Skip to main content
Log in

Parasites promote host gene flow in a metapopulation

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Local adaptation is a powerful mechanism to maintain genetic diversity in subdivided populations. It counteracts the homogenizing effect of gene flow because immigrants have an inferior fitness in the new habitat. This picture may be reversed in host populations where parasites influence the success of immigrating hosts. Here we report two experiments testing whether parasite abundance and genetic background influences the success of host migration among pools in a Daphnia magna metapopulation. In 22 natural populations of D. magna, immigrant hosts were found to be on average more successful when the resident populations experienced high prevalences of a local microsporidian parasite. We then determined whether this success is due to parasitism per se, or the genetic background of the parasites. In a common garden competition experiment, we found that parasites reduced the fitness of their local hosts relatively more than the fitness of allopatric host genotypes. Our experiments are consistent with theoretical predictions based on coevolutionary host-parasite models in metapopulations. A direct consequence of the observed mechanism is an elevated effective migration rate for the host in the metapopulation.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Arnold SJ (1977) Polymorphism and geographic variation in feeding-behavior of garter snake Thamnophis elegans. Science 197:676–678

    Article  Google Scholar 

  • Bengtsson J, Ebert D (1998) Distribution and impacts of microparasites on Daphnia in a rockpool metapopulation. Oecologia (Berlin) 115:213–221

    Article  Google Scholar 

  • Bélichon S, Clobert J, Massot M (1996) Are there differences in fitness components between philopatric and dispersing individuals? Acta Œcologica 17:503–517

    Google Scholar 

  • Crawley MJ (2002) Statistical computing. An introduction to data analysis using S-Plus. Wiley, Chichester

    Google Scholar 

  • De Meester L, Gomez A, Okamura B, Schwenk K (2002) The monopolization hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecol-Int J Ecol 23:121–135

    Article  Google Scholar 

  • Ebert D (1994) Virulence and local adaptation of a horizontally transmitted parasite. Science 265:1084–1086

    Article  Google Scholar 

  • Ebert D (1998) Experimental evolution of parasites. Science 282:1432–1435

    Article  PubMed  CAS  Google Scholar 

  • Ebert D (2005) Ecology, epidemiology, and evolution of parasitism in Daphnia. National Library of Medicine (US), National Center for Biotechnology Information, Bethesda, MD

  • Ebert D, Haag C, Kirkpatrick M, Riek M, Hottinger JW, Pajunen VI (2002) A selective advantage to immigrant genes in a Daphnia metapopulation. Science 295:485–488

    Article  PubMed  CAS  Google Scholar 

  • Ebert D, Hottinger JW, Pajunen VI (2001) Temporal and spatial dynamics of parasites in a Daphnia metapopulation: which factors explain parasite richness? Ecology 82:3417–3434

    Google Scholar 

  • Fry JD (1990) Trade-off in fitness on different hosts: evidence from a selection experiment with a pythophagous mite. Am Nat 136:569–580

    Article  Google Scholar 

  • Gandon S, Capowiez Y, Dubois Y, Michalakis Y, Olivieri I (1996) Local adaptation and gene-for-gene coevolution in a metapopulation model. Proc R Soc Lond Ser B-Biol Sci 263:1003–1009

    Article  Google Scholar 

  • Gonzalez A, Lawton JH, Gilbert FS, Blackburn TM, Evans-Freke I (1998) Metapopulation dynamics, abundance, and distribution in a microecosystem. Science 281:2045–2047

    Article  PubMed  CAS  Google Scholar 

  • Gower CM, Webster JP (2005) Intraspecific competition and the evolution of virulence in a parasitic trematode. Evolution 59:544–553

    PubMed  CAS  Google Scholar 

  • Green J (1957) Parasites and epibionts of Cladocera in rockpools of Tvärminne archipelago. Arch Soc Zool Bot Fenn Vanamo 12:5–12

    Google Scholar 

  • Haag CR, Riek M, Hottinger JW, Pajunen VI, Ebert D (2005) Genetic diversity and genetic differentiation in Daphnia metapopulations with subpopulations of known age. Genetics 170:1809–1820

    Article  PubMed  CAS  Google Scholar 

  • Hanski I (1999) Metapopulation ecology. Oxford University Press, Oxford

    Google Scholar 

  • Hanski I, Pöyry J, Pakkala T, Kuussaari M (1995) Multiple equilibira in metapopulation dynamics. Nature 377:618–621

    Article  CAS  Google Scholar 

  • Hartl DL, Clark AG (1997) Principles of population genetics, 3rd edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Hebert PDN, Beaton MJ (1993) Methodologies for allozyme analysis using cellulose acetate electrophoresis, 2nd edn. Helena Laboratories, Beaumont, TX

