Skip to main content
SpringerLink
Log in

Effects of Common Origin and Common Rearing Environment on Variance in Ectoparasite Load and Phenotype of Nestling Alpine Swifts

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Knowledge of the quantitative genetics of resistance to parasitism is key to appraise host evolutionary responses to parasite selection. Here, we studied effects of common origin (i.e. genetic and pre-hatching parental effects) and common rearing environment (i.e. post-hatching parental effects and other environment effects) on variance in ectoparasite load in nestling Alpine swifts (Apus melba). This colonial bird is intensely parasitized by blood sucking louse-flies that impair nestling development and survival. By cross-fostering half of the hatchlings between pairs of nests, we show strong significant effect of common rearing environment on variance (90.7% in 2002 and 90.9% in 2003) in the number of louse-flies per nestling and no significant effect of common origin on variance in the number of louse-flies per nestling. In contrast, significant effects of common origin were found for all the nestling morphological traits (i.e. body mass, wing length, tail length, fork length and sternum length) under investigation. Hence, our study suggests that genetic and pre-hatching parental effects play little role in the distribution of parasites among nestling Alpine swifts, and thus that nestlings have only limited scope for evolutionary responses against parasites. Our results highlight the need to take into consideration environmental factors, including the evolution of post-hatching parental effects such as nest sanitation, in our understanding of host-parasite relationships.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Ardia, D. R., & Rice, E. B. (2006). Variation in heritability of immune function in the tree swallow. Evolutionary Ecology, 20, 491–500.

    Google Scholar 

  • Arn, H. (1960). Biologische Studien am Alpensegler. Solothurn, Switzerland: Verlag Vogt-Schild AG.

    Google Scholar 

  • Badyaev, A. V., Hamstra, T. L., Oh, K. P., & Acevedo Seaman, D. A. (2006). Sex-biased maternal effects reduce ectoparasite-induced mortality in a passerine bird. Proceeding of the National Academy of Sciences of the United States of America, 103, 14406–14411.

    Article  CAS  Google Scholar 

  • Bize, P., Jeanneret, C., Klopfenstein, A., & Roulin, A. (2008). What makes a host profitable? Experimental evidence that parasites balance host nutritive resources against immunity. American Naturalist, 171, 107–118. doi:10.1086/523943.

    Article  PubMed  Google Scholar 

  • Bize, P., Metcalfe, N. B., & Roulin, A. (2006). Catch up growth strategies differ between body structures: Interactions between age and structure-specific growth in wild nestling Alpine swifts. Functional Ecology, 20, 857–864. doi:10.1111/j.1365-2435.2006.01157.x.

    Article  Google Scholar 

  • Bize, P., Roulin, A., Bersier, L.-F., Pfluger, D., & Richner, H. (2003). Parasitism and developmental plasticity in Alpine swift nestlings. Journal of Animal Ecology, 72, 633–639. doi:10.1046/j.1365-2656.2003.00734.x.

    Article  Google Scholar 

  • Bize, P., Roulin, A., & Richner, H. (2004a). Parasitism, developmental plasticity and bilateral asymmetry of wing feathers in Alpine swift (Apus melba) nestlings. Oikos, 106, 317–323. doi:10.1111/j.0030-1299.2004.13019.x.

    Article  Google Scholar 

  • Bize, P., Roulin, A., Tella, J. L., Bersier, L.-F., & Richner, H. (2004b). Additive effects of ectoparasites over the reproductive attempts in the long-lived Alpine swifts. Journal of Animal Ecology, 73, 1080–1088. doi:10.1111/j.0021-8790.2004.00880.x.

    Article  Google Scholar 

  • Bize, P., Roulin, A., Tella, J. L., & Richner, H. (2005). Female-biased mortality in experimentally parasitized Alpine swift Apus melba nestlings. Functional Ecology, 19, 405–413. doi:10.1111/j.1365-2435.2005.00995.x.

    Article  Google Scholar 

  • Blanford, S., Thomas, M. B., Pugh, C., & Pell, J. K. (2003). Temperature checks the Red Queen? Resistance and virulence in a fluctuating environment. Ecology Letters, 6, 2–5. doi:10.1046/j.1461-0248.2003.00387.x.

