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Chapter Ten - Parasite-mediated selection in red grouse – consequences for population dynamics and mate choice

from Part II - Understanding between-host processes

Published online by Cambridge University Press:  28 October 2019

Kenneth Wilson
Lancaster University
Andy Fenton
University of Liverpool
Dan Tompkins
Predator Free 2050 Ltd
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Parasites inflict many costs on their hosts. Understanding host–parasite relationship eco-evolutionary dynamics needs appreciation of how parasites affect individual fitness, survival and reproductive potential, and how they combine to influence population demography, dynamics and viability; also, how these processes drive microevolutionary processes that define natural and sexual selection. We synthesise work on the relationship between the red grouse and its main parasite, a gastrointestinal nematode. At individual level, we show how parasites impose a physiological cost, measured by immunosuppression and increased oxidative stress, and how their impact varies depending on contexts. We describe how parasite infection constrains expression of sexually selected traits and summarise how relationships between parasite, host and environment shape host population demography and dynamics. Genetic analyses in red grouse suggest nematode burden is moderately heritable, underpinned by a potentially large array of genes involved in the immune system, energy balance and broader homeostatic processes. There is no clear association between allele frequencies among populations and differences in nematode burdens. Possibly, beneficial alleles for parasite resistance cannot spread through the population due to the strong diversifying e?ects of gene ?ow and genetic drift.

Wildlife Disease Ecology
Linking Theory to Data and Application
, pp. 296 - 320
Publisher: Cambridge University Press
Print publication year: 2019

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Allen, P.C. (1987) Physiological response of chicken gut tissue to coccidial infection: comparative effects of Eimeria acervulina and Eimeria mitis on mucosal mass, carotenoid content, and brush border enzyme activity. Poultry Science, 66, 13061315.CrossRefGoogle Scholar
Allen, P.C. (1997) Production of free radical species during Eimeria maxima infections in chickens. Poultry Science, 76, 814821.CrossRefGoogle ScholarPubMed
Alonso-Alvarez, C., Bertrand, S., Faivre, B., Chastel, O. & Sorci, G. (2007) Testosterone and oxidative stress: the oxidation handicap hypothesis. Proceedings of the Royal Society of London B, 274, 819.CrossRefGoogle ScholarPubMed
Amundsen, T. (2000) Why are female birds ornamented? Trends in Ecology & Evolution, 15, 149155.CrossRefGoogle ScholarPubMed
Amundsen, T.P.H. & Pärn, H. (2006) Female coloration: review of functional and non functional hypotheses. In Hill, G.E. & McGraw, K.J. (eds.), Bird Coloration. Volume 2. Function and Evolution (pp. 280345). Cambridge, MA: Harvard University Press.Google Scholar
Andersson, M. (1994) Sexual Selection. Princeton, NJ: Princeton University Press.Google Scholar
Andersson, M. & Simmons, L.W. (2006) Sexual selection and mate choice. Trends in Ecology & Evolution, 21, 296302.CrossRefGoogle ScholarPubMed
Biron, D.G. & Loxdale, H.D. (2012) Host–parasite molecular cross-talk during the manipulative process of a host by its parasite. The Journal of Experimental Biology, 216, 148.CrossRefGoogle Scholar
Bortolotti, G.R., Marchant, T., Blas, J. & Cabezas, S. (2009a) Tracking stress: localisation, deposition and stability of corticosterone in feathers. Journal of Experimental Biology, 212, 14771482.CrossRefGoogle ScholarPubMed
Bortolotti, G.R., Mougeot, F., Martínez-Padilla, J., Webster, L.M.I. & Piertney, S.B. (2009b) Physiological stress mediates the honesty of social signals. PLoS ONE, 4, e4983.CrossRefGoogle ScholarPubMed
