmetry, male dominance and female mate preferences in the Iberian rock lizard, Lacerta monticola. Behav Ecol Sociobiol 52:342–347

    Article  Google Scholar 

  • López P, Martín J, Cuadrado M (2003) Chemosensory cues allow male lizards Psammodromus algirus to override visual concealment of sexual identity by satellite males. Behav Ecol Sociobiol 54:218–224

    Article  Google Scholar 

  • López P, Amo L, Martín J (2006) Reliable signaling by chemical cues of male traits and health state in male lizards, Lacerta monticola. J Chem Ecol 32:473–488

    Article  PubMed  Google Scholar 

  • López P, Gabirot M, Martín J (2009a) Immune challenge affects sexual coloration of male Iberian wall lizards. J Exp Zool A 331:96–104

    Article  Google Scholar 

  • López P, Moreira PL, Martín J (2009b) Chemical polymorphism and chemosensory recognition between Iberolacerta monticola lizard color morphs. Chem Senses 34:723–731

    Article  PubMed  Google Scholar 

  • Louw S, Burger BV, Le Roux M, Van Wyk JH (2007) Lizard epidermal gland secretions I: chemical characterization of the femoral gland secretion of the sungazer, Cordylus giganteus. J Chem Ecol 33:1806–1818

    Article  CAS  PubMed  Google Scholar 

  • Martín J, López P (2006a) Vitamin D supplementation increases the attractiveness of males’ scent for female Iberian rock lizards. Proc R Soc Lond B Biol Sci 273:2619–2624

    Article  Google Scholar 

  • Martín J, López P (2006b) 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 (2006c) Age-related variation in lipophilic chemical compounds from femoral gland secretions of male lizards Psammodromus algirus. Biochem Syst Ecol 34:691–697

    Article  Google Scholar 

  • Martín J, López P (2011) Pheromones and reproduction in reptiles. In: Norris DO, Lopez KH (eds) Hormones and reproduction in vertebrates—reptiles. Academic Press, San Diego, pp 141–167

    Chapter  Google Scholar 

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

    Article  Google Scholar 

  • Martín J, Amo L, López P (2008) Parasites and health affect multiple sexual signals in male common wall lizards, Podarcis muralis. Naturwissenschaften 95:293–300

    Article  PubMed  Google Scholar 

  • Mason RT (1992) Reptilian pheromones. In: Gans C (ed) Biology of the Reptilia: hormones, brain, and behavior, vol 18. University of Chicago Press, Chicago, pp 114–228

    Google Scholar 

  • Mazer SJ, Damuth J (2001) Nature and causes of variation. In: Fox CW, Roff DA, Fairbrain DJ (eds) Evolutionary ecology: concepts and case studies. Oxford University Press, Oxford, pp 3–15

    Google Scholar 

  • McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297

    Article  Google Scholar 

  • McKinnon JS, Pierotti ME (2010) Colour polymorphism and correlated characters: genetic mechanisms and evolution. Mol Ecol 19(23):5101–5125

    Article  PubMed  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 Biol Sci 270:254–256

    Article  Google Scholar 

  • Pérez i de Lanuza G, Font E, Carazo P (2013) Color-assortative mating in a color-polymorphic lacertid lizard. Behav Ecol 24:273–279

    Article  Google Scholar 

  • Pérez C, Lores M, Velando A (2008) Availability of nonpigmentary antioxidant affects red coloration in gulls. Behav Ecol 19:967–973

    Article  Google Scholar 

  • Pike TV, Blount JD, Lindstrom J, Metcalfe NB (2007) Availability of non-carotenoid antioxidants affects the expression of a carotenoid-based sexual ornament. Biol Lett 3:353–356

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pryke SR, Griffith SC (2007) The relative role of male versus female mate choice in maintaining assortative pairing among discrete colour morphs. J Evol Biol 20:1512–1521

    Article  CAS  PubMed  Google Scholar 

  • Puebla O, Bermingham E, Guichard F, Whiteman E (2007) Colour pattern as a single trait driving speciation in Hypoplectrus coral reef fishes? Proc R Soc Lond B Biol Sci 274:1265–1271

    Article  Google Scholar 

  • Reynolds RG, Fitzpatrick BM (2007) Assortative mating in poison-dart frogs based on an ecologically important trait. Evolution 61:2253–2259

    Article  PubMed  Google Scholar 

  • Roulin A (2004) The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biol Rev 79:1–34

    Google Scholar 

  • Sacchi R, Scali S, Pupin F, Gentilli A, Galeotti P, Fasola M (2007a) Microgeographic variation of color morph frequency and biometry of common wall lizards. J Zool 273:389–396

    Article  Google Scholar 

  • Sacchi R, Rubolini D, Gentilli A, Pupin F, Razzetti E, Scali S, Galeotti P, Fasola M (2007b) Morph-specific immunity in males of the common wall lizard, Podarcis muralis. Amphibia Reptilia 28:408–412