    Article  Google Scholar 

  • Boulinier, T., & Staszewski, V. (2008). Maternal transfer of antibodies: Raising immuno-ecology issues. Trends in Ecology & Evolution, 23, 282–288. doi:10.1016/j.tree.2007.12.006.

    Article  Google Scholar 

  • Charmantier, A., & Garant, D. (2005). Environmental quality and evolutionary potential: Lessons from wild populations. Proceedings of the Royal Society of London. Series B: Biological Sciences, 272, 1415–1425. doi:10.1098/rspb.2005.3117.

    Article  PubMed  Google Scholar 

  • Christe, P., Møller, A. P., & de Lope, F. (1998). Immunocompetence and nestling survival in the house martin: The tasty chick hypothesis. Oikos, 83, 175–179. doi:10.2307/3546559.

    Article  CAS  Google Scholar 

  • Christe, P., Møller, A. P., Saino, N., & de Lope, F. (2000). Genetic and environmental components of phenotypic variation in immune response and body size of a colonial bird, Delichon urbica (the house martin). Heredity, 85, 75–83. doi:10.1046/j.1365-2540.2000.00732.x.

    Article  PubMed  Google Scholar 

  • Christe, P., Oppliger, A., Bancalà, F., Castella, G., & Chapuisat, M. (2003). Evidence for collective medication in ants. Ecology Letters, 6, 19–22. doi:10.1046/j.1461-0248.2003.00395.x.

    Article  Google Scholar 

  • Christe, P., Richner, H., & Oppliger, A. (1996). Of great tits and fleas: Sleep baby sleep. Animal Behaviour, 52, 1087–1092. doi:10.1006/anbe.1996.0256.

    Article  Google Scholar 

  • Clayton, D. H., Lee, P. L. M., Tompkins, D. M., Brodie, E. D., III. (1999). Reciprocal natural selection on host-parasite phenotypes. American Naturalist, 154, 261–270. doi:10.1086/303237.

    Article  PubMed  Google Scholar 

  • Clayton, D. H., & Moore, H. (Eds.). (1997). Host-parasite evolution general principles and Avian models. Oxford: Oxford University Press.

    Google Scholar 

  • Clayton, D. H., Moyer, B. R., Bush, S. E., Jones, T. G., Gardiner, D. W., Rhodes, B. B., et al. (2005). Adaptive significance of avian beak morphology for ectoparasite control. Proceedings of the Royal Society of London. Series B: Biological Sciences, 272, 811–817. doi:10.1098/rspb.2004.3036.

    Article  PubMed  Google Scholar 

  • Combes, C. (2001). Parasitism: The ecology and evolution of intimate interactions. Chicago: University of Chicago Press.

    Google Scholar 

  • de Roode, J. C., Pedersen, A. B., Hunter, M. D., & Altizer, S. (2008). Host plant species affects virulence in monarch butterfly parasites. Journal of Animal Ecology, 77, 120–126. doi:10.1111/j.1365-2656.2007.01305.x.

    Article  PubMed  Google Scholar 

  • Dybdahl, M. F., & Krist, A. C. (2004). Genotypic vs condition effects on parasite-driven rare advantage. Journal of Evolutionary Biology, 17, 967–973. doi:10.1111/j.1420-9101.2004.00759.x.

    Article  PubMed  CAS  Google Scholar 

  • Falconer, D. S., & Mackay, T. F. C. (1996). Introduction to quantitative genetics. London: Longman.

    Google Scholar 

  • Ferguson, H. M., & Read, A. F. (2002). Genetic and environmental determinants of malaria parasite virulence in mosquitoes. Proceedings of the Royal Society of London. Series B: Biological Sciences, 269, 1217–1224. doi:10.1098/rspb.2002.2023.

    Article  PubMed  CAS  Google Scholar 

  • Gasparini, J., Piault, R., Bize, P., & Roulin, A. Pre-hatching maternal effects inhibit nestling humoral immune response in the tawny owl. Journal of Avian Biology (in press).

  • Greischar, M. A., & Koskella, B. (2007). A synthesis of experimental work on parasite local adaptation. Ecology Letters, 10, 418–434. doi:10.1111/j.1461-0248.2007.01028.x.

