Skip to main content
Log in

Female sensory bias may allow honest chemical signaling by male Iberian rock lizards

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Some mate choice theories propose that only male signals that are honest and condition-dependent can be stable, while another hypothesis states that males evolve signals that exploit the sensory system of females. However, sensory traps might evolve into honest signals if they are differentially costly for males. We tested whether a pre-existing sensory bias for food chemicals explained chemosensory preferences of female Iberian rock lizards for male scents. We manipulated hunger levels of females and found that food-deprived females had increased chemosensory responses to chemical stimuli from both invertebrate prey and femoral secretions of males, but not to control water. Further tests suggested that cholesta-5,7-dien-3-ol (provitamin D3), a lipid found in both prey and males’ scent, may be one of the chemicals eliciting these responses. Moreover, hungry females spent more time on scent marks of males that had experimentally increased cholesta-5,7-dien-3-ol than on scent marks of males alone, whereas for control females this effect was not significant. We suggest that preexisting sensory bias for essential nutrients (i.e., provitamin D) may be the origin of similar female responses to male chemicals. However, previous studies have suggested that the allocation of these chemicals to ornaments is costly and only high quality males can afford it. Therefore, preexisting sensory bias for essential nutrients may further allow the evolution and maintenance of honest sexual displays.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • 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 

  • Allen ME, Bush M, Oftedal OT, Roscoe R, Walsh T, Holick MF (1994) Update on vitamin D and ultraviolet light in basking lizards. Proc Am Assoc Zoo Vet 25:314–316

    Google Scholar 

  • Basolo AL (1990) Female preference predates the evolution of the sword in swordtail fish. Science 250:808–810

    Article  PubMed  Google Scholar 

  • Basolo AL (1995) Phylogenetic evidence for the role of a preexisting bias in sexual selection. Proc R Soc Lond B 259:307–311

    Article  CAS  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 

  • Christy JH (1995) Mimicry, mate choice, and the sensory trap hypothesis. Am Nat 146:171–181

    Article  Google Scholar 

  • Clark RW (2004) Timber rattlesnakes (Crotalus horridus) use chemical cues to select ambush sites. J Chem Ecol 30:607–617

    Article  PubMed  CAS  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 (2003) Prey chemicals do not affect perch choice by an ambushing lizard, Sceloporus malachiticus. J Herpetol 37:425–427

    Article  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, Whiting MJ (2003) Prey chemicals do not affect giving-up time at ambush posts by the cordylid lizard Platysaurus broadley. Herpetologica 59:455–458

    Article  Google Scholar 

  • Dawkins MS, Guilford T (1996) Sensory bias and the adaptiveness of female choice. Am Nat 148:937–942

    Article  Google Scholar 

  • Ferguson GW, Gehrmann WH, Karsten KB, Landwer AJ, Carman EN, Chen TC, Holick MF (2005) Ultraviolet exposure and vitamin D synthesis in a sun-dwelling and a shade-dwelling species of Anolis: are there adaptations for lower ultraviolet B and dietary vitamin D3 availability in the shade? Physiol Biochem Zool 78:193–200

    Article  PubMed  CAS  Google Scholar 

  • Fisher HS, Rosenthal GG (2006) Hungry females show stronger mating preferences. Behav Ecol 17:979–981

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fuller RC, Houle D, Travis J (2005) Sensory bias as an explanation for the evolution of mate preferences. Am Nat 166:437–446

    Article  PubMed  Google Scholar 

  • Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546

    Article  PubMed  CAS  Google Scholar 

  • Grether GF, Hudon J, Millie DF (1999) Carotenoid limitation of sexual coloration along an environmental gradient in guppies. Proc R Soc Lond B 266:1317–1322

    Article  CAS  Google Scholar 

  • Grether GF, Kolluru GR, Rodd FH, de la Cerda J, Shimazaki K (2005) Carotenoid availability affects the development of a colour-based mate preference and the sensory bias to which it is genetically linked. Proc R Soc Lond B 272:2181–2188

    Article  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 

  • Holick MF, Tian XQ, Allen M (1995) Evolutionary importance for the membrane enhancement of the production of vitamin D3 in the skin of poikilothermic animals. Proc Natl Acad Sci U S A 92:3124–3126

    Article  PubMed  CAS  Google Scholar 

  • Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev 82:265–289

    Article  PubMed  Google Scholar 

  • Kokko H, Brooks R, Jennions MD, Morley J (2003) The evolution of mate choice and mating biases. Proc R Soc Lond B 270:653–664

    Article  Google Scholar 

  • Krasnoff SB, Dussourd DE (1989) Dihydropyrrolizine attractants for arctiid moths that visit plants containing pyrrolizidine alkaloids. J Chem Ecol 15:47–60

    Article  CAS  Google Scholar 

  • Labra A (2007) The peculiar case of an insectivorous iguanid lizard that detects chemical cues from prey. Chemoecol 17:103–108

