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Naturwissenschaften

, Volume 100, Issue 6, pp 551–558 | Cite as

Negative correlation between nuptial throat colour and blood parasite load in male European green lizards supports the Hamilton–Zuk hypothesis

  • Orsolya MolnárEmail author
  • Katalin Bajer
  • Boglárka Mészáros
  • János Török
  • Gábor Herczeg
Original Paper

Abstract

During female mate choice, conspicuous male sexual signals are used to infer male quality and choose the best sire for the offspring. The theory of parasite-mediated sexual selection (Hamilton–Zuk hypothesis) presumes that parasite infection can influence the elaboration of sexual signals: resistant individuals can invest more energy into signal expression and thus advertise their individual quality through signal intensity. By preferring these males, females can provide resistance genes for their offspring. Previous research showed that nuptial throat colour of male European green lizard, Lacerta viridis, plays a role in both inter- and intrasexual selections as a condition-dependent multiple signalling system. The aim of this study was to test the predictions of the Hamilton–Zuk hypothesis on male European green lizards. By blood sampling 30 adult males during the reproductive season, we found members of the Haemogregarinidae family in all but one individual (prevalence = 96 %). The infection intensity showed strong negative correlation with the throat and belly colour brightness in line with the predictions of the Hamilton–Zuk hypothesis. In addition, we found other correlations between infection intensity and other fitness-related traits, suggesting that parasite load has a remarkable effect on individual fitness. This study shows that throat patch colour of the European green lizards not only is a multiple signalling system but also possibly acts as an honest sexual signal of health state in accordance with the Hamilton–Zuk hypothesis.

Keywords

Hamilton–Zuk hypothesis Nuptial coloration Blood parasite Haemogregarinidae Lizard 

Notes

Acknowledgments

We would like to thank Prof. Joseph J. Schall for his indispensable help in identifying the blood parasites. We also thank Michael L. Logan for his useful comments and correcting the English. The study was supported by OTKA (Hungarian Scientific Research Fund, ref. no. F68403 and K105517). We thank Middle–Danube–Valley Environmental, Nature and Water Inspectorate for the permission to conduct this study (project no. 31203-3/2010).