Chenoweth, S.F., Doughty, P. & Kokko, H. (2006) Can non-directional male mating preferences facilitate honest female ornamentation? Ecology Letters, 9, 179184.CrossRefGoogle ScholarPubMed
Cobbold, T.S. (1873) Contributions to our knowledge of grouse disease, including the description of a new species of entozoon, with remarks on a case of rot in the hare. Veterinarian, 46, 163172.Google Scholar
Cornwallis, C.K. & Uller, T. (2009) Towards an evolutionary ecology of sexual traits. Trends in Ecology & Evolution, 25, 145152.CrossRefGoogle ScholarPubMed
Costantini, D. (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecology Letters, 11, 12381251.CrossRefGoogle ScholarPubMed
Cotton, S., Fowler, K. & Pomiankowski, A. (2004) Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proceedings of the Royal Society of London B, 271, 771783.CrossRefGoogle ScholarPubMed
Darwin, C.R. (1871) Descent of Man, and Selection in Relation to Sex. London: John Murray.Google Scholar
Ferrari, N., Cattadori, I.M., Nespereira, J., Rizzoli, A. & Hudson, P.J. (2004) The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecology Letters, 7, 8894.CrossRefGoogle Scholar
Fisher, R.A. (1930) The Genetical Theory of Natural Selection. Oxford: Clarendon Press.CrossRefGoogle Scholar
Folstad, I. & Karter, A.J. (1992) Parasites, bright males, and the immunocompetence handicap. The American Naturalist, 139, 603622.CrossRefGoogle Scholar
Gómez, P., Ashby, B. & Buckling, A. (2015) Population mixing promotes arms race host–parasite coevolution. Proceedings of the Royal Society of London B, 282, 20142297.CrossRefGoogle ScholarPubMed
Goodwin, T.W. (1984) The Biochemistry of Carotenoids. London: Springer.CrossRefGoogle Scholar
Grafen, A. (1990) Biological signals as handicaps. Journal of Theoretical Biology, 144, 517546.CrossRefGoogle ScholarPubMed
Gustafsson, L., Nordling, D., Andersson, M.S., Sheldon, B.C. & Qvarnström, A. (1994) Infectious diseases, reproductive effort and the cost of reproduction in birds. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 346, 323331.Google ScholarPubMed
Haines, J.A. (2010) Female ornamentation in red grouse and its potential role in sexual selection. MPhil, University of Aberdeen.
Halliwell, B. & Gutteridge, J. (2007) Free Radicals in Biology and Medicine. New York, NY: Oxford University Press.Google Scholar
Hamilton, W.D. & Zuk, M. (1982) Heritable true fitness and bright birds: a role for parasites? Science, 218, 384387.CrossRefGoogle Scholar
Haydon, D.T., Shaw, D.J., Cattadori, I.M., Hudson, P.J. & Thirgood, S.J. (2002) Analysing noisy time-series: describing regional variation in the cyclic dynamics of red grouse. Proceedings of the Royal Society of London B, 269, 16091617.CrossRefGoogle ScholarPubMed
Hill, G.E. (2011) Condition-dependent traits as signals of the functionality of vital cellular processes. Ecology Letters, 14, 625634.CrossRefGoogle ScholarPubMed
Horak, P., Saks, L., Zilmer, M., Karu, U. & Zilmer, K. (2007) Do dietary antioxidants alleviate the cost of immune activation? An experiment with greenfinches. The American Naturalist, 170, 625635.CrossRefGoogle ScholarPubMed
Hudson, P.J. (1986a) The effect of a parasitic nematode on the breeding production of red grouse. Journal of Animal Ecology, 55, 85–92.CrossRefGoogle Scholar
Hudson, P.J. (1986b) The Red Grouse: The Biology and Management of a Wild Gamebird. Fordingbridge: The Game Conservancy Trust.Google Scholar
Hudson, P.J., Dobson, A.P., Cattadori, I.M., et al. (2002) Trophic interactions and population growth rates: describing patterns and identifying mechanisms. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 357, 12591271.CrossRefGoogle ScholarPubMed
Hudson, P.J., Dobson, A.P. & Newborn, D. (1998) Prevention of population cycles by parasite removal. Science, 282, 14.CrossRefGoogle ScholarPubMed
