Naturwissenschaften

, Volume 95, Issue 4, pp 293–300 | Cite as

Parasites and health affect multiple sexual signals in male common wall lizards, Podarcis muralis

Original Paper

Abstract

Multiple advertising sexual traits may either advertise different characteristics of male condition or be redundant to reinforce reliability of signals. Research has focused on multiple visual traits. However, in animals that use different multiple additional sensory systems, such as chemoreception, different types of traits might have evolved to signal similar characteristics of a male quality using different sensory channels. We examined whether ventral coloration and chemicals in femoral gland secretions of male common wall lizards, Podarcis muralis, are affected by their health state (blood-parasite load and cell-mediated immune response). Our results indicated that less parasitized lizards had brighter and more yellowish ventral colorations and also femoral secretions with higher proportions of two esters of octadecenoic acid. In addition, lizards with a greater immune response had more saturated coloration and secretions with higher proportions of octadecenoic acid methyl ester. We suggest that these signals would be reliable because only healthier males seemed able to allocate more carotenoids to coloration and presumably costly chemicals to secretions. The use of multiple sensory channels may provide more opportunities to signal a male quality under different circumstances, but also may reinforce the reliability of the signal when both types of traits may be perceived simultaneously.

Keywords

Sexual signals Parasites Immune response Coloration Femoral glands 

Notes

Acknowledgements

We thank three anonymous reviewers for helpful comments, “El Ventorrillo” MNCN Field Station for use of their facilities, and J. Moreno for allowing us to use the spectrophotometer. Financial support was provided by the MEC project CGL2005–00391/BOS, and by an “El Ventorrillo” CSIC and a MEC postdoctoral fellowship grants to L. Amo. The experiments comply with the current laws of the country (Spain) in which they were performed.