Ethical standards

Experiments were performed according to the guidelines of the Hungarian Act of Animal Care and Experimentation (1998, XXVIII, section 243/ 1998), which conforms to the regulation of animal experiments by the European Union.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Al-Ghamdy AO (2011) A light microscopic study on the haemogregarine species infecting the lizard Acanthodactylus schmidti from Saudi Arabia. J Egypt Soc Parasitol 41(1):7–15PubMedGoogle Scholar
  2. Amo L, Lopez P, Martin J (2005) Prevalence and intensity of haemogregarine blood parasites and their mite vectors in the common wall lizard, Podarcis muralis. Parasitol Res 96(6):378–381PubMedCrossRefGoogle Scholar
  3. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  4. Bajer K, Molnar O, Torok J, Herczeg G (2010) Female European green lizards (Lacerta viridis) prefer males with high ultraviolet throat reflectance. Behav Ecol Sociobiol 64(12):2007–2014CrossRefGoogle Scholar
  5. Bajer K, Molnar O, Torok J, Herczeg G (2011) Ultraviolet nuptial colour determines fight success in male European green lizards (Lacerta viridis). Biol Lett 7(6):866–868. doi: 10.1098/rsbl.2011.0520 PubMedCrossRefGoogle Scholar
  6. Bajer K, Molnar O, Torok J, Herczeg G (2012) Temperature, but not available energy, affects the expression of a sexually selected ultraviolet (UV) colour trait in male European green lizards. PLoS ONE 7 (3):e34359. DOI  10.1371/journal.pone.0034359
  7. Barnard SM, Upton SJ (1994) A veterinary guide to the parasites of reptiles, vol. 1. Protozoa. Krieger, MalabarGoogle Scholar
  8. Borgia G (1986) Satin bowerbird parasites—a test of the bright male hypothesis. Behav Ecol Sociobiol 19:355–358CrossRefGoogle Scholar
  9. Borgia G, Collis K (1990) Parasites and bright male plumage in the satin bowerbird (Ptilonorhynchus violaceus). Am Zool 30:279–285Google Scholar
  10. Boulinier T, Sorci G, Monnat JY, Danchin E (1997) Parent–offspring regression suggests heritable susceptibility to ectoparasites in a natural population of kittiwake Rissa tridactyla. J Evol Biol 10(1):77–85CrossRefGoogle Scholar
  11. Bouma MJ, Smallridge CJ, Bull CM, Komdeur J (2007) Susceptibility to infection by a haemogregarine parasite and the impact of infection in the Australian sleepy lizard Tiliqua rugosa. Parasitol Res 100(5):949–954PubMedCrossRefGoogle Scholar
  12. Brawner WR, Hill GE, Sundermann CA (2000) Effects of coccidial and mycoplasmal infections on carotenoid-based plumage pigmentation in male house finches. Auk 117:952–963CrossRefGoogle Scholar
  13. Brown GP, Shilton CM, Shine R (2006) Do parasites matter? Assessing the fitness consequences of haemogregarine infection in snakes. Can J Zool 84(5):668–676CrossRefGoogle Scholar
  14. Budden AE, Dickinson JL (2009) Signals of quality and age: the information content of multiple plumage ornaments in male western bluebirds Sialia mexicana. J Avian Biol 40(1):18–27. doi: 10.1111/j.1600-048X.2008.04344.x CrossRefGoogle Scholar
  15. Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78(4):575–595PubMedCrossRefGoogle Scholar
  16. Charge R, Saint Jalme M, Lacroix F, Cadet A, Sorci G (2010) Male health status, signalled by courtship display, reveals ejaculate quality and hatching success in a lekking species. J Anim Ecol 79(4):843–850PubMedGoogle Scholar
  17. Clayton DH (1990) Mate choice in experimentally parasitized rock doves—lousy males lose. Am Zool 30(2):251–262Google Scholar
  18. Clayton DH (1991) The influence of parasites on host sexual selection. Par Tod 7:329–334CrossRefGoogle Scholar
  19. Davies AJ, Reed CC, Smit NJ (2003) An unusual intraerythrocytic parasite of Parablennius cornutus from South Africa. J Parasitol 89(5):913–917PubMedCrossRefGoogle Scholar
  20. del Cerro S, Merino S, Martinez-de la Puente J, Lobato E, Ruiz-de Castañeda R, Rivero-de Aaguilar J, Martinez J, Morales J, Tomas G, Moreno J (2010) Carotenoid-based plumage colouration is associated with blood parasite richness and stress protein levels in blue tits (Cyanistes caeruleus). Oecologia 162:825–835PubMedCrossRefGoogle Scholar
  21. Dunlap KD (1993) Effects of nymphal ticks and their interaction with malaria on the physiology of male fence lizards. Copeia 4:1045–1048CrossRefGoogle Scholar
  22. Garcia-Ramirez A, Delgado-Garcia JD, Foronda-Rodriguez P, Abreu-Acosta N (2005) Haematozoans, mites and body condition in the oceanic island lizard Gallotia atlantica (Peters and Doria, 1882) (Reptilia: Lacertidae). J Nat Hist 39(17):1299–1305CrossRefGoogle Scholar