Hudson, P.J., Newborn, D. & Dobson, A.P. (1992) Regulation and stability of a free-living host–parasite system: Trichostrongylus tenuis in red grouse. I. Monitoring and parasite reduction experiments. Journal of Animal Ecology, 61, 477486.CrossRefGoogle Scholar
Husak, J.F. & Moore, I.T. (2008) Stress hormones and mate choice. Trends in Ecology & Evolution, 23, 532534.CrossRefGoogle ScholarPubMed
Jenkins, D., Watson, A. & Miller, G.R. (1963) Population studies on red grouse, Lagopus lagopus scoticus (Lath.) in north-east Scotland. Journal of Animal Ecology, 32, 317376.CrossRefGoogle Scholar
Kodric-Brown, A. & Brown, J.H. (1984) Truth in advertising: the kinds of traits favored by sexual selection. The American Naturalist, 124, 305322.CrossRefGoogle Scholar
Kotiaho, J.S. & Puurtinen, M. (2007) Mate choice for indirect genetic benefits: scrutiny of the current paradigm. Functional Ecology, 21, 638644.CrossRefGoogle Scholar
Kraaijeveld, K., Kraaijeveld-Smit, F.J.L. & Komdeur, J. (2007) The evolution of mutual ornamentation. Animal Behaviour, 74, 657677.CrossRefGoogle Scholar
Lambin, X., Krebs, C.J., Moss, R., Stenseth, N.C. & Yoccoz, N.G. (1999) Population cycles and parasitism. Science, 286, 24252425.CrossRefGoogle Scholar
Lande, R. (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution, 34, 292305.CrossRefGoogle ScholarPubMed
Larbi, A., Kempf, J. & Pawelec, G. (2007) Oxidative stress modulation and T cell activation. Experimental Gerontology, 42, 852858.CrossRefGoogle ScholarPubMed
Lenz, T.L., Eizaguirre, C., Rotter, B., Kalbe, M. & Milinski, M. (2013) Exploring local immunological adaptation of two stickleback ecotypes by experimental infection and transcriptome-wide digital gene expression analysis. Molecular Ecology, 22, 774786.CrossRefGoogle ScholarPubMed
Lochmiller, R.L. (1996) Immunocompetence and animal population regulation. Oikos, 76, 594602.CrossRefGoogle Scholar
Lochmiller, R.L. & Deerenberg, C. (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos, 88, 8798.CrossRefGoogle Scholar
Lovat, L. (1911) The Grouse in Health and in Disease. London: Smith & Elder.Google Scholar
Martínez-de la Puente, J., Merino, S., Tomás, G., et al. (2010) The blood parasite Haemoproteus reduces survival in a wild bird: a medication experiment. Biology Letters, 6, 663665.Google Scholar
Martínez-Padilla, J., Mougeot, F., Perez-Rodriguez, L. & Bortolotti, G.R. (2007) Nematode parasites reduce carotenoid-based signalling in male red grouse. Biology Letters, 3, 161164.CrossRefGoogle ScholarPubMed
Martínez-Padilla, J., Mougeot, F., Webster, L.M.I., Perez-Rodriguez, L. & Piertney, S.B.B. (2010) Testing the interactive effects of testosterone and parasites on carotenoid-based ornamentation in a wild bird. Journal of Evolutionary Biology, 23, 902913.CrossRefGoogle Scholar
Martínez-Padilla, J., Pérez-Rodríguez, L., Mougeot, F., Ludwig, S. & Redpath, S.M. (2014a) Intra-sexual competition alters the relationship between testosterone and ornament expression in a wild territorial bird. Hormones and Behavior, 65, 435444.CrossRefGoogle Scholar
Martínez-Padilla, J., Pérez-Rodríguez, L., Mougeot, F., Ludwig, S.C. & Redpath, S.M. (2014b) Experimentally elevated levels of testosterone at independence reduce fitness in a territorial bird. Ecology, 95, 10331044.CrossRefGoogle Scholar
Martínez-Padilla, J., Redpath, S.M., Zeineddine, M. & Mougeot, F. (2014c) Insights into population ecology from long-term studies of red grouse Lagopus lagopus scoticus. Journal of Animal Ecology, 83, 8598.CrossRefGoogle ScholarPubMed
Martínez-Padilla, J., Vergara, P., Mougeot, F. & Redpath, S.M. (2012) Parasitized mates increase infection risk for partners. The American Naturalist, 179, 811820.CrossRefGoogle ScholarPubMed
