Functionally opposing effects of testosterone on two different types of parasite: Implications for the immunocompetence handicap hypothesis

Functional Ecology

Volumn 25, Issue 1, 2011, Pages 132-138

  Fuxjager, Matthew J ^a   Foufopoulos, Johannes ^a,b   Diaz Uriarte, Ramon ^a   Marler, Catherine A ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Behaviour; Ectoparasites; Endoparasites; Immunocompetence handicap hypothesis; Lizard; Sceloporus jarrovi; Territoriality; Testosterone

Indexed keywords

ABUNDANCE; ECTOPARASITE; ENDOPARASITE; HANDICAP PRINCIPLE; IMMUNE SYSTEM; IMMUNOCOMPETENCE; LIFE HISTORY TRAIT; LIZARD; MITE; NEMATODE; TERRITORIALITY; TESTOSTERONE;

ACARI; NEMATODA; PHYSALOPTERA RETUSA; PLASMODIUM CHIRICAHUAE; SCELOPORUS JARROVII; SCELOPORUS JARROVII JARROVII; SPAULIGODON GIGANTICUS; SQUAMATA; TROMBICULIDAE; VERMES;

EID: 78751695299     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/j.1365-2435.2010.01784.x     Document Type: Article

References (49)

1. Arriero, E. & Moller, A.P. (2008) Host ecology and life-history traits associated with blood parasite species richness in birds. Journal of Evolutionary Biology, 21, 1504-1513.
2. Bennett, S.G. (1977) Ecology and Systematics of Trombiculid Mites on Lizards from Southern Arizona. MS thesis, California State University-Long Beach, Long Beach, CA.
3. Braude, S., Tang-Martinez, Z. & Taylor, G.T. (1999) Stress, testosterone, and the immunoredistribution hypothesis. Behavioral Ecology, 10, 345-350.
4. Buchanan, K.L. (2000) Stress and the evolution of condition-dependent signals. Trends in Ecology & Evolution, 15, 156-160.
5. Bull, C.M. & Burzacott, D.A. (2006) The influence of parasites on the retention of long-term partnerships in the Australian sleepy lizard, Tiliqua rugosa. Oecologia, 146, 675-680.
6. Burnham, K.P. & Anderson, D.R. (2002) Model Selection and Multimodal Inference: A Practical Information - Theoretic Approach. Springer, New York, USA.
7. Bursey, C.R. & Goldberg, S.R. (1991) Monthly prevalences of Physaloptera retusa in naturally infected yarrow spiny lizards. Journal of Wildlife Diseases, 27, 710-715.
8. Bursey, C.R. & Goldberg, S.R. (1992) Monthly prevalences of Spauligodon giganticus (nematoda, Pharyngodonidae) in naturally infected yarrow spiny lizard Sceloporus jarrovi jarrovi (iguanidae). American Midland Naturalist, 127, 204-207.
9. Buttemer, W.A. & Astheimer, L.B. (2000) Testosterone does not affect basal metabolic rate or blood parasite load in captive male white-plumed honeyeaters, Lichenostomus penicillatus. Journal of Avian Biology, 31, 479-488.
10. Casto, J.M., Nolan, V. & Ketterson, E.D. (2001) Steroid hormones and immune function: experimental studies in wild and captive dark-eyed juncos (Junco hyemalis). American Naturalist, 157, 408-420.
11. Claerbout, E. & Vercruysse, J. (2000) The immune response and the evaluation of acquired immunity against gastroinstestinal nematodes in cattle: a review. Parasitology, 120, S25-S42.
12. Cox, R.M. & John-Alder, H.B. (2007) Increased mite parasitism as a cost of testosterone in male striped plateau lizards, Sceloporus virgatus. Functional Ecology, 21, 327-334.
13. De Fazio, A., Simon, C.A., Middendorf, G.A. & Romano, D. (1977) Iguanid substrate licking: a response to a novel situation in Sceloporus jarrovi. Copeia, 1977, 706-709.
14. Denardo, D.F. & Sinervo, B. (1994) Effects of steroid hormone interactions on activity and home-range size in male lizards. Hormones and Behavior, 28, 273-287.
15. Duckworth, R.A., Mendonca, M.T. & Hill, G.E. (2001) A condition dependent link between testosterone and disease resistance in the house finch. Proceedings of the Royal Society of London, Series B: Biological Sciences, 268, 2467-2472.
16. Duffy, D.L., Bentley, G.E., Drazen, D.L. & Ball, G.F. (2000) Effects of testosterone on cell-mediated and humoral immunity in non-breeding adult European starlings. Behavioral Ecology, 11, 654-662.
17. Eisen, R.J. & Denardo, D.F. (2000) Life history of a malaria parasite (Plasmodium mexicanum) in its host, the western fence lizard (Sceloporus occidentalis): host testosterone as a source of seasonal and among-host variation? Journal of Parasitology, 86, 1041-1045.
18. Ezenwa, V.O. (2004) Host social behavior and parasitic infection: a multifactorial approach. Behavioral Ecology, 15, 446-454.
19. Folstad, I. & Karter, A.J. (1992) Parasites, bright males, and the immunocompetence handicap. American Naturalist, 139, 603-622.
20. Foufopoulos, J. (1999) Host-parasite interactions in the mountain spiny lizard, Sceloporus jarrovi. PhD thesis, University of Wisconsin-Madison, Madison.
21. Freeman, G.H. & Halton, J.H. (1951) Note on the exact treatment of contingency, goodness of fit and other problems of significance. Biometrika, 38, 141-149.
22. Goldberg, S.R. & Holshuh, H.J. (1992) Ectoparasite-induced lesions in mite pockets of the yarrow's spiny lizard, Sceloporus jarrovii (Phrynosomatidae). Journal of Wildlife Diseases, 28, 537-541.