  23. Grether GF, Kolluru GR, Nersissian K (2004) Individual colour patches as multicomponent signals. Biol Rev 79:583–610. doi: 10.1017/S1464793103006390 PubMedCrossRefGoogle Scholar
  24. Hagelin JC (2002) The kinds of traits involved in male–male competition: a comparison of plumage, behavior, and body size in quail. Behav Ecol 13:384–387CrossRefGoogle Scholar
  25. Hamilton PS, Sullivan BK (2005) Female mate attraction in ornate tree lizards, Urosaurus ornatus: a multivariate analysis. Anim Behav 69:219–224. doi: 10.1016/j.anbehav.2004.03.011 CrossRefGoogle Scholar
  26. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds—a role for parasites. Science 218(4570):384–387PubMedCrossRefGoogle Scholar
  27. Healey M, Uller T, Olsson M (2007) Seeing red: morph-specific contest success and survival rates in a colour-polymorphic agamid lizard. Anim Behav 74:337–341CrossRefGoogle Scholar
  28. Hussein ANA (2006) Light and transmission electron microscopic studies of a haemogregarine in naturally infected fan-footed gecko (Ptyodactylus hasselquistii). Parasitol Res 98(5):468–471. doi: 10.1007/s00436-005-0084-9 PubMedCrossRefGoogle Scholar
  29. Huyghe K, Herrel A, Adriaens D, Tadic Z, Van Damme R (2009) It is all in the head: morphological basis for differences in bite force among colour morphs of the Dalmatian wall lizard. Biol J Linn Soc 96(1):13–22. doi: 10.1111/j.1095-8312.2008.01103.x CrossRefGoogle Scholar
  30. Lainson R, De Souza MC, Franco CM (2007) Natural and experimental infection of the lizard Ameiva ameiva with Hemolivia stellata (Adeleina : Haemogregarinidae) of the toad Bufo marinus. Parasite-Journal De La Societe Francaise De Parasitologie 14(4):323–328CrossRefGoogle Scholar
  31. Lebas NR, Marshall NJ (2001) No evidence of female choice for a condition-dependent trait in the agamid lizard, Ctenophorus ornatus. Behaviour 138:965–980CrossRefGoogle Scholar
  32. Lefcort H, Blaustein AR (1991) Parasite load and brightness in lizards—an interspecific test of the Hamilton and Zuk hypothesis. J Zool 224:491–499CrossRefGoogle Scholar
  33. Leu ST, Kappeler PM, Bull CM (2010) Refuge sharing network predicts ectoparasite load in a lizard. Behav Ecol Sociobiol 64(9):1495–1503PubMedCrossRefGoogle Scholar
  34. Martin J, Amo L, Lopez P (2008) Parasites and health affect multiple sexual signals in male common wall lizards, Podarcis muralis. Naturwissenschaften 95(4):293–300. doi: 10.1007/s00114-007-0328-x PubMedCrossRefGoogle Scholar
  35. Martin J, Civantos E, Amo L, Lopez P (2007) Chemical ornaments of male lizards Psammodromus algirus may reveal their parasite load and health state to females. Behav Ecol Sociobiol 62(2):173–179. doi: 10.1007/s00265-007-0451-x CrossRefGoogle Scholar
  36. Martin J, Lopez P (2009) Multiple color signals may reveal multiple messages in male Schreiber's green lizards, Lacerta schreiberi. Behav Ecol Sociobiol 63(12):1743–1755CrossRefGoogle Scholar
  37. McGraw KJ, Hill GE (2000) Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration. Proc R Soc B Biol Sci 267(1452):1525–1531CrossRefGoogle Scholar
  38. McGraw KJ, Mackillop EA, Dale J, Hauber ME (2002) Different colors reveal different information: how nutritional stress affects the expression of melanin- and structurally based ornamental plumage. J Exp Biol 205(23):3747–3755PubMedGoogle Scholar
  39. Moller AP (1990) Parasites and sexual selection—current status of the Hamilton and Zuk hypothesis. J Evol Biol 3(5–6):319–328CrossRefGoogle Scholar
  40. Moller AP (1994) Directional selection on directional asymmetry: testes size and secondary sexual characters in birds. Proc R Soc B Biol Sci 258(1352):147–151. doi: 10.1098/rspb.1994.0155 CrossRefGoogle Scholar
  41. Moller AP, Jennions MD (2002) How much variance can be explained by ecologists and evolutionary biologists? Oecologia 132(4):492–500. doi: 10.1007/s00442-002-0952-2 CrossRefGoogle Scholar
  42. Molnar O, Bajer K, Torok J, Herczeg G (2012) Individual quality and nuptial throat colour in male European green lizards. J Zool 287(4):233–239. doi: 10.1111/j.1469-7998.2012.00916.x CrossRefGoogle Scholar
  43. Murtaugh PA (2009) Performance of several variable-selection methods applied to real ecological data. Ecol Lett 12(10):1061–1068PubMedCrossRefGoogle Scholar
  44. Olsson M, Wapstra E, Madsen T, Ujvari B, Rugfelt C (2005) Costly parasite resistance: a genotype-dependent handicap in sand lizards? Biol Lett 1(3):375–377. doi: 10.1098/rsbl.2005.0339 PubMedCrossRefGoogle Scholar
  45. Oppliger A, Celerier ML, Clobert J (1996) Physiological and behaviour changes in common lizards parasitized by haemogregarines. Parasitology 113:433–438CrossRefGoogle Scholar