Martínez-Padilla, J., Vergara, P., Perez-Rodriguez, L., et al. (2011) Condition- and parasite-dependent expression of a male-like trait in a female bird. Biology Letters, 7, 364367.CrossRefGoogle Scholar
McGraw, K.J. (2006) Mechanics of carotenoid-based coloration. In: Hill, G.E. & McGraw, K.J. (eds.),Bird Coloration (pp. 177242). Cambridge, MA: Harvard University Press.Google ScholarPubMed
Moss, R. & Watson, A. (2001) Population cycles in birds of the Grouse family (Tetranoidae). Advances in Ecological Research, 32, 53111.CrossRefGoogle Scholar
Moss, R. Watson, A. & Parr, R. (1996) Experimental prevention of a population cycle in Red grouse. Ecology, 77, 15121530.CrossRefGoogle Scholar
Moss, R., Watson, A., Trenholm, I.B. & Parr, R. (1993) Cecal threadworms Trichostrongylus tenuis in red grouse Lagopus lagopus scoticus – effects of weather and host density upon estimated worm burdens. Parasitology, 107, 199209.CrossRefGoogle Scholar
Mougeot, F., Dawson, A., Redpath, S.M. & Leckie, F. (2005b) Testosterone and autumn territorial behavior in male red grouse Lagopus lagopus scoticus. Hormones and Behavior, 47, 576584.CrossRefGoogle ScholarPubMed
Mougeot, F., Evans, S.A. & Redpath, S.M. (2005a) Interactions between population processes in a cyclic species: parasites reduce autumn territorial behaviour of male red grouse. Oecologia, 144, 289298.CrossRefGoogle Scholar
Mougeot, F., Irvine, J.R., Seivwright, L., Redpath, S.M. & Piertney, S. (2004) Honest sexual signaling in male red grouse. Behavioral Ecology, 15, 930937.CrossRefGoogle Scholar
Mougeot, F., Martínez-Padilla, J., Blount, J.D., et al. (2010) Oxidative stress and the effect of parasites on a carotenoid-based ornament. Journal of Experimental Biology, 213, 400407.CrossRefGoogle ScholarPubMed
Mougeot, F., Martínez-Padilla, J., Perez-Rodriguez, L. & Bortolotti, G.R. (2007a) Carotenoid-based colouration and ultraviolet reflectance of the sexual ornaments of grouse. Behavioral Ecology and Sociobiology, 61, 741751.CrossRefGoogle Scholar
Mougeot, F., Martínez-Padilla, J., Webster, L.M.I., et al. (2009) Honest sexual signalling mediated by parasite and testosterone effects on oxidative balance. Proceedings of the Royal Society of London B, 276, 10931100.CrossRefGoogle ScholarPubMed
Mougeot, F., Perez-Rodriguez, L., Martínez-Padilla, J., Leckie, F. & Redpath, S.M. (2007b) Parasites, testosterone and honest carotenoid-based signalling of health. Functional Ecology, 21, 886898.CrossRefGoogle Scholar
Mougeot, F., Piertney, S.B.B., Leckie, F., et al. (2005c) Experimentally increased aggressiveness reduces population kin structure and subsequent recruitment in red grouse Lagopus lagopus scoticus. Journal of Animal Ecology, 74, 488497.CrossRefGoogle Scholar
Mougeot, F. & Redpath, S.M. (2004) Sexual ornamentation relates to immune function in male red grouse Lagopus lagopus scoticus. Journal of Avian Biology, 35, 425433.CrossRefGoogle Scholar
Mougeot, F., Redpath, S.M., Leckie, F. & Hudson, P.J. (2003a) The effect of aggressiveness on the population dynamics of a territorial bird. Nature, 421, 737739.CrossRefGoogle ScholarPubMed
Mougeot, F., Redpath, S.M., Moss, R., et al. (2003b) Territorial behaviour and population dynamics in red grouse Lagopus lagopus scoticus. I. Population experiments. Journal of Animal Ecology, 72, 10731082.CrossRefGoogle Scholar
Mougeot, F., Redpath, S.M. & Piertney, S.B. (2006) Elevated spring testosterone increases parasite intensity in male red grouse. Behavioral Ecology, 17, 117125.CrossRefGoogle Scholar
Mougeot, F., Redpath, S.M., Piertney, S.B. & Hudson, P.J. (2005d) Separating behavioral and physiological mechanisms in testosterone-mediated trade-offs. The American Naturalist, 166, 158168.CrossRefGoogle ScholarPubMed
Mougeot, F.L., Ádám, Z., Martínez-Padilla, J., et al. (2016) Parasites, mate attractiveness and female feather corticosterone levels in a socially monogamous bird. Behavioral Ecology and Sociobiology, 70, 277283.CrossRefGoogle Scholar
