Behavioral Ecology and Sociobiology

, Volume 67, Issue 2, pp 221–234 | Cite as

A transcriptomic investigation of handicap models in sexual selection

  • Marius A. WenzelEmail author
  • Lucy M. I. Webster
  • Steve Paterson
  • François Mougeot
  • Jesús Martínez-Padilla
  • Stuart B. Piertney
Original Paper


Handicap models link the evolution of secondary sexual ornaments to physiological costs and thus provide a mechanistic explanation for signal honesty in sexual selection. Two commonly invoked models, the immunocompetence handicap hypothesis (ICHH) and the oxidative stress handicap hypothesis (OSHH), propose suppression of immunocompetence or increase of oxidative stress by testosterone, but empirical evidence for both models is controversial and based on morphological and physiological assays. Here, we investigated these two models on the gene transcription level using microarrays to quantify the transcriptomic response of red grouse (Lagopus lagopus scoticus) caecal, spleen and liver tissues to experimental manipulation of testosterone levels. We used a geneontology framework to identify genes related to immune function and response to reactive oxygen species and examined how transcription levels changed under experimentally increased testosterone levels in birds with parasites present or absent. Contrary to our expectations, testosterone had virtually no effect on gene transcription in spleen and liver. A small number of genes were significantly differentially regulated in caecum, and while their functions and transcription changes are consistent with the ICHH, we found little support for the OSHH. More genes responded to testosterone in the presence rather than absence of parasites, suggesting that handicap mechanisms may be context dependent and more pronounced in the presence of adverse environmental conditions. These findings illustrate the utility of transcriptomics to investigating handicap models, suggest that classic models may not underlie the handicap mechanism, and indicate that novel emerging models involving different mediators and physiological systems should be examined.


Sexual selection Immunocompetence handicap hypothesis ICHH Oxidative stress handicap hypothesis OSHH Transcriptomics 



We are grateful to D. Calder and T. Helps for access to study sites, and G. Murray-Dickson and M. Oliver for help with fieldwork and comments on manuscript drafts. This work was funded by NERC grant NE/D000602/1 (SBP), a NERC advanced fellowship (FM) and a BBSRC studentship (MAW).

Ethical standards

The necessary UK Home Office licences for conducting the fieldwork procedures described in this study were held.

Conflicts of interest

The authors declare that they have no conflicts of interest.

Supplementary material

265_2012_1442_MOESM1_ESM.pdf (203 kb)
Tables S1–S2 Top blast hit descriptions for identified immune genes (S1) and ROS response genes (S2) (PDF 202 kb)
265_2012_1442_MOESM2_ESM.pdf (339 kb)
Tables S3–S4 Full geneontology annotations for all significantly (q < 0.05) differentially regulated immune genes (S3) and ROS response genes (S4) (PDF 338 kb)


