Honest sexual signalling mediated by parasite and testosterone effects on oxidative balance

Proceedings of the Royal Society B: Biological Sciences

Volumn 276, Issue 1659, 2009, Pages 1093-1100

  Mougeot, Francois ^a,b   Martínez Padilla, Jesús ^c   Webster, Lucy M I ^c   Blount, Jonathan D ^d   Pérez Rodríguez, Lorenzo ^b,c   Piertney, Stuart B ^c  

^a DEPARTAMENTO DE ECOLOGÍA FUNCIONAL Y EVOLUTIVA   (Spain)

^b INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS IREC CSIC UCLM JCCM   (Spain)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

^d UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

Antioxidant; Ornament; Oxidative stress; Red grouse Lagopus lagopus scoticus; Trade off; Trichostrongylus tenuis

Indexed keywords

DEFENSE MECHANISM; EVOLUTION; GAMEBIRD; HONEST SIGNALING; NEMATODE; ORNAMENTATION; OXIDATION; PARASITE; PIGMENT; SEXUAL BEHAVIOR; TESTOSTERONE;

AVES; LAGOPUS LAGOPUS SCOTICUS; TETRAONIDAE; TRICHOSTRONGYLUS TENUIS;

EID: 60049091052     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2008.1570     Document Type: Article

References (41)