Newborn, D. & Foster, R. (2002) Control of parasite burdens in wild red grouse Lagopus lagopus scoticus through the indirect application of anthelmintics. Journal of Applied Ecology, 39, 909914.CrossRefGoogle Scholar
Owen-Ashley, N.T., Hasselquist, D. & Wingfield, J.C. (2004) Androgens and the immunocompetence handicap hypothesis: Unraveling direct and indirect pathways of immunosuppression in song sparrows. The American Naturalist, 164, 490505.CrossRefGoogle ScholarPubMed
Paterson, S. & Piertney, S.B. (2011) Frontiers in host–parasite ecology and evolution. Molecular Ecology, 20, 869871.CrossRefGoogle ScholarPubMed
Pérez-Rodríguez, L. (2009) Carotenoids in evolutionary ecology: re-evaluating the antioxidant role. BioEssays, 31, 11161126.CrossRefGoogle ScholarPubMed
Pérez-Rodríguez, L., de Blas, E.G., Martínez-Padilla, J., Mougeot, F. & Mateo, R. (2016) Carotenoid profile and vitamins in the combs of the red grouse (Lagopus lagopus scoticus): implications for the honesty of a sexual signal. Journal of Ornithology, 157, 145153.CrossRefGoogle Scholar
Piertney, S.B.B., Lambin, X., MacColl, A.D.C., et al. (2008) Temporal changes in kin structure through a population cycle in a territorial bird, the red grouse Lagopus lagopus scoticus. Molecular Ecology, 17, 25442551.CrossRefGoogle Scholar
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, 230242.CrossRefGoogle Scholar
Potts, G.R., Tapper, S.C. & Hudson, P.J. (1984) Population fluctuations in Red grouse – analysis of bag records and a simulation-model. Journal of Animal Ecology, 53, 2136.CrossRefGoogle Scholar
Poulin, R. & Thomas, F. (2008) Epigenetic effects of infection on the phenotype of host offspring: parasites reaching across host generations. Oikos, 117, 331335.CrossRefGoogle Scholar
Prudic, K.L., Jeon, C., Cao, H. & Monteiro, A. (2011) Developmental plasticity in sexual roles of butterfly species drives mutual sexual ornamentation. Science, 331, 7375.CrossRefGoogle ScholarPubMed
Quigley, B.J.Z., García López, D., Buckling, A., McKane, A.J. & Brown, S.P. (2012) The mode of host–parasite interaction shapes coevolutionary dynamics and the fate of host cooperation. Proceedings of the Royal Society of London B, 279, 3742.CrossRefGoogle ScholarPubMed
Redpath, S.M., Mougeot, F., Leckie, F. & Evans, A.D. (2006a) The effects of autumn testosterone on survival and productivity in red grouse Lagopus lagopus scoticus. Animal Behaviour, 71, 12971305.CrossRefGoogle Scholar
Redpath, S.M., Mougeot, F., Leckie, F.M., Elston, D.A. & Hudson, P.J. (2006b) Testing the role of parasites in driving the cyclic population dynamics of a gamebird. Ecology Letters, 9, 410418.CrossRefGoogle ScholarPubMed
Richardson, W.S., Spivak, H., Hudson, J.E., Budacz, M.A. & Hunter, J.G. (1997) Teflon buttress inhibits recanalization of the ‘uncut’ Roux limb. Gastroenterology, 112, A1468A1468.Google Scholar
Roberts, M.L., Buchanan, K.L. & Evans, M.R. (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Animal Behaviour, 68, 227239.CrossRefGoogle Scholar
Romero, F.J., Bosch-Morell, F., Romero, M.J., et al. (1998) Lipid peroxidation products and antioxidants in human disease. Environmental Health Perspectives, 106, 12291234.Google ScholarPubMed
Romero, L.M. (2004) Physiological stress in ecology: lessons from biomedical research. Trends in Ecology & Evolution, 19, 249255.CrossRefGoogle ScholarPubMed
Saino, N., Møller, 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, 397404.CrossRefGoogle Scholar
Schmid-Hempel, P. (2011) Evolutionary Parasitology: The Integrated Study of Infections, Immunology, Ecology, and Genetics. Oxford: Oxford University Press.Google Scholar
Schmid-Hempel, P.E. & Ebert, D. (2003) On the evolutionary ecology of specific immune defence. Trends in Ecology & Evolution, 18, 2732.CrossRefGoogle Scholar