  1. Alonso-Alvarez C, Bertrand S, Faivre B, Chastel O, Sorci G (2007) Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc R Soc Lond B 274:819–825CrossRefGoogle Scholar
  2. Alonso-Alvarez C, Pérez-Rodríguez L, Mateo R, Chastel O, Viñuela J (2008) The oxidation handicap hypothesis and the carotenoid allocation trade-off. J Evol Biol 21:1789–1797PubMedCrossRefGoogle Scholar
  3. Alonso-Alvarez C, Pérez-Rodríguez L, Garcia JT, Viñuela J (2009) Testosterone-mediated trade-offs in the old age: a new approach to the immunocompetence handicap and carotenoid-based sexual signalling. Proc R Soc Lond B 276:2093–2101CrossRefGoogle Scholar
  4. Andersson M (1982) Sexual selection, natural selection and quality advertisement. Biol J Linn Soc 17:375–393CrossRefGoogle Scholar
  5. Andersson M (1994) Sexual Selection. Princeton University Press, PrincetonGoogle Scholar
  6. Andersson MS, Ödeen A, Håstad O (2006) A partly coverable badge signalling avian virus resistance. Acta Zool 87:71–76CrossRefGoogle Scholar
  7. Bankoti R, Stäger S (2012) Differential regulation of the immune response in the spleen and liver of mice infected with Leishmania donovani. J Trop Med 639304Google Scholar
  8. Bayeva M, Ardehali H (2010) Mitochondrial dysfunction and oxidative damage to sarcomeric proteins. Curr Hypertens Rep 12:426–432PubMedCrossRefGoogle Scholar
  9. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300Google Scholar
  10. Berger S, Martin LB, Wikelski M, Romero LM, Kalko EK, Vitousek MN, Rödl T (2005) Corticosterone suppresses immune activity in territorial Galapagos marine iguanas during reproduction. Horm Behav 47:419–429PubMedCrossRefGoogle Scholar
  11. Besedovsky H, Rey AD, Sorkin E, Dinarello CA (1986) Immunoregulatory feedback between interleukin-1 and glucocorticoid hormones. Science 233:652–654PubMedCrossRefGoogle Scholar
  12. Blas J, Pérez-Rodríguez L, Bortolotti GR, Vinuela J, Marchant TA (2006) Testosterone increases bioavailability of carotenoids: insights into the honesty of sexual signaling. Proc Natl Acad Sci U S A 103:18,633–18,637CrossRefGoogle Scholar
  13. Blount JD, Speed MP, Ruxton GD, Stephens PA (2003) Warning displays may function as honest signals of toxicity. Proc R Soc Lond B 276:871–877CrossRefGoogle Scholar
  14. Boonekamp JJ, Ros AHF, Verhulst S (2008) Immune activation suppresses plasma testosterone level: a meta-analysis. Biol Lett 4:741–744PubMedCrossRefGoogle Scholar
  15. Bortolotti GR, Mougeot F, Martínez-Padilla J, Webster LMI, Piertney SB (2009) Physiological stress mediates the honesty of social signals. PLoS One 4:e4983PubMedCrossRefGoogle Scholar
  16. Brockmann R, Beyer A, Heinisch JJ, Wilhelm T (2007) Posttranscriptional expression regulation: what determines translation rates? PLoS Comput Biol 3:e57PubMedCrossRefGoogle Scholar
  17. Buchanan KL (2000) Stress and the evolution of condition-dependent signals. Trends Ecol Evol 15:156–160PubMedCrossRefGoogle Scholar
  18. Buchanan KL, Evans MR, Goldsmith AR, Bryant DM, Rowe LV (2001) Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling? Proc R Soc Lond B 268:1337–1344CrossRefGoogle Scholar
  19. Buchanan KL, Evans MR, Goldsmith AR (2003) Testosterone, dominance signalling and immunosuppression in the house sparrow, Passer domesticus. Behav Ecol Sociobiol 55:50–59CrossRefGoogle Scholar
  20. Carson SD, Chapman NM (2001) Coxsackievirus and adenovirus receptor (CAR) binds immunoglobulins. Biochemistry 40:14,324–14,329CrossRefGoogle Scholar
  21. Casagrande S, Groothuis TGG (2011) The interplay between gonadal steroids and immune defence in affecting a carotenoid-dependent trait. Behav Ecol Sociobiol 65:2007–2019PubMedCrossRefGoogle Scholar
  22. Casto JM, Nolan V Jr, Ketterson ED (2001) Steroid hormones and immune function: experimental studies in wild and captive dark-eyed juncos (Junco hyemalis). Am Nat 157:408–420PubMedCrossRefGoogle Scholar
  23. Conesa A, Götz S (2008) blast2go: A comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 619832Google Scholar