    Article  PubMed  Google Scholar 

  • Hagemeijer, E. J. M., & Blair, M. J. (Eds.). (1997). The EBCC atlas of European breeding birds: Their distribution and abundance. London: T & A D Poyser.

    Google Scholar 

  • Hamilton, W. D. (1980). Sex versus non-sex versus parasites. Oikos, 35, 282–290. doi:10.2307/3544435.

    Article  Google Scholar 

  • Heeb, P., Kölliker, M., & Richner, H. (2000). Bird-ectoparasite interactions nest humidity and ectoparasite community structure. Ecology, 81, 958–968.

    Google Scholar 

  • Jaenike, J. (1978). An hypothesis to account for the maintenance of sex within population. Evolutionary Theory, 3, 191–194.

    Google Scholar 

  • Krasnov, B. R., Khokhlova, I. S., Arakelyan, M. S., & Degen, A. A. (2005). Is a starving host tastier? Reproduction in fleas parasitizing food-limited rodents. Functional Ecology, 19, 625–631. doi:10.1111/j.1365-2435.2005.01015.x.

    Article  Google Scholar 

  • Laine, A. L. (2008). Temperature-mediated patterns of local adaptation in a natural plant-pathogen metapopulation. Ecology Letters, 11, 327–337. doi:10.1111/j.1461-0248.2007.01146.x.

    Article  PubMed  Google Scholar 

  • Lambrechts, L., Chavatte, J. M., Snounou, G., & Koella, J. C. (2006). Environmental influence on the genetic basis of mosquito resistance to malaria parasites. Proceedings of the Royal Society of London. Series B: Biological Sciences, 273, 1501–1506. doi:10.1098/rspb.2006.3483.

    Article  PubMed  Google Scholar 

  • Little, T. J., & Ebert, D. (2000). The cause of parasitic infection in natural populations of Daphnia (Crustacea: Cladocera): The role of host genetics. Proceedings of the Royal Society of London. Series B: Biological Sciences, 267, 2037–2042. doi:10.1098/rspb.2000.1246.

    Article  PubMed  CAS  Google Scholar 

  • Lively, C. M. (1999). Migration virulence and the geographic mosaic of adaptation by parasites. American Naturalist, 153, S34–S47. doi:10.1086/303210.

    Article  Google Scholar 

  • Lively, C. M., & Dybdahl, M. F. (2000). Parasite adaptation to locally common host genotypes. Nature, 405, 679–681. doi:10.1038/35015069.

    Article  PubMed  CAS  Google Scholar 

  • McCoy, K. D., Boulinier, T., Schjørring, S., & Michalakis, Y. (2002). Local adaptation of an ectoparasite Ixodes uriae to its seabird host. Evolutionary Ecology Research, 4, 441–456.

    Google Scholar 

  • Merilä, J. (1996). Genetic variation in offspring condition: An experiment. Functional Ecology, 10, 465–474. doi:10.2307/2389939.

    Article  Google Scholar 

  • Møller, A. P. (1990). Effects of a haematophagous mite on the barn swallow (Hirundo rustica): A test of the Hamilton and Zuck hypothesis. Evolution; International Journal of Organic Evolution, 44, 771–784. doi:10.2307/2409545.

    Google Scholar 

  • Møller, A. P., Martinelli, R., & Saino, N. (2004). Genetic variation in infestation with a directly transmitted ectoparasite. Journal of Evolutionary Biology, 17, 41–47. doi:10.1046/j.1420-9101.2003.00660.x.

    Article  PubMed  Google Scholar 

  • Mousseau, T. A., & Fox, C. W. (1998). The adaptive significance of maternal effects. Trends in Ecology & Evolution, 13, 403–407. doi:10.1016/S0169-5347(98)01472-4.

    Article  Google Scholar 

  • Mousseau, T. A., & Roff, D. A. (1986). Natural selection and the heritability of fitness components. Heredity, 59, 181–197. doi:10.1038/hdy.1987.113.

    Article  Google Scholar 

  • Müller, W., Groothuis, T. G., Kasprzik, A., Dijkstra, C., Alatalo, R. V., & Siitari, H. (2005). Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks. Proceedings of the Royal Society of London. Series B: Biological Sciences, 272, 1971–1977. doi:10.1098/rspb.2005.3178.

