Abstract
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.
References
Bart J, Earnst SL (1999) Relative importance of male and territory quality in pairing success of male rock ptarmigan (Lagopus mutus). Behav Ecol Sociobiol 45:355–359
Candolin U (2000) Changes in expression and honestly of sexual signaling over the reproductive lifetime of sticklebacks. Proc R Soc Lond B 267:2425–2430
Chenoweth SF, Doughty P, Kokko H (2006) Can non-directional male mating preferences facilitate honest female ornamentation? Ecol Lett 9:179–184
Cornwallis CK, Uller T (2009) Towards an evolutionary ecology of sexual traits. Trend Ecol Evol 25:145–152
Cothran RD, Jeyasingh PD (2010) Condition dependence of a sexually selected trait in a crustacean species complex: importance of the ecological context. Evolution 64:2535–2546
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 271:771–783
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 58:1038–1046
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 98:501–511
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 110:473–482
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 21:226–233
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 76:201–209
Haines JA (2010) Female ornamentation in red grouse and its potential role in sexual selection. MPhil dissertation, University of Aberdeen
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 75:977–989
Hoffmann AA, Merilä J (1999) Heritable variation and evolution under favourable and unfavourable conditions. Trends Ecol Evol 14:96–101
Holder K, Montgomerie R (1993) Context and consequences of comb displays by male rock ptarmigan. Anim Behav 45:457–470
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 61:477–486
Ingleby FC, Hunt J, Hosken DJ (2010) The role of genotype-by-environment interactions in sexual selection. J Evol Biol 23:2031–2045
MacColl ADC, Piertney SB, Moss R, Lambin X (2000) Spatial arrangement of kin affects recruitment success in young male red grouse. Oikos 90:261–270
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 23:902–913
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 7:364–367
Morales J, Velando A, Torres R (2009) Fecundity compromises attractiveness when pigments are scarce. Behav Ecol 20:117–123
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 5:58–84
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 107:199–209
Moss R, Watson A, Parr R (1996) Experimental prevention of a population cycle in red grouse. Ecology 77:1512–1530
Mougeot F, Irvine JR, Seivwright L, Redpath SM, Piertney SB (2004) Testosterone, immunocompetence, and honest signalling in male red grouse. Behav Ecol 15:930–937
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 36:203–209
Mougeot F, Redpath SM, Piertney SB (2006) Elevated spring testosterone increases parasite intensity in male red grouse. Behav Ecol 17:127–135
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 174:548–556
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 71:1297–1305
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 9:410–418
Robinson MR, Pilkington JG, Clutton-Brock TH, Pemberton JM, Kruuk LEB (2008) Environmental heterogeneity generates fluctuating selection on a secondary sexual trait. Current Biol 18:751–757
Roulin A (2009) Covariation between eumelanic pigmentation and body mass only under specific conditions. Naturwissenschaften 96:375–382
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 62:507–519
Seivwright LJ (2004) Patterns of Trichostrongylus tenuis infection in individual red grouse (Lagopus lagopus scoticus). PhD thesis, University of Stirling
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 78:69–76
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 97:781–790
Watson A, Jenkins D (1964) Notes on the behaviour of the red grouse. British Birds 57:137–170
Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214
Acknowledgments
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).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Alexandre Roulin
Rights and permissions
About this article
Cite this article
Vergara, P., Martínez-Padilla, J., Redpath, S.M. et al. The ornament–condition relationship varies with parasite abundance at population level in a female bird. Naturwissenschaften 98, 897 (2011). https://doi.org/10.1007/s00114-011-0833-9
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-011-0833-9