  24. Conesa A, Götz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) blast2go: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676PubMedCrossRefGoogle Scholar
  25. Costantini D, Møller AP (2008) Carotenoids are minor antioxidants for birds. Funct Ecol 22:367–370CrossRefGoogle Scholar
  26. Costantini D, Fanfani A, Dell’Omo G (2008) Effects of corticosteroids on oxidative damage and circulating carotenoids in captive adult kestrels (Falco tinnunculus). J Comp Physiol B 178:829–835PubMedCrossRefGoogle Scholar
  27. Cox RM, John-Alder HB (2007) Increased mite parasitism as a cost of testosterone in male striped plateau lizards Sceloporus virgatus. Funct Ecol 21:327–334CrossRefGoogle Scholar
  28. Dahl E, Orizaola G, Winberg S, Laurila A (2012) Geographic variation in corticosterone response to chronic predator stress in tadpoles. J Evol Biol 25:1066–1076PubMedCrossRefGoogle Scholar
  29. Day DA, Tuite MF (1998) Post-transcriptional gene regulatory mechanisms in eukaryotes: an overview. J Endocrinol 157:361–371PubMedCrossRefGoogle Scholar
  30. Debes PV, Normandeau E, Fraser DJ, Bernatchez L, Hutchings JA (2012) Differences in transcription levels among wild, domesticated, and hybrid atlantic salmon (Salmo salar) from two environments. Mol Ecol 21:2574–2587PubMedCrossRefGoogle Scholar
  31. Delahay RJ, Speakman JR, 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 110:473–482CrossRefGoogle Scholar
  32. Deviche P, Cortez L (2005) Androgen control of immunocompetence in the male house finch, Carpodacus mexicanus Müller. J Exp Biol 208:1287–1295PubMedCrossRefGoogle Scholar
  33. Deviche P, Parris J (2006) Testosterone treatment to free-ranging male darkeyed juncos (Junco hyemalis) exacerbates hemoparasitic infection. Auk 123:548–562CrossRefGoogle Scholar
  34. Edler R, Goymann W, Schwabl I, Friedl TWP (2011) Experimentally elevated testosterone levels enhance courtship behaviour and territoriality but depress acquired immune response in red bishops Euplectes orix. Ibis 153:46–58CrossRefGoogle Scholar
  35. Efron B (2007) Size, power and false discovery rates. Ann Stat 35:1351–1377CrossRefGoogle Scholar
  36. Evans MR, Goldsmith AR, Norris SRA (2000) The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus). Behav Ecol Sociobiol 47:156–163CrossRefGoogle Scholar
  37. Ezenwa VO, Ekernas LS, Creel S (2012) Unravelling complex associations between testosterone and parasite infection in the wild. Funct Ecol 26:123–133CrossRefGoogle Scholar
  38. Farah ME, Sirotkin V, Haarer B, Kakhniashvili D, Amberg DC (2011) Diverse protective roles of the actin cytoskeleton during oxidative stress. Cytoskeleton 68:340–354PubMedCrossRefGoogle Scholar
  39. Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247PubMedCrossRefGoogle Scholar
  40. Floyd RA (1999) Antioxidants, oxidative stress, and degenerative neurological disorders. Proc Soc Exp Biol Med 222:236–245PubMedCrossRefGoogle Scholar
  41. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622CrossRefGoogle Scholar
  42. Freeman-Gallant CR, Amidon J, Berdy B, Wein S, Taff CC, Haussmann MF (2011) Oxidative damage to DNA related to survivorship and carotenoid-based sexual ornamentation in the common yellowthroat. Biol Lett 7:429–432PubMedCrossRefGoogle Scholar
  43. Fuxjager MJ, Foufopoulos J, Diaz-Uriarte R, Marler CA (2011) Functionally opposing effects of testosterone on two different types of parasite: implications for the immunocompetence handicap hypothesis. Funct Ecol 25:132–138CrossRefGoogle Scholar
  44. Gil D, Culver R (2011) Male ornament size in a passerine predicts the inhibitory effect of testosterone on macrophage phagocytosis. Funct Ecol 25:1278–1283CrossRefGoogle Scholar
  45. Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546PubMedCrossRefGoogle Scholar
  46. Gray CP, Franco AV, Arosio P, Hersey P (2001) Immunosuppressive effects of melanoma-derived heavy-chain ferritin are dependent on stimulation of IL-10 production. Int J Cancer 92:843–850PubMedCrossRefGoogle Scholar