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Löfstedt C, Vickers NJ, Roelofs WL, Baker TC (1989) Diet related courtship success in the oriental fruit moth, Grapholita molesta (Tortricidae). Oikos 55:402–408

    Article  Google Scholar 

  • López P, Martín J (2005a) 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 (2005b) 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, 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, Aragón P, Martín J (2003) Responses of female lizards, Lacerta monticola, to males’ chemical cues reflect their mating preference for older males. Behav Ecol Sociobiol 55:73–79

    Article  Google Scholar 

  • Macías-García C, Ramirez E (2005) Evidence that sensory traps can evolve into honest signals. Nature 434:501–505

    Article  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) Vitamin D supplementation increases the attractiveness of males’ scent for female Iberian rock lizards. Proc R Soc Lond B 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, Salvador A (1993) Tail loss and foraging tactics of Iberian rock-lizards, Lacerta monticola. Oikos 66:318–324

    Article  Google Scholar 

  • Martín J, Salvador A (1997) Effects of tail loss on the time budgets, movements, and spacing patterns of Iberian rock lizards, Lacerta monticola. Herpetologica 53:117–125

    Google Scholar 

  • Martín J, Civantos E, Amo L, López P (2007) Chemical ornaments of male lizards Psammodromus algirus may reveal their parasite load and health state to females. Behav Ecol Sociobiol 62:173–179

    Article  Google Scholar 

  • Mason RT (1992) Reptilian pheromones. In: Gans C, Crews D (eds) Biology of the reptilia, vol 18. University of Chicago, Chicago, pp 114–228

    Google Scholar 

  • Nishida R, Baker TC, Roelofs WL (1982) Hair pencil pheromone components of male oriental fruit moths, Grapholita molesta. J Chem Ecol 8:947–959

    Article  CAS  Google Scholar 

  • Nishida R, Fukami H, Baker TC, Roelofs WL (1985) Oriental fruit moth pheromone: attraction of females by an herbal essence. In: Acree TE, Soderlud DM (eds) Semiochemistry, flavors and Pheromones. De Gruyter, Berlin, pp 47–60

    Google Scholar 

  • Olsson M, Madsen T (1998) Sexual selection and sperm competition in reptiles. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, San Diego, California, pp 503–578

    Chapter  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:S254–S256

    Article  CAS  Google Scholar 

  • Penn DJ, Potts WK (1998) Chemical signals and parasite mediated sexual selection. Trends Ecol Evol 13:391–396

    Article  Google Scholar 

  • Pérez-Mellado V (1998) Lacerta monticola Boulenger, 1905. In: Salvador A (ed) Reptiles. Fauna Ibérica, vol. 10. Museo Nacional de Ciencias Naturales, Madrid, pp 207–215

  • Pomiankowski AN (1988) The evolution of female mate preferences for male genetic quality. Oxford Surv Evol Biol 5:136–184

    Google Scholar 

  • Rantala MJ, Jokinen I, Kortet R, Vainikka A, Suhonen J (2002) Do pheromones reveal male immunocompetence? Proc R Soc Lond B 269:1681–1685

    Article  Google Scholar 

  • 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 17:534–540

    Article  Google Scholar 

  • Rodd FH, Hughes KA, Grether GF, Baril CT (2002) A possible non-sexual origin of mate preference: are male guppies mimicking fruit? Proc R Soc Lond B 269:475–481

    Article  Google Scholar 

  • Ryan MJ (1998) Sexual selection, receiver biases, and the evolution of sex differences. Science 281:1999–2003

    Article  PubMed  CAS  Google Scholar 

  • Sakaluk SK (2000) Sensory exploitation as an evolutionary origin to nuptial food gifts in insects. Proc R Soc Lond B 267:339–343

    Article  CAS  Google Scholar 

  • Searcy WA, Nowicki S (2005) The evolution of animal communication. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Smith C, Barber I, Wootton RJ, Chittka L (2004) A receiver bias in the origin of three-spined stickleback mate choice. Proc R Soc Lond B 271:949–955

    Article  Google Scholar 

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

    Google Scholar 

  • Wyatt TD (2003) Pheromones and animal behaviour. Cambridge University Press, Cambridge

    Google Scholar 

  • Zahavi A (1975) Mate selection—A selection for a handicap. J Theor Biol 53:205–214

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank W.E. Cooper, M.J. Rantala, and an anonymous reviewer for helpful comments, and the “El Ventorrillo” MNCN Field Station for use of their facilities. Financial support was provided by the MEC project CGL2005-00391/BOS. Experiments were performed under license from the “Comunidad de Madrid” Environmental Agency.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José Martín.

Additional information

Communicated by W. Cooper

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martín, J., López, P. Female sensory bias may allow honest chemical signaling by male Iberian rock lizards. Behav Ecol Sociobiol 62, 1927–1934 (2008). https://doi.org/10.1007/s00265-008-0624-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-008-0624-2

Keywords

Navigation