23. Hughes, V.L. & Randolph, S.E. (2001) Testosterone depresses innate and acquired resistance to ticks in natural rodent hosts: a force for aggregated distributions of parasites. Journal of Parasitology, 87, 49-54.
24. Klukowski, M. & Nelson, C.E. (2001) Ectoparasite loads in free-ranging northern fence lizards, Sceloporus undulatus hyacinthinus: effects of testosterone and sex. Behavioral Ecology and Sociobiology, 49, 289-295.
25. Marler, C.A. & Moore, M.C. (1988) Evolutionary costs of aggression revealed by testosterone manipulations in free-living male lizards. Behavioral Ecology and Sociobiology, 23, 21-26.
26. Marler, C.A. & Moore, M.C. (1989) Time and energy costs of aggression in testosterone-implanted free-living male mountain spiny lizards (Sceloporus jarrovi). Physiological Zoology, 62, 1334-1350.
27. Marler, C.A. & Moore, M.C. (1991) Supplementary feeding compensates for testosterone-induced costs of aggression in male mountain spiny lizards, Sceloporus jarrovi. Animal Behaviour, 42, 209-219.
28. 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. Behavioral Ecology and Sociobiology, 62, 173-179.
29. Moore, M.C. (1986) Elevated testosterone levels during nonbreeding-season territoriality in a fall-breeding lizard, Sceloporus jarrovi. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 158, 159-163.
30. Moore, M.C. (1987) Castration affects territorial and sexual behavior of free-living male lizards, Sceloporus jarrovi. Animal Behaviour, 35, 1193-1199.
31. Moore, M.C. (1988) Testosterone control of territorial behavior: tonic release implants fully restore seasonal and short term aggressive responses in free-living castrated lizards. General and Comparative Endocrinology, 70, 450-459.
32. Moore, M.C. & Marler, C.A. (1987) Effects of testosterone manipulations on nonbreeding season territorial aggression in free-living male lizards, Sceloporus jarrovi. General and Comparative Endocrinology, 65, 225-232.
33. Nunn, C.L. & Dokey, A.T.W. (2006) Ranging patterns and parasitism in primates. Biology Letters, 2, 351-354.
34. Olsson, M., Wapstra, E., Madsen, T. & Silverin, B. (2000) Testosterone, ticks and travels: a test of the immunocompetence-handicap hypothesis in free-ranging male sand lizards. Proceedings of the Royal Society of London, Series B: Biological Sciences, 267, 2339-2343.
35. Oppliger, A., Giorgi, M.S., Conelli, A., Nembrini, M. & John-Alder, H.B. (2004) Effect of testosterone on immunocompetence, parasite load, and metabolism in the common wall lizard (Podarcis muralis). Canadian Journal of Zoology/Revue Canadienne de Zoologie, 82, 1713-1719.
36. Poiani, A., Goldsmith, A.R. & Evans, M.R. (2000) Ectoparasites of house sparrows (Passer domesticus): an experimental test of the immunocompetence handicap hypothesis and a new model. Behavioral Ecology and Sociobiology, 47, 230-242.
37. Raberg, L., Grahn, M., Hasselquist, D. & Svensson, E. (1998) On the adaptive significance of stress-induced immunosuppression. Proceedings of the Royal Society of London, Series B: Biological Sciences, 265, 1637-1641.
38. Read, C.P. & Amrein, Y.U. (1953) North American nematodes of the genus Pharyngodon Diesing (Oxyuridae). Journal of Parasitology, 39, 365-370.
39. Roberts, M.L., Buchanan, K.L. & Evans, M.R. (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Animal Behaviour, 68, 227-239.
40. Rudolphi, C.A. (1819) Entozoorum Synopsis, Cui Accedunt Mantissa Duplex et Indices Locupletissimi. Augusti Rucker, Berlin, Germany.
41. Saino, N., Moller, A.P. & Bolzern, A.M. (1995) Testosterone effects on the immune system and parasite infestations in the barn swallow (Hirundo rustica): an experimental test of the immunocompetence hypothesis. Behavioral Ecology, 6, 397-404.
42. Schall, J.J. (1983) Lizard malaria: parasite-host ecology. Lizard Ecology (eds R. B. Huey, E. R. Pianka & T. W. Schoener ), pp. 84-100. Havard University Press, Cambridge.
43. Sheldon, B.C. & Verhulst, S. (1996) Ecological immunity: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology & Evolution, 11, 317-321.
44. Sorci, G. & Clobert, J. (1995) Effects of maternal parasite load on offspring life-history traits in the common lizard (Lacerta vivipara). Journal of Evolutionary Biology, 8, 711-723.
45. Telford, S.R. (1970) A comparative study of endoparasitism among some southern California lizard populations. American Midland Naturalist, 83, 516-554.
46. Veiga, J.P., 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.
47. Wang, H., Paesen, G.C., Nuttall, P.A. & Barbour, A.G. (1998) Male ticks helps their mates to feed. Nature, 391, 753-754.
48. Wikelski, M., Lynn, S., Breuner, C., Wingfield, J.C. & Kenagy, G.J. (1999) Energy metabolism, testosterone and corticosterone in white-crowned sparrows. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology, 185, 463-470.
49. Zar, J.H. (1999) Biostatistical Analysis. Prentice Hall, Upper Saddle River, New Jersey USA.