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

Naturwissenschaften

Volumn 95, Issue 4, 2008, Pages 293-300

  Martín, José ^a   Amo, Luisa ^a,b   López, Pilar ^a  

^a MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^b NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

Author keywords

Coloration; Femoral glands; Immune response; Parasites; Sexual signals

Indexed keywords

CAROTENOID;

CAROTENOID; COLOR MORPH; ENDOCRINE SYSTEM; IMMUNE RESPONSE; LIZARD; PARASITE INFESTATION; REPRODUCTIVE COST; RESOURCE ALLOCATION; SECRETION; SEXUAL BEHAVIOR; SIGNALING;

ARTICLE; COLOR VISION; HEALTH STATUS; IMMUNE RESPONSE; LIZARD; MALE; NONHUMAN; PARASITOSIS; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION;

ANIMALS; CAROTENOIDS; HAIR; HOST-PARASITE INTERACTIONS; LIZARDS; MALE; MATING PREFERENCE, ANIMAL; PARASITES; PARASITIC DISEASES; PIGMENTATION; SEXUAL BEHAVIOR, ANIMAL;

ANIMALIA; PODARCIS MURALIS; SQUAMATA;

EID: 41049115961     PISSN: 00281042     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00114-007-0328-x     Document Type: Article

References (73)