References

  1. Aitchison J (1986) The statistical analysis of compositional data. Chapman and Hall, LondonGoogle Scholar
  2. Alberts AC (1992) Constraints on the design of chemical communication systems in terrestrial vertebrates. Am Nat 139:62–89CrossRefGoogle Scholar
  3. Alberts AC (1993) Chemical and behavioral studies of femoral gland secretions in iguanid lizards. Brain Behav Evol 41:255–260PubMedCrossRefGoogle Scholar
  4. Amo L, López P, Martín J (2005) Prevalence and intensity of haemogregarine blood parasites and their mite vectors in the common wall lizard, Podarcis muralis. Parasitol Res 96:378–381PubMedCrossRefGoogle Scholar
  5. Anderholm S, Olsson M, Wapstra E, Ryberg K (2004) Fit and fat from enlarged badges: a field experiment on male sand lizards. Proc R Soc Lond B 271(Suppl):142–144CrossRefGoogle Scholar
  6. Andersson S, Pryke SR, Ornborg J, Lawes MJ, Andersson M (2002) Multiple receivers, multiple ornaments, and a tradeoff between agonistic and epigamic signaling in a widowbird. Am Nat 160:683–691CrossRefPubMedGoogle Scholar
  7. Baird TA, Fox SF, McCoy JK (1997) 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. Behav Ecol 8:506–517CrossRefGoogle Scholar
  8. Blount JD (2004) Carotenoids and life-history evolution in animals. Arch Biochem Biophys 430:10–15PubMedCrossRefGoogle Scholar
  9. Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127PubMedCrossRefGoogle Scholar
  10. Bradbury JW, Vehrencamp SL (1998) Principles of animal comunication. Sinauer, Sunderland, MAGoogle Scholar
  11. Cooper WE, Burns N (1987) Social significance of ventrolateral coloration in the fence lizard, Sceloporus undulatus. Anim Behav 35:526–532CrossRefGoogle Scholar
  12. Cooper WE, Greenberg N (1992) Reptilian coloration and behavior. In: Gans C, Crews D (eds) Biology of the reptilia, vol 18. University of Chicago Press, Chicago, pp 298–422Google Scholar
  13. Cooper WE, Pérez-Mellado V, Vitt LJ (2002) Lingual and biting responses to selected lipids by the lizard Podarcis lilfordi. Physiol Behav 75:237–241PubMedCrossRefGoogle Scholar
  14. 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 100:10341–10346PubMedCrossRefGoogle Scholar
  15. Doucet S, Montgomerie R (2003) Multiple sexual ornaments in satin bowerbirds: ultraviolet plumage and bowers signal different aspects of male quality. Behav Ecol 14:503–509CrossRefGoogle Scholar
  16. Edsman L (1990) Territoriality and competition in wall lizards. PhD Thesis. Univ Stockholm, SwedenGoogle Scholar
  17. Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:125–153CrossRefGoogle Scholar
  18. Faivre B, Grégoire A, Préault M, Cézilly F, Sorci G (2003) Immune activation rapidly mirrored in a carotenoid-based secondary sexual trait. Science 300:103PubMedCrossRefGoogle Scholar
  19. Figuerola J, Muñoz E, Gutierrez R, Ferrer D (1999) Blood parasites, leucocytes and plumage brightness in the cirl bunting, Emberiza cirlus. Funct Ecol 13:594–601CrossRefGoogle Scholar
  20. Funari SS, Barcelo F, Escriba PV (2003) Effects of oleic acid and its congeners, elaidic and stearic acids, on the structural properties of phosphatidylethanolamine membranes. J Lipid Res 44:567–575PubMedCrossRefGoogle Scholar
  21. Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546PubMedGoogle Scholar
  22. Gruschwitz M, Böhme W (1986) Podarcis muralis, Mauereidechse. In: Böhme W (ed) Handbuch der Reptilien und Amphibien Europas. Aula Verlag, Wiesbaden, Germany, pp 209–23Google Scholar
  23. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites. Science 218:384–387PubMedCrossRefGoogle Scholar
  24. Iwasa Y, Pomiankowski A (1994) The evolution of mate preferences for multiple sexual ornaments. Evolution 48:853–867CrossRefGoogle Scholar
  25. Johnstone RA (1995) Honest advertisement of multiple qualities using multiple signals. J Theor Biol 177:87–94CrossRefGoogle Scholar
  26. Kavaliers M, Colwell DD (1995) Discrimination by female mice between the odours of parasitized and non- parasitized males. Proc R Soc Lond B 261:31–35CrossRefGoogle Scholar
  27. Kwiatkowski MA, Sullivan BK (2002) Geographic variation in sexual selection among populations of an Iguanid lizard, Sauromalus obesus (=ater). Evolution 56:2039–3051PubMedGoogle Scholar
  28. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121Google Scholar
  29. López P, Martín J (2002) Chemical rival recognition decreases aggression levels in male Iberian wall lizards, Podarcis hispanica. Behav Ecol Sociobiol 51:461–465CrossRefGoogle Scholar
  30. López P, Martín J (2005) Female Iberian wall lizards prefer male scents that signal a better cell-mediated immune response. Biol Lett 1:404–406PubMedCrossRefGoogle Scholar
  31. López P, Martín J, Cuadrado M (2002) Pheromone mediated intrasexual aggression in male lizards, Podarcis hispanicus. Aggr Behav 28:154–163CrossRefGoogle Scholar
  32. 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 54:218–224CrossRefGoogle Scholar
  33. 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 32:473–488PubMedCrossRefGoogle Scholar
  34. Loyau A, Saint Jalme M, Cagniant C, Sorci G (2005) Multiple sexual advertisements honestly reflect health status in peacocks (Pavo cristatus). Behav Ecol Sociobiol 58:552–557CrossRefGoogle Scholar
  35. Macedonia JM, James S, Wittle LW, Clark DL (2000) Skin pigments and coloration in the Jamaican radiation of Anolis lizards. J Herpetol 34:99–109CrossRefGoogle Scholar
  36. Martín J, López P (2006a) 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 16:31–38CrossRefGoogle Scholar
  37. Martín J, López P (2006b) Links between male quality, male chemical signals, and female mate choice in Iberian rock lizards. Funct Ecol 20:1087–1096CrossRefGoogle Scholar
  38. Martín J, López P (2006c) Vitamin D supplementation increases the attractiveness of males’ scent for female Iberian rock lizards. Proc R Soc Lond B 273:2619–2624CrossRefGoogle Scholar