  46. Palacios MG, Winkler DW, Klasing KC, Hasselquist D, Vleck CM (2011) Consequences of immune system aging in nature: a study of immunosenescence costs in free-living tree swallows. Ecology 92(4):952–966PubMedCrossRefGoogle Scholar
  47. Palmer AR, Strobeck C (1986) Fluctuating asymmetry—measurement, analysis, patterns. Annu Rev Ecol Syst 17:391–421CrossRefGoogle Scholar
  48. Paperna I, Lainson R (2004) Hepatozoon cf. terzii (Sambon & Seligman, 1907) infection in the snake boa constrictor constrictor from north Brazil: transmission to the mosquito Culex quinquefasciatus and the lizard Tropidurus torquatus. Parasite-Journal De La Societe Francaise De Parasitologie 11(2):175–181Google Scholar
  49. Peters A, Delhey K, Johnsen A, Kempenaers B (2007) The condition-dependent development of carotenoid-based and structural plumage in nestling blue tits: males and females differ. Am Nat 169:122–136CrossRefGoogle Scholar
  50. Petit G, Landau I, Baccam D, Lainson R (1990) Description et cycle biologique d’Hemolivia stellata n. g., n. sp., hémogrégarine de crapauds brésiliens. Ann Parasitol Hum Comp 65:3–15Google Scholar
  51. Ressel S, Schall JJ (1989) Parasites and showy males—malarial infection and color variation in fence lizards. Oecologia 78(2):158–164. doi: 10.1007/Bf00377151 CrossRefGoogle Scholar
  52. Roca V, Galdon MA (2010) Haemogregarine blood parasites in the lizards Podarcis bocagei (Seoane) and P. carbonelli (Perez-Mellado) (Sauria: Lacertidae) from NW Portugal. Syst Parasitol 75:75–79PubMedCrossRefGoogle Scholar
  53. Saks L, Ots I, Horak P (2003) Carotenoid-based plumage coloration of male greenfinches reflects health and immunocompetence. Oecologia 134(3):301–307. doi: 10.1007/s00442-002-1125-z PubMedGoogle Scholar
  54. Schall JJ, Dearing MD (1987) Malarial parasitism and male competition for mates in the western fence lizard, Sceloporus occidentalis. Oecologia 73(3):389–392. doi: 10.1007/Bf00385255 CrossRefGoogle Scholar
  55. Schall JJ, Staats CM (1997) Parasites and the evolution of extravagant male characters: Anolis lizards on Caribbean islands as a test of the Hamilton–Zuk hypothesis. Oecologia 111(4):543–548CrossRefGoogle Scholar
  56. Sinervo B, Lively CM (1996) The rock-paper-scissors game and the evolution of alternative male strategies. Nature 380(6571):240–243. doi: 10.1038/380240a0 CrossRefGoogle Scholar
  57. Smallridge CJ, Bull CM (1999) Transmission of the blood parasite Hemolivia mariae between its lizard and tick hosts. Parasitol Res 85(10):858–863PubMedCrossRefGoogle Scholar
  58. Stapley J, Whiting MJ (2006) Ultraviolet signals fighting ability in a lizard. Biol Lett 2(2):169–172. doi: 10.1098/rsbl.2005.0419 PubMedCrossRefGoogle Scholar
  59. Telford SR (2009) Haemoparasites of the Reptilia. CRC, Boca RatonGoogle Scholar
  60. Tripet F, Richner H (1999) Density-dependent processes in the population dynamics of a bird ectoparasite Ceratophyllus gallinae. Ecology 80(4):1267–1277. doi: 10.1890/0012-9658(1999)080[1267:Ddpitp]2.0.Co;2 Google Scholar
  61. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man, 1871–197. Aldine, Chicago, pp 136–179Google Scholar
  62. van Valen L (1962) A study of fluctuating asymmetry. Evolution 16:125–142CrossRefGoogle Scholar
  63. Weiss SL (2006) Female-specific color is a signal of quality in the striped plateau lizard (Sceloporus virgatus). Behav Ecol 17(5):726–732CrossRefGoogle Scholar
  64. Whiting MJ, Stuart-Fox DM, O'Connor D, Firth D, Bennett NC, Blomberg SP (2006) Ultraviolet signals ultra-aggression in a lizard. Anim Behav 72:353–363CrossRefGoogle Scholar
  65. Wikel SK, Ramachandra RN, Bergman DK, Burkot TR, Piesman J (1997) Infestation with pathogen-free nymphs of the tick Ixodes scapularis induces host resistance to transmission of Borrelia burgdorferi by ticks. Infect Immun 65:335–338PubMedGoogle Scholar
  66. Zahavi A (1975) Mate selection—selection for a handicap. J Theor Biol 53:205–214PubMedCrossRefGoogle Scholar
  67. Zahavi A (1977) Cost of honesty—(further remarks on handicap principle). J Theor Biol 67(3):603–605PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Orsolya Molnár
    • 1
    • 3
    Email author
  • Katalin Bajer
    • 2
    • 3
  • Boglárka Mészáros
    • 3
  • János Török
    • 3
  • Gábor Herczeg
    • 3
  1. 1.Department of Biological Sciences, Life Sciences CenterDartmouth CollegeHanoverUSA
  2. 2.Universidade Federal do Rio Grande do NorteNatalBrazil
  3. 3.Behavioural Ecology Group, Department of Systematic Zoology and EcologyEötvös Loránd UniversityBudapestHungary

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