  47. Hamilton W, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387PubMedCrossRefGoogle Scholar
  48. Hasselquist D, Marsh JA, Sherman PW, Wingfield JC (1999) Is avian humoral immunocompetence suppressed by testosterone? Behav Ecol Sociobiol 45:167–175CrossRefGoogle Scholar
  49. Hill GE (2011) Condition-dependent traits as signals of the functionality of vital cellular processes. Ecol Lett 14:625–634PubMedCrossRefGoogle Scholar
  50. Hill GE, Farmer KL (2005) Carotenoid-based plumage coloration predicts resistance to a novel parasite in the house finch. Naturwissenschaften 92:30–34PubMedCrossRefGoogle Scholar
  51. Hudson PJ, Dobson AP, Newborn D (1992) Do parasites make prey vulnerable to predation? Red grouse and parasites. J Anim Ecol 61:681–692CrossRefGoogle Scholar
  52. Kurtz J (2007) The correlation between immunocompetence and an ornament trait changes over lifetime in Panorpa vulgaris scorpionflies. Zoology 110:336–343PubMedCrossRefGoogle Scholar
  53. Kurtz J, Kalbe M, Langefors A, Mayer I, Milinski M, Hasselquist D (2007) An experimental test of the immunocompetence handicap hypothesis in a teleost fish: 11-ketotestosterone suppresses innate immunity in three-spined sticklebacks. Am Nat 170:509–519PubMedCrossRefGoogle Scholar
  54. Martínez A, Rodríguez-Gironés MA, Barbosa A (2009) Can bird carotenoids play an antioxidant role oxidizing other substances? Ardeola 56:287–294Google Scholar
  55. Martínez-Padilla J, Mougeot F, Pérez-Rodríguez L, Bortolotti GR (2007) Nematode parasites reduce carotenoid-based signalling in male red grouse. Biol Lett 3:161–164PubMedCrossRefGoogle Scholar
  56. Martínez-Padilla J, Mougeot F, Webster LMI, Pérez-Rodríguez L, Piertney SB (2010) Testing the interactive effects of testosterone and parasites on carotenoid-based ornamentation in a wild bird. J Evol Biol 23:902–913PubMedCrossRefGoogle Scholar
  57. Mateos C (2005) The subordination stress paradigm and the relation between testosterone and corticosterone in male ring-necked pheasants. Anim Behav 69:249–255CrossRefGoogle Scholar
  58. Matzkin LM (2012) Population transcriptomics of cactus host shifts in Drosophila mojavensis. Mol Ecol 21:2428–2439PubMedCrossRefGoogle Scholar
  59. Maynard Smith J (1974) The theory of games and the evolution of animal conflicts. J Theor Biol 47:209–221CrossRefGoogle Scholar
  60. McGraw KJ, Correa SM, Adkins-Regan E (2006) Testosterone upregulates lipoprotein status to control sexual attractiveness in a colorful songbird. Behav Ecol Sociobiol 60:117–122CrossRefGoogle Scholar
  61. Møller AP, Saino N (1994) Parasites, immunology of hosts, and host sexual selection. J Parasitol 80:850–858PubMedCrossRefGoogle Scholar
  62. Møller AP, Dufva R, Erritzoe J (1998) Host immune function and sexual selection in birds. J Evol Biol 11:703–719CrossRefGoogle Scholar
  63. Møller AP, Christe P, Lux E (1999) Parasitism, host immune function, and sexual selection. Q Rev Biol 74:3–20PubMedCrossRefGoogle Scholar
  64. Moore SL, Wilson K (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297:2015–2018PubMedCrossRefGoogle Scholar
  65. Moore FR, Cornwell RE, Law Smith MJ, Al Dujaili EAS, Sharp M, Perrett DI (2011) Evidence for the stress-linked immunocompetence handicap hypothesis in human male faces. Proc R Soc Lond B 278:774–780CrossRefGoogle Scholar
  66. Mougeot F (2008) Ornamental comb colour predicts T-cell-mediated immunity in male red grouse Lagopus lagopus scoticus. Naturwissenschaften 95:125–132PubMedCrossRefGoogle Scholar
  67. Mougeot F, Redpath SM (2004) Sexual ornamentation relates to immune function in male red grouse Lagopus lagopus scoticus. J Avian Biol 35:425–433CrossRefGoogle Scholar
  68. Mougeot F, Irvine JR, Seivwright L, Redpath SM, Piertney S (2004) Testosterone, immunocompetence, and honest sexual signaling in male red grouse. Behav Ecol 15:930–937CrossRefGoogle Scholar
  69. Mougeot F, Redpath SM, Piertney SB (2006) Elevated spring testosterone increases parasite intensity in male red grouse. Behav Ecol 17:117–125CrossRefGoogle Scholar
