, 98:897 | Cite as

The ornament–condition relationship varies with parasite abundance at population level in a female bird

  • Pablo Vergara
  • Jesús Martínez-Padilla
  • Stephen M. Redpath
  • Francois Mougeot
Short Communication


Environmental heterogeneity is expected to create variation in the ornament–condition relationship. This topic has been studied in males with less attention being given to females. Here, we explore inter-population variation in the relationship between the size of a male-like trait, supra-orbital combs, and body mass in female red grouse Lagopus lagopus scoticus. We used the abundance of the nematode Trichostrongylus tenuis, a parasite with strong negative effects on this species, as a proxy of environmental conditions. We studied six populations over 5 years and showed that the comb size–body mass relationship varied with mean parasite abundance, with stronger ornament–condition relationships in populations with higher parasite infection levels. Our study supports the idea that environmental conditions, and in particular parasite infection levels, may affect the reliability of female ornaments as condition indicators.


Environmental conditions Lagopus lagopus scoticus Secondary sexual traits Sexual selection Trichostrongylus tenuis 



We are grateful to the people that helped in the field, and to owners and gamekeepers, British Army, RSPB, and English Natural Heritage for allowing us to work on their moors. A. Roulin and an anonymous reviewer provided valuable comments. PV and FM were supported by a Marie Curie Intra-European Fellowship (PIEF-GA-2009-252499) and a NERC advanced fellowship, respectively. This study was funded by Natural Environment Research Council grants (NER/A/S/1999/00074, NE/D000602/1 and NE/D014352/1). We held the necessary licenses for conducting these procedures (PPL80/1437 and PPL60/3824).