Seivwright, L., Redpath, S.M., Mougeot, F., Watts, L. & Hudson, P.J. (2004) Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus. Journal of Helminthology, 78, 6976.CrossRefGoogle ScholarPubMed
Seivwright, L.J., Redpath, S.M., 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. Proceedings of the Royal Society of London B, 272, 22992304.CrossRefGoogle Scholar
Shaw, J.L. (1988) Arrested development of Trichostrongylus tenuis as 3rd stage larvae in red grouse. Research in Veterinary Science, 45, 256258.CrossRefGoogle Scholar
Shaw, J.L. & Moss, R. (1989) The role of parasite fecundity and longevity in the success of Trichostrongylus tenuis in low-density red grouse populations. Parasitology, 99, 253258.CrossRefGoogle ScholarPubMed
Shaw, J.L., Moss, R. & Pike, A.W. (1989) Development and survival of the free-living stages of Trichostrongylus tenuis, a cecal parasite of red grouse Lagopus lagopus scoticus. Parasitology, 99, 105113.CrossRefGoogle Scholar
Sheldon, B.C. & Verhulst, S. (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology & Evolution, 11, 317321.CrossRefGoogle ScholarPubMed
Splettstoesser, W.D. & Schuff-Werner, P. (2002) Oxidative stress in phagocytes – ‘the enemy within’. Microscopy Research and Technique, 57, 441455.CrossRefGoogle Scholar
Stear, M.J., Fitton, L., Innocent, G.T., et al. (2007) The dynamic influence of genetic variation on the susceptibility of sheep to gastrointestinal nematode infection. Journal of the Royal Society Interface, 4, 767.Google ScholarPubMed
Tarjuelo, R., Vergara, P. & Martínez-Padilla, J. (2016) Intra-sexual competition modulates calling behavior and its association with secondary sexual traits. Behavioral Ecology and Sociobiology, 70, 16331641.CrossRefGoogle Scholar
Thirgood, S.J., Redpath, S.M., Haydon, D.T., et al. (2000) Habitat loss and raptor predation: disentangling long- and short-term causes of red grouse declines. Proceedings of the Royal Society of London B, 267, 651656.CrossRefGoogle ScholarPubMed
Thrall, P.H., Antonovics, J. & Bever, J.D. (1997) Sexual transmission of disease and host mating systems: within-season reproductive success. The American Naturalist, 149, 485506.CrossRefGoogle Scholar
Turchin, P. (2003) Complex Population Dynamics: A Theoretical/Empirical Synthesis. Princeton, NJ: Princeton University Press.Google Scholar
Vergara, P. & Martínez-Padilla, J. (2012) Social context decouples the relationship between a sexual ornament and testosterone levels in a male wild bird. Hormones and Behavior, 62, 407412.CrossRefGoogle Scholar
Vergara, P., Martínez-Padilla, J., Mougeot, F., Leckie, F. & Redpath, S.M. (2012a) Environmental heterogeneity influences the reliability of secondary sexual traits as condition indicators. Journal of Evolutionary Biology, 25, 2028.CrossRefGoogle ScholarPubMed
Vergara, P., Martínez-Padilla, J., Redpath, S.M. & Mougeot, F. (2011) The ornament–condition relationship varies with parasite abundance at population level in a female bird. Naturwissenschaften, 98, 897902.CrossRefGoogle Scholar
Vergara, P., Mougeot, F., Martínez-Padilla, J., Leckie, F. & Redpath, S.M. (2012b) The condition dependence of a secondary sexual trait is stronger under high parasite infection level. Behavioral Ecology, 23, 502511.CrossRefGoogle Scholar
Vergara, P., Redpath, S.M., Martínez‐Padilla, J. & Mougeot, F. (2012c) Environmental conditions influence red grouse ornamentation at a population level. Biological Journal of the Linnean Society, 107, 788798.CrossRefGoogle Scholar
von Schantz, T., Bensch, S., Grahn, M., Hasselquist, D. & Wittzell, H. (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proceedings of the Royal Society of London B, 266, 112.CrossRefGoogle ScholarPubMed
Watson, A. (1985) Social class, socially-induced loss, recruitment and breeding of red grouse. Oecologia, 67, 493498.CrossRefGoogle ScholarPubMed