  39. Martin LB, Han P, Lewittes J, Kuhlman JR, Klasing KC, Wikelski M (2006) Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct Ecol 20:290–299CrossRefGoogle Scholar
  40. Mason RT (1992) Reptilian pheromones. In: Gans C, Crews D (eds) Biology of the reptilia, vol 18. University of Chicago Press, Chicago, pp 114–228Google Scholar
  41. McGraw KJ (2005) The antioxidant function of many animal pigments: are there consistent health benefits of sexually selected colourants. Anim Behav 69:757–764CrossRefGoogle Scholar
  42. McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712PubMedCrossRefGoogle Scholar
  43. Møller AP, Biard C, Blount JD, Houston DC, Ninni P, Saino N, Surai PF (2000) Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence, or detoxification ability. Avian Poult Rev 11:137–159Google Scholar
  44. Montgomerie R (2006) Analyzing colors. In: Hill GE, McGraw KJ (ed). Bird coloration, Vol 1. Mechanisms and measurements. Harvard University Press, Cambridge, Massachusetts, pp 90–147Google Scholar
  45. Olsson M (1994) Nuptial coloration in the sand lizard, Lacerta agilis: an intra-sexually selected cue to fighting ability. Anim Behav 48:607–613CrossRefGoogle Scholar
  46. 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) 270:254–256CrossRefGoogle Scholar
  47. Oppliger A, Celerier ML, Clobert J (1996) Physiological and behaviour changes in common lizards parasitized by haemogregarines. Parasitol 113:433–438CrossRefGoogle Scholar
  48. Oppliger A, Giorgi MS, Conelli A, Nembrini M, John-Alder HB (2004) Effect of testosterone on immunocompetence, parasite load, and metabolism in the common wall lizard (Podarcis muralis). Can J Zool 82:1713–1719CrossRefGoogle Scholar
  49. Ortiz E, Throckmorton LH, Williams-Ashman HG (1962) Drosopterins in the throat-fans of some Puerto Rican lizards. Nature 196:595–596CrossRefGoogle Scholar
  50. Penn D, Potts WK (1998) Chemical signals and parasite mediated sexual selection. Trends Ecol Evol 13:391–396CrossRefGoogle Scholar
  51. Penn DJ, Schneider G, White K, Slev P, Potts W (1998) Influenza infection neutralizes the attractiveness of male odor to female mice (Mus musculus). Ethology 104:685–694CrossRefGoogle Scholar
  52. Pomiankowski AN (1988) The evolution of female mate preferences for male genetic quality. Oxford Surv Evol Biol 5:136–184Google Scholar
  53. Rantala MJ, Jokinen I, Kortet R, Vainikka A, Suhonen J (2002) Do pheromones reveal male immunocompetence. Proc R Soc Lond B 269:1681–1685CrossRefGoogle Scholar
  54. Rantala MJ, Kortet R, Kotiaho JS, Vainikka A, Suhonen J (2003) Condition dependence of pheromones and immune function in the grain beetle Tenebrio molitor. Funct Ecol 17:534–540CrossRefGoogle Scholar
  55. Ressel S, Schall JJ (1989) Parasites and showy males: malarial infection and color variation in fence lizards. Oecologia 78:158–164CrossRefGoogle Scholar
  56. Rowe C (1999) Receiver psychology and the evolution of multicomponent signals. Anim Behav 58:921–931PubMedCrossRefGoogle Scholar
  57. Sacchi R, Rubolini D, Gentilli A, Pupin F, Razzetti E, Scali S, Galeotti P, Fasola M (2007) Morph-specific immunity in male Podarcis muralis. Amphib-Rept 28:408–412CrossRefGoogle Scholar
  58. Saks L, Ots I, Hõrak P (2003a) Carotenoid-based plumage coloration of male greenfinches reflects health and immunocompetence. Oecologia 134:301–307PubMedGoogle Scholar
  59. Saks L, McGraw K, Hõrak P (2003b) How feather colour reflects its carotenoid content. Funct Ecol 17:55–561CrossRefGoogle Scholar
  60. Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13:567–572CrossRefGoogle Scholar
  61. Sullivan MS (1994) Mate choice as an information gathering process under time constraint: implications for behaviour and signal design. Anim Behav 47:141–151CrossRefGoogle Scholar
  62. Svensson E, Sinervo B, Comendant T (2001) Density-dependent competition and selection on immune function in genetic lizard morphs. Proc Natl Acad Sci USA 98:12561–12565PubMedCrossRefGoogle Scholar
  63. Thompson CW, Moore MC (1991) Throat colour reliably signals status in male tree lizards Urosaurus ornatus. Anim Behav 42:298–442Google Scholar
  64. Veiga JP, Salvador A, Merino S, Puerta M (1998) Reproductive effort affects immune response and parasite infection in a lizard: a phenotypic manipulation using testosterone. Oikos 82:313–318CrossRefGoogle Scholar
  65. Wedekind C (1992) Detailed information about parasites revealed by sexual ornamentation. Proc R Soc Lond B 247:169–174CrossRefGoogle Scholar
  66. Wedekind C, Folstad I (1994) Adaptive or nonadaptive immunosuppression by sex hormones. Am Nat 143:936–938CrossRefGoogle Scholar
  67. Weiss SL (2006) Female-specific color is a signal of quality in the striped plateau lizard (Sceloporus virgatus). Behav Ecol 17:726–732CrossRefGoogle Scholar
  68. Westneat DF, Birkhead TR (1998) Alternative hypothesis linking the immune system and mate choice for good genes. Proc R Soc Lond B 265:1065–1073CrossRefGoogle Scholar
  69. Wintrobe MM (1991) Clinical haematology. Lea and Feiberger, Philadelphia, PAGoogle Scholar
  70. Wyatt TD (2003) Pheromones and animal behaviour. Cambridge University Press, CambridgeGoogle Scholar
  71. Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214PubMedCrossRefGoogle Scholar
  72. Zala SM, Potts WK, Penn DJ (2004) Scent-marking displays provide honest signals of health and infection. Behav Ecol 15:338–344CrossRefGoogle Scholar
  73. Zucker N (1994) A dual status-signalling system: a matter of redundancy or differing roles. Anim Behav 47:15–22CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Departamento de Ecología EvolutivaMuseo Nacional de Ciencias Naturales, C.S.I.C.MadridSpain
  2. 2.Department of Animal Population BiologyCentre for Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW)HeterenThe Netherlands

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