1. Aitchison J (1986) The statistical analysis of compositional data. Chapman and Hall, London
2. Alberts AC (1992) Constraints on the design of chemical communication systems in terrestrial vertebrates. Am Nat 139:62-89
3. Alberts AC (1993) Chemical and behavioral studies of femoral gland secretions in iguanid lizards. Brain Behav Evol 41:255-260
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 96:378-381
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):142-144
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 160:683-691
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 8:506-517
8. Blount JD (2004) Carotenoids and life-history evolution in animals. Arch Biochem Biophys 430:10-15
9. Blount JD, Metcalfe NB, Birkhead TR, Surai PF (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125-127
10. Bradbury JW, Vehrencamp SL (1998) Principles of animal comunication. Sinauer, Sunderland, MA
11. Cooper WE, Burns N (1987) Social significance of ventrolateral coloration in the fence lizard, Sceloporus undulatus. Anim Behav 35:526-532
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 298-422
13. Cooper WE, Pérez-Mellado V, Vitt LJ (2002) Lingual and biting responses to selected lipids by the lizard Podarcis lilfordi. Physiol Behav 75:237-241
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 100:10341-10346
15. Doucet S, Montgomerie R (2003) Multiple sexual ornaments in satin bowerbirds: ultraviolet plumage and bowers signal different aspects of male quality. Behav Ecol 14:503-509
16. Edsman L (1990) Territoriality and competition in wall lizards. PhD Thesis. Univ Stockholm, Sweden
17. Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:125-153
18. Faivre B, Grégoire A, Préault M, Cézilly F, Sorci G (2003) Immune activation rapidly mirrored in a carotenoid-based secondary sexual trait. Science 300:103
19. Figuerola J, Muñoz E, Gutierrez R, Ferrer D (1999) Blood parasites, leucocytes and plumage brightness in the cirl bunting, Emberiza cirlus. Funct Ecol 13:594-601
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 44:567-575
21. Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517-546
22. Gruschwitz M, Böhme W (1986) Podarcis muralis, Mauereidechse. In: Böhme W (ed) Handbuch der Reptilien und Amphibien Europas. Aula Verlag, Wiesbaden, Germany, pp 209-23
23. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites. Science 218:384-387
24. Iwasa Y, Pomiankowski A (1994) The evolution of mate preferences for multiple sexual ornaments. Evolution 48:853-867
25. Johnstone RA (1995) Honest advertisement of multiple qualities using multiple signals. J Theor Biol 177:87-94
26. Kavaliers M, Colwell DD (1995) Discrimination by female mice between the odours of parasitized and non- parasitized males. Proc R Soc Lond B 261:31-35
27. Kwiatkowski MA, Sullivan BK (2002) Geographic variation in sexual selection among populations of an Iguanid lizard, Sauromalus obesus (=ater). Evolution 56:2039-3051
28. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116-121
29. López P, Martín J (2002) Chemical rival recognition decreases aggression levels in male Iberian wall lizards, Podarcis hispanica. Behav Ecol Sociobiol 51:461-465
30. López P, Martín J (2005) Female Iberian wall lizards prefer male scents that signal a better cell-mediated immune response. Biol Lett 1:404-406
31. López P, Martín J, Cuadrado M (2002) Pheromone mediated intrasexual aggression in male lizards, Podarcis hispanicus. Aggr Behav 28:154-163
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 54:218-224
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 32:473-488
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 58:552-557
35. Macedonia JM, James S, Wittle LW, Clark DL (2000) Skin pigments and coloration in the Jamaican radiation of Anolis lizards. J Herpetol 34:99-109
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 16:31-38
37. Martín J, López P (2006b) Links between male quality, male chemical signals, and female mate choice in Iberian rock lizards. Funct Ecol 20:1087-1096
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 273:2619-2624
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 20:290-299
40. Mason RT (1992) Reptilian pheromones. In: Gans C, Crews D (eds) Biology of the reptilia, vol 18. University of Chicago Press, Chicago, pp 114-228
41. McGraw KJ (2005) The antioxidant function of many animal pigments: are there consistent health benefits of sexually selected colourants. Anim Behav 69:757-764
42. McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704-712
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 11:137-159
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 90-147
45. Olsson M (1994) Nuptial coloration in the sand lizard, Lacerta agilis: an intra-sexually selected cue to fighting ability. Anim Behav 48:607-613
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) 270:254-256
47. Oppliger A, Celerier ML, Clobert J (1996) Physiological and behaviour changes in common lizards parasitized by haemogregarines. Parasitol 113:433-438
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 82:1713-1719
49. Ortiz E, Throckmorton LH, Williams-Ashman HG (1962) Drosopterins in the throat-fans of some Puerto Rican lizards. Nature 196:595-596
50. Penn D, Potts WK (1998) Chemical signals and parasite mediated sexual selection. Trends Ecol Evol 13:391-396
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 104:685-694
52. Pomiankowski AN (1988) The evolution of female mate preferences for male genetic quality. Oxford Surv Evol Biol 5:136-184
53. Rantala MJ, Jokinen I, Kortet R, Vainikka A, Suhonen J (2002) Do pheromones reveal male immunocompetence. Proc R Soc Lond B 269:1681-1685
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 17:534-540
55. Ressel S, Schall JJ (1989) Parasites and showy males: malarial infection and color variation in fence lizards. Oecologia 78:158-164
56. Rowe C (1999) Receiver psychology and the evolution of multicomponent signals. Anim Behav 58:921-931
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 28:408-412
58. Saks L, Ots I, Hõrak P (2003a) Carotenoid-based plumage coloration of male greenfinches reflects health and immunocompetence. Oecologia 134:301-307
59. Saks L, McGraw K, Hõrak P (2003b) How feather colour reflects its carotenoid content. Funct Ecol 17:55-561
60. Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13:567-572
61. Sullivan MS (1994) Mate choice as an information gathering process under time constraint: implications for behaviour and signal design. Anim Behav 47:141-151
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 98:12561-12565
63. Thompson CW, Moore MC (1991) Throat colour reliably signals status in male tree lizards Urosaurus ornatus. Anim Behav 42:298-442
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 82:313-318
65. Wedekind C (1992) Detailed information about parasites revealed by sexual ornamentation. Proc R Soc Lond B 247:169-174
66. Wedekind C, Folstad I (1994) Adaptive or nonadaptive immunosuppression by sex hormones. Am Nat 143:936-938
67. Weiss SL (2006) Female-specific color is a signal of quality in the striped plateau lizard (Sceloporus virgatus). Behav Ecol 17:726-732
68. Westneat DF, Birkhead TR (1998) Alternative hypothesis linking the immune system and mate choice for good genes. Proc R Soc Lond B 265:1065-1073
69. Wintrobe MM (1991) Clinical haematology. Lea and Feiberger, Philadelphia, PA
70. Wyatt TD (2003) Pheromones and animal behaviour. Cambridge University Press, Cambridge
71. Zahavi A (1975) Mate selection-a selection for a handicap. J Theor Biol 53:205-214
72. Zala SM, Potts WK, Penn DJ (2004) Scent-marking displays provide honest signals of health and infection. Behav Ecol 15:338-344
73. Zucker N (1994) A dual status-signalling system: a matter of redundancy or differing roles. Anim Behav 47:15-22