  70. Mougeot F, Pérez-Rodríguez L, Martínez-Padilla J, Leckie F, Redpath SM (2007) Parasites, testosterone and honest carotenoid-based signalling of health. Funct Ecol 21:886–898CrossRefGoogle Scholar
  71. Mougeot F, Martínez-Padilla J, Webster LMI, Blount JD, Pérez-Rodríguez L, Piertney SB (2009) Honest sexual signalling mediated by parasite and testosterone effects on oxidative balance. Proc R Soc Lond B 276:1093–1100CrossRefGoogle Scholar
  72. Mougeot F, Martínez-Padilla J, Blount JD, Pérez-Rodríguez L, Webster LMI, Piertney SB (2010a) Oxidative stress and the effect of parasites on a carotenoid-based ornament. J Exp Biol 213:400–407PubMedCrossRefGoogle Scholar
  73. Mougeot F, Martínez-Padilla J, Bortolotti GR, Webster LMI, Piertney SB (2010b) Physiological stress links parasites to carotenoid-based colour signals. J Evol Biol 23:643–650PubMedCrossRefGoogle Scholar
  74. Muehlenbein MP, Bribiescas RG (2005) Testosterone-mediated immune functions and male life histories. Am J Hum Biol 17:527–558PubMedCrossRefGoogle Scholar
  75. Myhre S, Tveit H, Mollestad T, Lægreid A (2006) Additional gene ontology structure for improved biological reasoning. Bioinformatics 22:2020–2027PubMedCrossRefGoogle Scholar
  76. Olson VA, Owens IP (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514PubMedCrossRefGoogle Scholar
  77. 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 82:1713–1719CrossRefGoogle Scholar
  78. Ottová E, Simková A, Jurajda P, Dávidová M, Ondracková M, Pecínková M, Gelnar M (2005) Sexual ornamentation and parasite infection in males of common bream (Abramis brama): a reflection of immunocompetence status or simple cost of reproduction? Evol Ecol Res 7:581–593Google Scholar
  79. Owen-Ashley NT, Hasselquist D, Wingfield JC (2004) Androgens and the immunocompetence handicap hypothesis: unraveling direct and indirect pathways of immunosuppression in song sparrows. Am Nat 164:490–505PubMedCrossRefGoogle Scholar
  80. Pemberton JM, Beraldi D, Craig BH, Hopkins J (2011) Digital gene expression analysis of gastrointestinal helminth resistance in Scottish blackface lambs. Mol Ecol 20:910–919PubMedCrossRefGoogle Scholar
  81. Pérez-Rodríguez L, Mougeot F, Alonso-Alvarez C (2010) Carotenoid-based coloration predicts resistance to oxidative damage during immune challenge. J Exp Biol 213:1685–1690PubMedCrossRefGoogle Scholar
  82. Peters A, Denk AG, Delhey K, Kempenaers B (2004) Carotenoid-based bill colour as an indicator of immunocompetence and sperm performance in male mallards. J Evol Biol 17:1111–1120PubMedCrossRefGoogle Scholar
  83. Rantala MJ, Moore FR, Skrinda I, Krama T, Kivleniece I, Kecko S, Krams I (2012) Evidence for the stress-linked immunocompetence handicap hypothesis in humans. Nat Commun 3:694PubMedCrossRefGoogle Scholar
  84. Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239CrossRefGoogle Scholar
  85. Roberts ML, Buchanan KL, Hasselquist D, Evans MR (2007) Effects of testosterone and corticosterone on immunocompetence in the zebra finch. Horm Behav 51:126–134PubMedCrossRefGoogle Scholar
  86. Roberts ML, Buchanan KL, Evans MR, Marin RH, Satterlee DG (2009a) The effects of testosterone on immune function in quail selected for divergent plasma corticosterone response. J Exp Biol 212:3125–3131PubMedCrossRefGoogle Scholar
  87. Roberts ML, Ras E, Peters A (2009b) Testosterone increases UV reflectance of sexually selected crown plumage in male blue tits. Behav Ecol 20:535–541CrossRefGoogle Scholar
  88. Ros AFH, Bouton N, Santos RS, Oliveira RF (2006) Alternative male reproductive tactics and the immunocompetence handicap in the Azorean rock-pool blenny, Parablennius parvicornis. Proc R Soc Lond B 273:901–909CrossRefGoogle Scholar
  89. Rowe L, Houle D (1996) The lek paradox and the capture of genetic variance by condition dependent traits. Proc R Soc Lond B 263:1415–1421CrossRefGoogle Scholar
  90. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89PubMedCrossRefGoogle Scholar