    Article  PubMed  CAS  Google Scholar 

  • Petit, C., Hossaert-McKey, M., Perret, P., Blondel, J., & Lambrechts, M. M. (2002). Blue tits use selected plants and olfaction to maintain an aromatic environment for nestlings. Ecology Letters, 5, 585–589. doi:10.1046/j.1461-0248.2002.00361.x.

    Article  Google Scholar 

  • Roff, D. A. (1997). Evolutionary quantitative genetics. New York: Chapman Hall.

    Google Scholar 

  • Roulin, A., Brinkhof, M. W. G., Bize, P., Richner, H., Jungi, T. W., Bavoux, C., et al. (2003). Which chick is tasty to parasites? The importance of host immunology versus parasite life history. Journal of Animal Ecology, 72, 75–81. doi:10.1046/j.1365-2656.2003.00677.x.

    Article  Google Scholar 

  • Roulin, A., Christe, P., Dijkstra, C., Durcrest, A. L., & Jungi, T. W. (2007). Origin-related environmental sex and age determinants of immunocompetence susceptibility to ectoparasites and disease symptoms in the barn owl. Biological Journal of the Linnaean Society, 90, 703–718. doi:10.1111/j.1095-8312.2007.00759.x.

    Article  Google Scholar 

  • Roulin, A., Gasparini, J., & Froissart, L. (2008). Pre-hatching maternal effects and the tasty chick hypothesis. Evolutionary Ecology Research, 10, 463–473.

    Google Scholar 

  • Shaw, D. J., Grenfell, B. T., & Dobson, A. P. (1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology, 117, 597–610. doi:10.1017/S0031182098003448.

    Article  PubMed  Google Scholar 

  • Sorci, G., Møller, A. P., & Boulinier, T. (1997). Genetics of host–parasite interactions. Trends in Ecology & Evolution, 12, 196–200. doi:10.1016/S0169-5347(97)01056-2.

    Article  Google Scholar 

  • Tinsley, M. C., Blanford, S., & Jiggins, F. M. (2006). Genetic variation in Drosophila melanogaster pathogen susceptibility. Parasitology, 132, 767–773. doi:10.1017/S0031182006009929.

    Article  PubMed  CAS  Google Scholar 

  • Tschirren, B., Fitze, P. S., & Richner, H. (2003). Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings. Journal of Animal Ecology, 72, 839–845. doi:10.1046/j.1365-2656.2003.00755.x.

    Article  Google Scholar 

  • Wiehn, J., & Korpimäki, E. (1998). Resource levels reproduction and resistance to haematozoan infections. Proceedings of the Royal Society of London. Series B: Biological Sciences, 265, 1197–1201. doi:10.1098/rspb.1998.0419.

    Article  Google Scholar 

  • Wolf, J. B., Broodie, E. D., I. I. I., Cheverud, J. M., Moore, A. J., & Wade, M. J. (1998). Evolutionary consequences of indirect genetic effects. Trends in Ecology & Evolution, 13, 64–69. doi:10.1016/S0169-5347(97)01233-0.

    Article  Google Scholar 

Download references

Acknowledgements

We thank Dominik Pfluger and the late Theo Marbot for allowing us to access the colonies, the Swiss National Science Foundation for support (grants n° PP00A-109009 to PB and n° PP00A-102913 to AR), and two anonymous referees for helpful comments. Cross-fostering experiments were carried out under the authorization of the Veterinary Offices of the Cantons Bern and Solothurn.

Author information

Authors and Affiliations

  1. Department of Ecology & Evolution, Biophore, University of Lausanne, 1015, Lausanne, Switzerland

    P. Bize & A. Roulin

Authors
  1. P. Bize
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Roulin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. Bize.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bize, P., Roulin, A. Effects of Common Origin and Common Rearing Environment on Variance in Ectoparasite Load and Phenotype of Nestling Alpine Swifts. Evol Biol 36, 301–310 (2009). https://doi.org/10.1007/s11692-009-9063-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-009-9063-x

Keywords

Search

Navigation