1. Agarwal, R. & Chase, S. D. 2002 Rapid fluorimetric-liquid chromatographic determination of malondialdehyde in biological samples. J. Chromatogr. B 775, 121-126.
2. Alonso-Alvarez, C., Bertrand, S., Faivre, B., Chastel, O. & Sorci, G. 2007 Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc. R. Soc. B 274, 819-825.
3. Alonso-Alvarez, C., Pérez-Rodr?́guez, L., Mateo, R., Chastel, O. & Viñuela, J. 2008 The oxidation handicap hypothesis and the carotenoid allocation trade-off. J. Evol. Biol. 21, 1789-1797.
4. Andersson, M. 1994 Sexual selection. Princeton, NJ: Princeton University Press.
5. Blas, J., Perez-Rodriguez, L., Bortolotti, G. R., Vinuela, J. & Marchant, T. A. 2006 Testosterone increases bioavailibility of carotenoids: insights into the honesty of sexual signalling. Proc. Natl Acad. Sci. USA 103, 18 633-18 637.
6. Buchanan, K. L., Evans, M. R., Goldsmith, A. R., Bryant, D. M. & Rowe, L. V. 2001 Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling? Proc. R. Soc. B 268, 1337-1344.
7. Costantini, D. & Møller, A. P. 2008 Carotenoids are minor antioxidants for birds. Funct. Ecol. 22, 367-370.
8. Delahay, R. J., Speakman, J. R. & Moss, R. 1995 The energetic consequences of parasitism - effects of a developing infection of Trichostrongylus tenuis (Nematoda) on red grouse (Lagopus lagopus scoticus): energy balance, body weight and condition. Parasitology 110, 473-482.
9. Finkel, T. & Holbrook, N. J. 2000 Oxidants, oxidative stress and the biology of ageing. Nature 408, 239-247.
10. Folstad, I. & Karter, A. J. 1992 Parasites, bright males, and the immunocompetence handicap. Am. Nat. 139, 603-622.
11. Galván, I. & Alonso-Alvarez, C. 2008 An intracellular antioxidant determines the expression of a melanin-based signal in a bird. PLoS One 3, e3335.
12. Getty, T. 2002 Signaling health versus parasites. Am. Nat. 159, 363-371.
13. Halliwell, B. & Gutteridge, J. 2007 Free radicals in biology and medicine. New York, NY: Oxford University Press.
14. Hamilton, W. D. & Zuk, M. 1982 Heritable true fitness and bright birds - a role for parasites. Science 218, 384-387.
15. Hudson, P. J. 1986 The red grouse: the biology and management of a wild gamebird. Fordingbridge, UK: The Game Conservancy Trust.
16. Hõrak, P., Saks, L., Zilmer, M., Karu, U. & Zilmer, K. 2007 Do dietary antioxidants alleviate the cost of immune activation? An experiment with greenfinches. Am. Nat. 170, 625-635.
17. Larbi, A., Kempf, J. & Pawelec, G. 2007 Oxidative stress modulation and T cell activation. Exp. Gerontol. 42, 852-858.
18. Martinez-Padilla, J., Mougeot, F., Pérez-Rodr?́guez, L. & Bortolotti, G. R. 2007 Nematode parasites reduce carotenoid-based signalling in male red grouse. Biol. Lett. 3, 161-164.
19. McGraw, K. J. 2005 The antioxidant function of many animal pigments: are there consistent health benefits of sexually selected colourants? Anim. Behav. 69, 757-764.
20. McGraw, K. J. & Ardia, D. R. 2007 Do carotenoids buffer testosterone-mediated immunosuppression? an experimental test in a colorful songbird. Biol. Lett. 3, 375-378.
21. McGraw, K. J., Correa, S. M. & Adkins-Regan, E. 2006 Testosterone upregulates lipoprotein status to control sexual attractiveness in a colorful songbird. Behav. Ecol. Sociobiol. 60, 117-122.
22. Moss, R., Trenholm, I. B., Watson, A. & Parr, R. 1990 Parasitism, predation and survival of hen red grouse Lagopus lagopus scoticus in spring. J. Anim. Ecol. 59, 631-642.
23. Mougeot, F., Redpath, S. M., Leckie, F. & Hudson, P. J. 2003 The effect of aggressiveness on the population dynamics of a territorial bird. Nature 421, 737-739.
24. Mougeot, F., Dawson, A., Redpath, S. & Leckie, F. 2005a Testosterone and autumn territorial behaviour in male red grouse Lagopus lagopus scoticus. Horm. Behav. 47, 576-584.
25. Mougeot, F., Redpath, S., Piertney, S. B. & Hudson, P. J. 2005b Separating behavioural and physiological mechanisms in testosterone mediated trade-offs. Am. Nat. 166, 158-168.
26. Mougeot, F., Martinez-Padilla, J., Pérez-Rodríguez, L. & Bortolotti, G. R. 2007a Carotenoid-based coloration and ultraviolet reflectance of the sexual ornaments of grouse. Behav. Ecol. Soc. 61, 741-751.
27. Mougeot, F., Pérez-Rodr?́guez, L., Mart?́nez-Padilla, J., Leckie, F. M. & Redpath, S. M. 2007b Parasites, testosterone and honest carotenoid-based signaling of health. Funct. Ecol. 21, 886-898.
28. Owen-Ashley, N. T., Hasselquist, D. & Wingfield, J. 2004 Androgens and the immunocompetence handicap hypothesis: unraveling direct and indirect pathways of immunosupression in song sparrows. Am. Nat. 164, 490-505.
29. Redpath, S., Mougeot, F., Leckie, F. & Evans, S. 2006 The effects of autumn testosterone on survival and productivity in red grouse Lagopus lagopus scoticus. Anim. Behav. 71, 1297-1305.
30. Roberts, M. L., Buchanan, K. L. & Evans, M. R. 2004 Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim. Behav. 68, 227-239.
31. Romero, F. J., Bosch-Morell, F., Romero, M. J., Jareno, E. J., Romero, B., Marin, N. & Roma, J. 1998 Lipid peroxidation products and antioxidant in human diseases. Environ. Health Perspect. 106, 1229-1234.
32. Råberg, L., Grahn, M., Hasselquist, D. & Svensson, E. 1998 On the adaptive significance of stress-induced immunosuppression. Proc. R. Soc. B 265, 1637-1641.
33. SAS 2001 SAS/STAT user's guide, v. 8.01. Cary, NC: SAS Insitute Inc.
34. Seivwright, L. J., Redpath, S., Mougeot, F., Watt, L. & Hudson, P. J. 2004 Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus. J. Helminthol. 78, 69-76.
35. Seivwright, L. J., Redpath, S., Mougeot, F., Leckie, F. & Hudson, P. J. 2005 Interactions between intrinsic and extrinsic mechanisms in a cyclic species: testosterone increases parasite infection in red grouse. Proc. R. Soc. B 272, 1299-1304.
36. Shaw, J. L. 1988 Epidemiology of the caecal threadworm Trichostrongylus tenuis in red grouse (Lagopus lagopus scoticus). PhD thesis, University of Aberdeen, Aberdeen, UK.
37. Splettstoesser, W. D. & Schuff-Werner, P. 2002 Oxidative stress in phagocytes: 'the enemy within'. Microsc. Res. Tech. 57, 441-455.
38. von Schantz, T., Bensch, S., Grahn, M., Hasselquist, D. & Wittzell, H. 1999 Good genes, oxidative stress and condition-dependent sexual signals. Proc. R. Soc. B 266, 1-12.
39. Washburn, B. E., Millspaugh, J. J., Morris, D. L., Schulz, J. H. & Faaborg, J. 2007 Using a commercially available enzyme immunoassay to quantify testosterone in avian plasma. Condor 109, 181-186.
40. Wingfield, J., Soma, K. K., Wikelski, M., Meddle, S. L. & Hau, M. 2001 Life cycles, behavioural traits and endocrine mechanisms. In Avian endochrinology (eds A. Dawson & C. M. Chaturvedi), pp. 3-17. New Delhi: Narosa Publishing House.
41. Zahavi, A. 1975 Mate selection - selection for a handicap. J. Theor. Biol. 53, 205-214.