  91. Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond B 270:357–366CrossRefGoogle Scholar
  92. Seivwright LJ, Redpath SM, Mougeot F, Leckie F, Hudson PJ (2005) Interactions between intrinsic and extrinsic mechanisms in a cyclic species: testosterone increases parasite infection in red grouse. Proc R Soc Lond B 272:2299–2304CrossRefGoogle Scholar
  93. Shaw JL, Moss R (1989) Factors affecting the establishment of the caecal threadworm Trichostrongylus tenuis in red grouse (Lagopus lagopus scoticus). Parasitology 99:259–264PubMedCrossRefGoogle Scholar
  94. Strimmer K (2008) A unified approach to false discovery rate estimation. BMC Bioinformatics 9:303PubMedCrossRefGoogle Scholar
  95. The Gene Ontology Consortium (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29CrossRefGoogle Scholar
  96. Thompson AW, Huang K, Saito MA, Chisholm SW (2011) Transcriptome response of high- and low-light-adapted Prochlorococcus strains to changing iron availability. ISME J 5:1580–1594PubMedCrossRefGoogle Scholar
  97. Vergara P, Martínez-Padilla J (2012) Social context decouples the relationship between a sexual ornament and testosterone levels in a male wild bird. Horm Behav 62:407–412PubMedCrossRefGoogle Scholar
  98. Vergara P, Martínez-Padilla J, Mougeot F, Leckie F, Redpath SM (2012a) Environmental heterogeneity influences the reliability of secondary sexual traits as condition indicators. J Evol Biol 25:20–28PubMedCrossRefGoogle Scholar
  99. Vergara P, Mougeot F, Martínez-Padilla J, Leckie F, Redpath SM (2012b) The condition dependence of a secondary sexual trait is stronger under high parasite infection level. Behav Ecol 23:502–511CrossRefGoogle Scholar
  100. Versteegh MA, Schwabl I, Jaquier S, Tieleman BI (2012) Do immunological, endocrine and metabolic traits fall on a single pace-of-life axis? covariation and constraints among physiological systems. J Evol Biol 25:1864–1876PubMedCrossRefGoogle Scholar
  101. Vinkler M, Albrecht T (2010) Carotenoid maintenance handicap and the physiology of carotenoid-based signalisation of health. Naturwissenschaften 97:19–28PubMedCrossRefGoogle Scholar
  102. von Schantz T, Bensch S, Grahna M, Hasselquist D, Wittzell H (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proc R Soc Lond B 266:1–12CrossRefGoogle Scholar
  103. Watson H, Lee DL, Hudson PJ (1987) The effect of Trichostrongylus tenuis on the caecal mucosa of young, old and anthelmintic-treated wild red grouse, Lagopus lagopus scoticus. Parasitology 94:405–411PubMedCrossRefGoogle Scholar
  104. Webster LMI, Mello LV, Mougeot F, Martínez-Padilla J, Paterson S, Piertney SB (2011a) Identification of genes responding to nematode infection in red grouse. Mol Ecol Res 11:305–313CrossRefGoogle Scholar
  105. Webster LMI, Paterson S, Mougeot F, Martínez-Padilla J, Piertney SB (2011b) Transcriptomic response of red grouse to gastro-intestinal nematode parasites and testosterone: implications for population dynamics. Mol Ecol 20:920–931PubMedCrossRefGoogle Scholar
  106. Wilson GR (1983) The prevalence of caecal threadworms (Trichostrongylus tenuis) in red grouse (Lagopus lagopus scoticus). Oecologia 58:265–268CrossRefGoogle Scholar
  107. Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Marius A. Wenzel
    • 1
    Email author
  • Lucy M. I. Webster
    • 1
    • 2
  • Steve Paterson
    • 3
  • François Mougeot
    • 4
    • 5
  • Jesús Martínez-Padilla
    • 6
  • Stuart B. Piertney
    • 1
  1. 1.Institute of Biological and Environmental SciencesUniversity of AberdeenAberdeenUK
  2. 2.Science and Advice for Scottish AgricultureEdinburghUK
  3. 3.Institute of Integrative BiologyUniversity of LiverpoolLiverpoolUK
  4. 4.Estación Experimental de Zonas Áridas (CSIC)AlmeríaSpain
  5. 5.Instituto de Investigaciones en Recursos Cinegéticos (IREC-CSIC)Ciudad RealSpain
  6. 6.Department of Evolutionary EcologyNational Museum of Natural History (MNCN-CSIC)MadridSpain

Personalised recommendations