  1. Bart J, Earnst SL (1999) Relative importance of male and territory quality in pairing success of male rock ptarmigan (Lagopus mutus). Behav Ecol Sociobiol 45:355–359CrossRefGoogle Scholar
  2. Candolin U (2000) Changes in expression and honestly of sexual signaling over the reproductive lifetime of sticklebacks. Proc R Soc Lond B 267:2425–2430CrossRefGoogle Scholar
  3. Chenoweth SF, Doughty P, Kokko H (2006) Can non-directional male mating preferences facilitate honest female ornamentation? Ecol Lett 9:179–184PubMedCrossRefGoogle Scholar
  4. Cornwallis CK, Uller T (2009) Towards an evolutionary ecology of sexual traits. Trend Ecol Evol 25:145–152CrossRefGoogle Scholar
  5. Cothran RD, Jeyasingh PD (2010) Condition dependence of a sexually selected trait in a crustacean species complex: importance of the ecological context. Evolution 64:2535–2546PubMedCrossRefGoogle Scholar
  6. Cotton S, Fowler K, Pomiankowski A (2004a) Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc R Soc Lond B 271:771–783CrossRefGoogle Scholar
  7. Cotton S, Fowler K, Pomiankowski A (2004b) Condition dependence of sexual ornament size and variation in the stalk-eyed fly Cyrtodiopsis damanni (Diptera: Diopsidae). Evolution 58:1038–1046PubMedGoogle Scholar
  8. Delahay RT, Moss R (1996) Food intake, weight changes and egg production in captive red grouse before and during laying: effects of the parasitic nematode Trichostrongylus tenuis. Condor 98:501–511CrossRefGoogle Scholar
  9. Delahay RT, 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. Parasitol 110:473–482CrossRefGoogle Scholar
  10. Doutrelant C, Gregoire A, Grnac N, Gomez D, Lambrechts MM, Perret P (2008) Female coloration indicates female reproductive capacity in blue tits. J Evol Biol 21:226–233PubMedGoogle Scholar
  11. Fargallo JA, Martínez-Padilla J, Toledano-Díaz A, Santiago-Moreno J, Davila JA (2007) Sex and testosterone effects on growth, immunity and melanin coloration of nestling Eurasian kestrels. J Anim Ecol 76:201–209PubMedCrossRefGoogle Scholar
  12. Haines JA (2010) Female ornamentation in red grouse and its potential role in sexual selection. MPhil dissertation, University of AberdeenGoogle Scholar
  13. Hegyi G, Rosivalli B, Szöllosi E, Hargitai R, Eens M, Török J (2008) Phenotypic plasticity in a conspicuous female plumage trait: information content and mating patterns. Anim Behav 75:977–989CrossRefGoogle Scholar
  14. Hoffmann AA, Merilä J (1999) Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol Evol 14:96–101PubMedCrossRefGoogle Scholar
  15. Holder K, Montgomerie R (1993) Context and consequences of comb displays by male rock ptarmigan. Anim Behav 45:457–470CrossRefGoogle Scholar
  16. Hudson PJ, Newborn D, Dobson AP (1992) Regulation and stability of a free-living host–parasite system—Trichostrongylus tenuis in red grouse. I. Monitoring and parasite reduction experiments. J Anim Ecol 61:477–486CrossRefGoogle Scholar
  17. Ingleby FC, Hunt J, Hosken DJ (2010) The role of genotype-by-environment interactions in sexual selection. J Evol Biol 23:2031–2045PubMedCrossRefGoogle Scholar
  18. MacColl ADC, Piertney SB, Moss R, Lambin X (2000) Spatial arrangement of kin affects recruitment success in young male red grouse. Oikos 90:261–270Google Scholar
  19. 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
  20. Martínez-Padilla J, Vergara P, Pérez-Rodríguez L, Mougeot F, Casas F, Ludwig SC, Haines JA, Zeineddine M, Redpath SM (2011) Condition- and parasite-dependent expression of a male-like trait in a female bird. Biol Lett 7:364–367PubMedCrossRefGoogle Scholar
  21. Morales J, Velando A, Torres R (2009) Fecundity compromises attractiveness when pigments are scarce. Behav Ecol 20:117–123CrossRefGoogle Scholar
  22. Moss R, Kolb HH, Marquiss M, Watson A, Treca B, Watt D, Glennie W (1979) Aggressiveness and dominance in captive cock red grouse. Aggress Behav 5:58–84CrossRefGoogle Scholar
  23. Moss R, Watson A, Trenholm IB, Parr R (1993) Caecal threadworms Trichostrongylus tenuis in red grouse Lagopus lagopus scoticus: effects of weather and host density upon estimated worms burdens. Parasitology 107:199–209PubMedCrossRefGoogle Scholar
  24. Moss R, Watson A, Parr R (1996) Experimental prevention of a population cycle in red grouse. Ecology 77:1512–1530CrossRefGoogle Scholar
  25. Mougeot F, Irvine JR, Seivwright L, Redpath SM, Piertney SB (2004) Testosterone, immunocompetence, and honest signalling in male red grouse. Behav Ecol 15:930–937CrossRefGoogle Scholar
  26. Mougeot F, Redpath SM, Leckie F (2005) Ultra-violet reflectance of male and female red grouse, Lagopus lagopus scoticus, sexual ornaments reflects nematode parasite intensity. J Avian Biol 36:203–209CrossRefGoogle Scholar
  27. Mougeot F, Redpath SM, Piertney SB (2006) Elevated spring testosterone increases parasite intensity in male red grouse. Behav Ecol 17:127–135Google Scholar
  28. Piault R, Gasparini J, Bize P, Jenni-Eiermann S, Roulin A (2009) Pheomelanin-based coloration and the ability to cope with variation in food supply and parasitism. Am Nat 174:548–556PubMedCrossRefGoogle Scholar
  29. Redpath S, Mougeot F, Leckie F, Evans S (2006a) The effects of autumn testosterone on survival and productivity in red grouse Lagopus lagopus scoticus. Anim Behav 71:1297–1305CrossRefGoogle Scholar
  30. Redpath SM, Mougeot F, Leckie F, Elston DA, Hudson PJ (2006b) Testing the role of parasites in driving the cyclic population dynamics of a gamebird. Ecol Lett 9:410–418PubMedCrossRefGoogle Scholar
  31. Robinson MR, Pilkington JG, Clutton-Brock TH, Pemberton JM, Kruuk LEB (2008) Environmental heterogeneity generates fluctuating selection on a secondary sexual trait. Current Biol 18:751–757CrossRefGoogle Scholar
  32. Roulin A (2009) Covariation between eumelanic pigmentation and body mass only under specific conditions. Naturwissenschaften 96:375–382PubMedCrossRefGoogle Scholar
  33. Roulin A, Gasparini J, Bize P, Ritschard M, Richner H (2008) Melanin-based colorations signal strategies to cope with poor and rich environments. Behav Ecol Sociobiol 62:507–519CrossRefGoogle Scholar
  34. Seivwright LJ (2004) Patterns of Trichostrongylus tenuis infection in individual red grouse (Lagopus lagopus scoticus). PhD thesis, University of StirlingGoogle Scholar
  35. Seivwright LJ, Redpath SM, Mougeot F, Watt L, Hudson PJ (2004) Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus. J Helminthol 78:69–76PubMedCrossRefGoogle Scholar
  36. Vergara P, Fargallo JA, Martínez-Padilla J, Lemus JA (2009) Inter-annual variation and information content of melanin-based colouration in female Eurasian kestrels. Biol J Linn Soc 97:781–790CrossRefGoogle Scholar
  37. Watson A, Jenkins D (1964) Notes on the behaviour of the red grouse. British Birds 57:137–170Google Scholar
  38. Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Pablo Vergara
    • 1
  • Jesús Martínez-Padilla
    • 1
    • 2
  • Stephen M. Redpath
    • 3
  • Francois Mougeot
    • 4
  1. 1.School of Biological SciencesUniversity of AberdeenAberdeenUK
  2. 2.Museo Nacional de Ciencias Naturales-CSICMadridSpain
  3. 3.Aberdeen Centre for Environmental Sustainability (ACES)University of Aberdeen & The Macaulay Institute, School of Biological SciencesAberdeenUK
  4. 4.Estación Experimental de Zonas Áridas (EEZA, CSIC)AlmeríaSpain

Personalised recommendations