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

Naturwissenschaften

Volumn 100, Issue 6, 2013, Pages 551-558

  Molnár, Orsolya ^a,c   Bajer, Katalin ^b,c   Mészáros, Boglárka ^c   Török, János ^c   Herczeg, Gábor ^c  

^a Lamont Doherty Earth Observatory   (United States)

^b FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

Blood parasite; Haemogregarinidae; Hamilton Zuk hypothesis; Lizard; Nuptial coloration

Indexed keywords

ADAPTATION; BLOOD; BRIGHTNESS TEMPERATURE; COLOR; CORRELATION; DEVELOPMENTAL BIOLOGY; FITNESS; GENE EXPRESSION; HOST-PARASITE INTERACTION; INTRASEXUAL INTERACTION; LIZARD; MATE CHOICE; SEXUAL SELECTION; SIGNALING;

ANIMAL; ARTICLE; BLOOD; COCCIDIA; COCCIDIOSIS; LIZARD; MALE; PARASITE LOAD; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; PIGMENTATION; SEXUAL BEHAVIOR;

ANIMALS; COCCIDIOSIS; EUCOCCIDIIDA; LIZARDS; MALE; PARASITE LOAD; PIGMENTATION; SEXUAL BEHAVIOR, ANIMAL;

LACERTA VIRIDIS; SQUAMATA;

EID: 84879554798     PISSN: 00281042     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00114-013-1051-4     Document Type: Article

References (67)

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):7-15
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):378-381
3. Andersson M (1994) Sexual selection. Princeton University Press, Princeton
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):2007-2014
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
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, Malabar
8. Borgia G (1986) Satin bowerbird parasites - a test of the bright male hypothesis. Behav Ecol Sociobiol 19:355-358
9. Borgia G, Collis K (1990) Parasites and bright male plumage in the satin bowerbird (Ptilonorhynchus violaceus). Am Zool 30:279-285
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):77-85
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):949-954
12. Brawner WR, Hill GE, Sundermann CA (2000) Effects of coccidial and mycoplasmal infections on carotenoid-based plumage pigmentation in male house finches. Auk 117:952-963
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):668-676
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
15. Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78(4):575-595
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):843-850
17. Clayton DH (1990) Mate choice in experimentally parasitized rock doves - lousy males lose. Am Zool 30(2):251-262
18. Clayton DH (1991) The influence of parasites on host sexual selection. Par Tod 7:329-334
19. Davies AJ, Reed CC, Smit NJ (2003) An unusual intraerythrocytic parasite of Parablennius cornutus from South Africa. J Parasitol 89(5):913-917
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 162:825-835
21. Dunlap KD (1993) Effects of nymphal ticks and their interaction with malaria on the physiology of male fence lizards. Copeia 4:1045-1048
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):1299-1305
23. Grether GF, Kolluru GR, Nersissian K (2004) Individual colour patches as multicomponent signals. Biol Rev 79:583-610. doi: 10.1017/S1464793103006390
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 13:384-387
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
26. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds - a role for parasites. Science 218(4570):384-387
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 74:337-341
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
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
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):323-328
31. Lebas NR, Marshall NJ (2001) No evidence of female choice for a condition-dependent trait in the agamid lizard, Ctenophorus ornatus. Behaviour 138:965-980
32. Lefcort H, Blaustein AR (1991) Parasite load and brightness in lizards - an interspecific test of the Hamilton and Zuk hypothesis. J Zool 224:491-499
33. Leu ST, Kappeler PM, Bull CM (2010) Refuge sharing network predicts ectoparasite load in a lizard. Behav Ecol Sociobiol 64(9):1495-1503
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
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
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):1743-1755
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):1525-1531
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):3747-3755
39. Moller AP (1990) Parasites and sexual selection - current status of the Hamilton and Zuk hypothesis. J Evol Biol 3(5-6):319-328
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
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
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
43. Murtaugh PA (2009) Performance of several variable-selection methods applied to real ecological data. Ecol Lett 12(10):1061-1068
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
45. Oppliger A, Celerier ML, Clobert J (1996) Physiological and behaviour changes in common lizards parasitized by haemogregarines. Parasitology 113:433-438
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):952-966
47. Palmer AR, Strobeck C (1986) Fluctuating asymmetry - measurement, analysis, patterns. Annu Rev Ecol Syst 17:391-421
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):175-181
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 169:122-136
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 65:3-15
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
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 75:75-79
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
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
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):543-548
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
57. Smallridge CJ, Bull CM (1999) Transmission of the blood parasite Hemolivia mariae between its lizard and tick hosts. Parasitol Res 85(10):858-863
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
59. Telford SR (2009) Haemoparasites of the Reptilia. CRC, Boca Raton
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
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 136-179
62. van Valen L (1962) A study of fluctuating asymmetry. Evolution 16:125-142
63. Weiss SL (2006) Female-specific color is a signal of quality in the striped plateau lizard (Sceloporus virgatus). Behav Ecol 17(5):726-732
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 72:353-363
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 65:335-338
66. Zahavi A (1975) Mate selection - selection for a handicap. J Theor Biol 53:205-214
67. Zahavi A (1977) Cost of honesty - (further remarks on handicap principle). J Theor Biol 67(3):603-605