    Google Scholar 

  • Hudson P, Greenman J (1998) Competition mediated by parasites: biological and theoretical progress. Trends Ecol Evol 13:387–390

    Article  Google Scholar 

  • Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241

    Article  Google Scholar 

  • Klüttgen B, Dülmer U, Engels M, Ratte HT (1994) ADaM, an artificial freshwater for the culture of zooplankton. Water Res 28:743–746

    Article  Google Scholar 

  • Kurtz J, Klappert K, Schneider W, Reinhold K (2002) Immune defence, dispersal and local adaptation. Evol Ecol Res 4:431–439

    Google Scholar 

  • Lass S, Ebert D (2006) Apparent seasonality of parasite dynamics: analysis of cyclic prevalence patterns. Proc R Soc B-Biol Sci 273:199–206

    Article  Google Scholar 

  • Levins R (1968) Evolution in changing environments. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Liberg O et al (2005) Severe inbreeding depression in a wild wolf (Canis lupus) population. Biol Lett 1:17–20

    Article  PubMed  CAS  Google Scholar 

  • Lively C, Dybdahl ME, Jokela J, Osnas EE, Delph LE (2004) Host sex and local adaptation by parasites in a snail-trematode interaction. Am Nat 164(Suppl):6–18

    Article  Google Scholar 

  • Lively CM (1989) Adaptation by a parasitic trematode to local-populations of its snail host. Evolution 43:1663–1671

    Article  Google Scholar 

  • Lively CM, Dybdahl MF (2000) Parasite adaptation to locally common host genotypes. Nature 405:679–681

    Article  PubMed  CAS  Google Scholar 

  • Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627

    Article  PubMed  CAS  Google Scholar 

  • Møller AP, Martin-Vivaldi M, Soler JJ (2004) Parasitism, host immune defence and dispersal. J Evol Biol 17:603–612

    Article  PubMed  Google Scholar 

  • Pajunen VI, Pajunen I (2003) Long-term dynamics in rockpool Daphnia metapopulations. Ecography 26:731–738

    Article  Google Scholar 

  • Poulin R (1998) Evolutionary ecology of parasites: from individuals to communities. Chapman & Hall, London

    Google Scholar 

  • Price PW (1980) Evolutionary biology of parasites. Princeton University Press, Princeton, NJ

    Google Scholar 

  • R Development Core Team (2003) R: a language and environment for statistical computing, version 1.6.2. R Foundation for Statistical Computing, Vienna, Austria

  • Ranta E (1979) Niche of Daphnia species in rockpools. Arch Hydrobiol 87:205–223

    Google Scholar 

  • Saccheri I, Kuusaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:392–395

    Article  CAS  Google Scholar 

  • Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792

    Article  PubMed  CAS  Google Scholar 

  • Telschow A, Engelstädter J, Yamamura N, Hammerstein P, Hurst GDD (2006) Asymmetric gene flow and constraints on adaptation caused by sex ratio distorters. J Evol Biol 9:869–878

    Article  Google Scholar 

  • Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630

    Article  PubMed  CAS  Google Scholar 

  • Vizoso DB, Ebert D (2004) Within-host dynamics of a microsporidium with horizontal and vertical transmission: Octosporea bayeri in Daphnia magna. Parasitology 128:31–38

    Article  PubMed  CAS  Google Scholar 

  • Weisser WW (2000) Metapopulation dynamics in an aphid-parasitoid system. Entomol Exp Appl 97:83–92

    Article  Google Scholar 

  • Westemeier RL et al (1998) Tracking the long-term decline and recovery of an isolated population. Science 282:1695–1698

    Article  PubMed  CAS  Google Scholar 

  • Zbinden M, Lass S, Refardt D, Hottinger J, Ebert D (2005) Octosporea bayeri: fumidil B inhibits vertical transmission in Daphnia magna. Exp Parasitol 109:58–61

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank H. Ganz, T. Kawecki, M. Kölliker, S. Lass, M. Zbinden, T. Zumbrunn, S. Zweizig and the anonymous reviewers for comments to earlier versions of the manuscript. The study was supported by the Swiss National Science Foundation. F.A. thanks the Tomcsik-Foundation and the Swiss Academy of Sciences for financial support during the fieldwork. This is part of project nr 97524006 at Tvärminne Zoological Station.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dieter Ebert.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Altermatt, F., Hottinger, J. & Ebert, D. Parasites promote host gene flow in a metapopulation. Evol Ecol 21, 561–575 (2007). https://doi.org/10.1007/s10682-006-9136-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-006-9136-6

Keywords

Navigation