Watson, A. & Moss, R. (1988) Spacing behaviour and population limitation in red grouse. The Auk, 105, 207208.CrossRefGoogle Scholar
Watson, A. & Moss, R. (2008) Grouse. London: Collins.Google Scholar
Watson, A., Moss, R. & Rae, S. (1998) Population dynamics of Scottish rock ptarmigan cycles. Ecology, 79, 11741192.CrossRefGoogle Scholar
Watson, M.J. (2013) What drives population-level effects of parasites? Meta-analysis meets life-history. International Journal for Parasitology: Parasites and Wildlife, 2, 190196.Google ScholarPubMed
Webster, L.M.I., Mello, L.V., Mougeot, F., et al. (2011) Identification of genes responding to nematode infection in red grouse. Molecular Ecology Resources, 11, 305313.CrossRefGoogle ScholarPubMed
Webster, L.M.I.P., Paterson, S., Mougeot, F., Martínez-Padilla, J. & Piertney, S.B.B. (2011) Transcriptomic response of red grouse to gastro-intestinal nematode parasites and testosterone: implications for population dynamics. Molecular Ecology, 20, 920931.CrossRefGoogle ScholarPubMed
Wenzel, M.A., Douglas, A., James, M.C., Redpath, S.M. & Piertney, S.B.B. (2016) The role of parasite-driven selection in shaping landscape genomic structure in red grouse (Lagopus lagopus scotica). Molecular Ecology, 25, 324341.CrossRefGoogle Scholar
Wenzel, M.A., James, M.C., Douglas, A. & Piertney, S.B. (2015a) Genome-wide association and genome partitioning reveal novel genomic regions underlying variation in gastrointestinal nematode burden in a wild bird. Molecular Ecology, 24, 41754192.CrossRefGoogle Scholar
Wenzel, M.A. & Piertney, S.B. (2014) Fine-scale population epigenetic structure in relation to gastro-intestinal parasite load in red grouse (Lagopus lagopus scotica). Molecular Ecology, 23, 42564273.CrossRefGoogle Scholar
Wenzel, M.A. & Piertney, S.B.B. (2015) Digging for gold nuggets: uncovering novel candidate genes for variation in gastrointestinal nematode burden in a wild bird species. Journal of Evolutionary Biology, 28, 807825.CrossRefGoogle Scholar
Wenzel, M.A., Webster, L.M.I., Paterson, S., et al. (2013) A transcriptomic investigation of handicap models in sexual selection. Behavioral Ecology and Sociobiology, 67, 221234.Google Scholar
Wenzel, M.A., Webster, L.M.I., Paterson, S. & Piertney, S.B. (2015b) Identification and characterisation of 17 polymorphic candidate genes for response to parasitic nematode (Trichostrongylus tenuis) infection in red grouse (Lagopus lagopus scotica). Conservation Genetics Resources, 7, 2328.CrossRefGoogle Scholar
Wilfert, L. & Schmid-Hempel, P. (2008) The genetic architecture of susceptibility to parasites. BMC Evolutionary Biology, 8, 187.CrossRefGoogle ScholarPubMed
Wilson, G.R. & Wilson, L.P. (1978) Haematology weight and condition of red grouse (Lagopus lagopus scoticus) infected with caecal threadworms (Trichostrongylus tenuis). Research in Veterinary Science, 25, 331336.CrossRefGoogle Scholar
Wongrak, K., Daş, G., von Borstel, U.K. & Gauly, M. (2015) Genetic variation for worm burdens in laying hens naturally infected with gastro-intestinal nematodes. British Poultry Science, 56, 1521.CrossRefGoogle Scholar
Zahavi, A. (1975) Mate selection – a selection for a handicap. Journal of Theoretical Biology, 53, 205214.CrossRefGoogle ScholarPubMed
Zuk, M. & Stochr, A. (2002) Immune defense and host life history. The American Naturalist, 160, S9S22.CrossRefGoogle ScholarPubMed

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Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats

Send book to Dropbox

To send content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about sending content to Dropbox.

Available formats

Send book to Google Drive

To send content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about sending content to Google Drive.

Available formats