Evolutionary Ecology

, Volume 21, Issue 4, pp 561–575 | Cite as

Parasites promote host gene flow in a metapopulation

  • Florian Altermatt
  • Jürgen Hottinger
  • Dieter Ebert
Original Paper


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.


Immigration Local parasite Metapopulation Coevolution Daphnia magna Octosporea bayeri 



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.


  1. Arnold SJ (1977) Polymorphism and geographic variation in feeding-behavior of garter snake Thamnophis elegans. Science 197:676–678CrossRefGoogle Scholar
  2. Bengtsson J, Ebert D (1998) Distribution and impacts of microparasites on Daphnia in a rockpool metapopulation. Oecologia (Berlin) 115:213–221CrossRefGoogle Scholar
  3. Bélichon S, Clobert J, Massot M (1996) Are there differences in fitness components between philopatric and dispersing individuals? Acta Œcologica 17:503–517Google Scholar
  4. Crawley MJ (2002) Statistical computing. An introduction to data analysis using S-Plus. Wiley, ChichesterGoogle Scholar
  5. 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 23:121–135CrossRefGoogle Scholar
  6. Ebert D (1994) Virulence and local adaptation of a horizontally transmitted parasite. Science 265:1084–1086CrossRefGoogle Scholar
  7. Ebert D (1998) Experimental evolution of parasites. Science 282:1432–1435PubMedCrossRefGoogle Scholar
  8. Ebert D (2005) Ecology, epidemiology, and evolution of parasitism in Daphnia. National Library of Medicine (US), National Center for Biotechnology Information, Bethesda, MDGoogle Scholar
  9. Ebert D, Haag C, Kirkpatrick M, Riek M, Hottinger JW, Pajunen VI (2002) A selective advantage to immigrant genes in a Daphnia metapopulation. Science 295:485–488PubMedCrossRefGoogle Scholar
  10. Ebert D, Hottinger JW, Pajunen VI (2001) Temporal and spatial dynamics of parasites in a Daphnia metapopulation: which factors explain parasite richness? Ecology 82:3417–3434Google Scholar
  11. Fry JD (1990) Trade-off in fitness on different hosts: evidence from a selection experiment with a pythophagous mite. Am Nat 136:569–580CrossRefGoogle Scholar
  12. 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 263:1003–1009CrossRefGoogle Scholar
  13. Gonzalez A, Lawton JH, Gilbert FS, Blackburn TM, Evans-Freke I (1998) Metapopulation dynamics, abundance, and distribution in a microecosystem. Science 281:2045–2047PubMedCrossRefGoogle Scholar
  14. Gower CM, Webster JP (2005) Intraspecific competition and the evolution of virulence in a parasitic trematode. Evolution 59:544–553PubMedGoogle Scholar
  15. Green J (1957) Parasites and epibionts of Cladocera in rockpools of Tvärminne archipelago. Arch Soc Zool Bot Fenn Vanamo 12:5–12Google Scholar
  16. 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 170:1809–1820PubMedCrossRefGoogle Scholar
  17. Hanski I (1999) Metapopulation ecology. Oxford University Press, OxfordGoogle Scholar
  18. Hanski I, Pöyry J, Pakkala T, Kuussaari M (1995) Multiple equilibira in metapopulation dynamics. Nature 377:618–621CrossRefGoogle Scholar
  19. Hartl DL, Clark AG (1997) Principles of population genetics, 3rd edn. Sinauer Associates, SunderlandGoogle Scholar
  20. Hebert PDN, Beaton MJ (1993) Methodologies for allozyme analysis using cellulose acetate electrophoresis, 2nd edn. Helena Laboratories, Beaumont, TXGoogle Scholar
  21. Hudson P, Greenman J (1998) Competition mediated by parasites: biological and theoretical progress. Trends Ecol Evol 13:387–390CrossRefGoogle Scholar
  22. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241CrossRefGoogle Scholar
  23. Klüttgen B, Dülmer U, Engels M, Ratte HT (1994) ADaM, an artificial freshwater for the culture of zooplankton. Water Res 28:743–746CrossRefGoogle Scholar
  24. Kurtz J, Klappert K, Schneider W, Reinhold K (2002) Immune defence, dispersal and local adaptation. Evol Ecol Res 4:431–439Google Scholar
  25. Lass S, Ebert D (2006) Apparent seasonality of parasite dynamics: analysis of cyclic prevalence patterns. Proc R Soc B-Biol Sci 273:199–206CrossRefGoogle Scholar
  26. Levins R (1968) Evolution in changing environments. Princeton University Press, Princeton, NJGoogle Scholar
  27. Liberg O et al (2005) Severe inbreeding depression in a wild wolf (Canis lupus) population. Biol Lett 1:17–20PubMedCrossRefGoogle Scholar
  28. 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):6–18CrossRefGoogle Scholar
  29. Lively CM (1989) Adaptation by a parasitic trematode to local-populations of its snail host. Evolution 43:1663–1671CrossRefGoogle Scholar
  30. Lively CM, Dybdahl MF (2000) Parasite adaptation to locally common host genotypes. Nature 405:679–681PubMedCrossRefGoogle Scholar
  31. Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627PubMedCrossRefGoogle Scholar
  32. Møller AP, Martin-Vivaldi M, Soler JJ (2004) Parasitism, host immune defence and dispersal. J Evol Biol 17:603–612PubMedCrossRefGoogle Scholar
  33. Pajunen VI, Pajunen I (2003) Long-term dynamics in rockpool Daphnia metapopulations. Ecography 26:731–738CrossRefGoogle Scholar
  34. Poulin R (1998) Evolutionary ecology of parasites: from individuals to communities. Chapman & Hall, LondonGoogle Scholar
  35. Price PW (1980) Evolutionary biology of parasites. Princeton University Press, Princeton, NJGoogle Scholar
  36. R Development Core Team (2003) R: a language and environment for statistical computing, version 1.6.2. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  37. Ranta E (1979) Niche of Daphnia species in rockpools. Arch Hydrobiol 87:205–223Google Scholar
  38. Saccheri I, Kuusaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:392–395CrossRefGoogle Scholar
  39. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792PubMedCrossRefGoogle Scholar
  40. 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 9:869–878CrossRefGoogle Scholar
  41. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630PubMedCrossRefGoogle Scholar
  42. Vizoso DB, Ebert D (2004) Within-host dynamics of a microsporidium with horizontal and vertical transmission: Octosporea bayeri in Daphnia magna. Parasitology 128:31–38PubMedCrossRefGoogle Scholar
  43. Weisser WW (2000) Metapopulation dynamics in an aphid-parasitoid system. Entomol Exp Appl 97:83–92CrossRefGoogle Scholar
  44. Westemeier RL et al (1998) Tracking the long-term decline and recovery of an isolated population. Science 282:1695–1698PubMedCrossRefGoogle Scholar
  45. Zbinden M, Lass S, Refardt D, Hottinger J, Ebert D (2005) Octosporea bayeri: fumidil B inhibits vertical transmission in Daphnia magna. Exp Parasitol 109:58–61PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Florian Altermatt
    • 1
    • 2
    • 3
  • Jürgen Hottinger
    • 1
    • 2
    • 3
  • Dieter Ebert
    • 1
    • 2
    • 3
  1. 1.Zoologisches InstitutUniversität BaselBaselSwitzerland
  2. 2.Département de Biologie, Unité d’Ecologie et EvolutionUniversité de FribourgFribourgSwitzerland
  3. 3.Tvärminne Zoological StationHankoFinland

Personalised recommendations