    Article  Google Scholar 

  • Sacchi R, Scali S, Pellitteri-Rosa D, Pupin F, Gentilli A, Tettamanti S, Cavigioli L, Racina L, Maiocchi V, Galeotti P, Fasola M (2010) Photographic identification in reptiles: a matter of scales. Amphibia Reptilia 31:489–502

    Article  Google Scholar 

  • Sacchi R, Pellitteri-Rosa D, Bellati A, Di Paoli A, Ghitti M, Scali S, Galeotti P, Fasola M (2013) Colour variation in the polymorphic common wall lizard (Podarcis muralis): an analysis using the RGB colour system. Zool Anz 252:431–439

    Article  Google Scholar 

  • San Jose LM, Granado-Lorencio F, Sinervo B, Fitze PS (2013) Iridophores and not carotenoids account for chromatic variation of carotenoid-based coloration in common lizards (Lacerta vivipara). Am Nat 181:396–409

    Article  PubMed  Google Scholar 

  • Sheridan MA (1994) Regulation of lipid-metabolism in poikilothermic vertebrates. Comp Biochem Physiol B 107:495–508

    Google Scholar 

  • Sinervo B (2000) Adaptation, natural selection, and optimal life history allocation in the face of genetically-based trade-offs. In: Mousseau T, Sinervo B, Endler JA (eds) Adaptive genetic variation in the wild. Oxford University Press, Oxford, pp 41–64

    Google Scholar 

  • Sinervo B, Lively CM (1996) The rock-paper-scissors game and the evolution of alternative mating strategies. Nature 380:240–243

    Article  CAS  Google Scholar 

  • Sinervo B, Zamudio KR (2001) The evolution of alternative reproductive strategies: fitness differential, heritability, and genetic correlation between sexes. J Heredity 92:198–205

    Article  CAS  Google Scholar 

  • Sinervo B, Miles DB, DeNardo D, Frankin T, Klukowski M (2000) Testosterone, endurance, and Darwinian fitness: natural and sexual selection on the physiological bases of alternative male behaviors in side-blotched lizards. Horm Behav 38:222–223

    Article  CAS  PubMed  Google Scholar 

  • Sinervo B, Bleay C, Adampoulou C (2001) Social causes of correlational selection and the resolution of heritable colour polymorphism in a lizard. Evolution 55:2040–2052

    CAS  PubMed  Google Scholar 

  • Thompson CW, Moore MC (1991) Synthopic occurrence of multiple dewlap color morphs in male Tree Lizards, Urosaurus ornatus. Copeia 1991:493–503

    Article  Google Scholar 

  • Thompson CW, Moore IT, Moore MC (1993) Social, environmental and genetic factors in the ontogeny of phenotypic differentiation in a lizard with alternative male reproductive strategies. Behav Ecol Sociobiol 33:137–146

    Article  Google Scholar 

  • Vercken E, Massot M, Sinervo B, Clobert J (2007) Colour variation and alternative reproductive strategies in females of the common lizard Lacerta vivipara. J Evol Biol 20:221–232

    Article  CAS  PubMed  Google Scholar 

  • Weldon PJ, Dunn BS, McDaniel CA, Werner DI (1990) Lipids in the femoral gland secretions of the green iguana (Iguana iguana). Comp Biochem Physiol B 95:541–543

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank one anonymous reviewer for helpful comments, and Luis Cuadra and Elena Fernández for technical assistance with chemical analyses. Financial support was provided by the project MICIIN-CGL2011-24150/BOS. This research was supported by PhD grants (Doctorate in Experimental Ecology and Geobotany) from Pavia University to D. P.-R. and A. B.

Ethical standard

The study was carried out in conformity with the Italian current laws for lizard collection and detention (Aut. Prot. DPN no. 2009-0016034).

Author information

Authors and Affiliations

  1. DSTA, Dipartimento di Scienze della Terra e dell’Ambiente, Università di Pavia, Via Ferrata 9, 27100, Pavia, Italy

    D. Pellitteri-Rosa, A. Bellati, R. Sacchi, M. Fasola & P. Galeotti

  2. Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006, Madrid, Spain

    J. Martín & P. López

Authors
  1. D. Pellitteri-Rosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Martín
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. López
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Bellati
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. Sacchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Fasola
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. P. Galeotti
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. Pellitteri-Rosa.

Additional information

Handling Editor: Günther Raspotnig.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pellitteri-Rosa, D., Martín, J., López, P. et al. Chemical polymorphism in male femoral gland secretions matches polymorphic coloration in common wall lizards (Podarcis muralis). Chemoecology 24, 67–78 (2014). https://doi.org/10.1007/s00049-014-0148-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00049-014-0148-3

Keywords

Search

Navigation