Marine Biology

, Volume 152, Issue 3, pp 687–695 | Cite as

Local adaptation of immunity against a trematode parasite in marine amphipod populations

  • Kim Bryan-Walker
  • Tommy L. F. Leung
  • Robert PoulinEmail author
Research Article


Resources allocated to defence against parasites are not available for investment in other functions such as growth or reproduction, resulting in trade-offs between different components of an organism’s fitness. In balancing the cost of infection and the cost of immunity, selection should only favour individuals that allocate more energy to resistance and immune responses in populations regularly exposed to debilitating parasites. Here, we compare the ability of amphipods, Paracalliope novizealandiae, to (1) avoid becoming infected and (2) to respond to infection by encapsulating and melanizing parasites, between two natural populations exposed to different risk of parasitism. One population faces high levels of infection by the debilitating trematode parasite Maritrema novaezealandensis, whereas the other population is not parasitised by this trematode nor by any other parasite. Under controlled experimental conditions, with exposure to a standardized dose of parasites, amphipods from the parasite-free population acquired significantly more parasites than those from the population regularly experiencing infection. Furthermore, a lower frequency of amphipods from the parasite-free population succeeded at melanizing (and thus killing) parasites, and they melanized a lower percentage of parasites on average, than amphipods from the parasitised population. These differences persist when individual factors, such as amphipod sex or body length, are taken into account as potential confounding variables. These results support the existence of local adaptation against parasites: an amphipod population that never experiences trematode infections is less capable of resisting infection, both in terms of its first line of defence (avoiding infection) and a later line of defence (fighting parasites following infection), than a population regularly exposed to infection.


Trematode Parasite Amphipod Population Trematode Prevalence Melanization Response Invertebrate Immunity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank the Ecological Parasitology Group of the University of Otago for commenting on an earlier version of this manuscript. The experimental work described in this paper complies with the current laws and animal ethics regulations of New Zealand.


  1. Cerenius L, Soderhall K (2004) The prophenoloxidase-activating system in invertebrates. Immunol Rev 198:116–126CrossRefGoogle Scholar
  2. Fleischer J, Grell M, Hoeg JT, Olesen J (1992) Morphology of grooming limbs in species of Petrolisthes and Pachycheles (Crustacea: Decapoda: Anomura: Porcellanidae): a scanning electron microscopy study. Mar Biol 113:425–435CrossRefGoogle Scholar
  3. Fredensborg BL, Mouritsen KN, Poulin R (2004) Intensity-dependent mortality of Paracalliope novizealandiae (Amphipoda: Crustacea) infected by a trematode: experimental infections and field observations. J Exp Mar Biol Ecol 311:253–265CrossRefGoogle Scholar
  4. Fredensborg BL, Poulin R (2006) Parasitism shaping host life-history evolution: adaptive responses in a marine gastropod to infection by trematodes. J Anim Ecol 75:44–53CrossRefGoogle Scholar
  5. Gillespie JP, Kanost MR, Trenczek T (1997) Biological mediators of insect immunity. Annu Rev Entomol 42:611–643CrossRefGoogle Scholar
  6. Gross P (1993) Insect behavioural and morphological defences against parasitoids. Annu Rev Entomol 38:251–273CrossRefGoogle Scholar
  7. Hart BL (1997) Behavioural defence. In: Clayton DH, Moore J (eds) Host-parasite evolution: general principles and avian models. Oxford University Press, Oxford, pp 59–77Google Scholar
  8. Hasu T, Valtonen ET, Jokela J (2006) Costs of parasite resistance for female survival and parental care in a freshwater isopod. Oikos 114:322–328CrossRefGoogle Scholar
  9. Jacot A, Scheuber H, Brinkhof MWG (2004) Costs of an induced immune response on sexual display and longevity in field crickets. Evolution 58:2280–2286CrossRefGoogle Scholar
  10. Johansson MW, Keyser P, Sritunyalucksana K, Soderhall K (2000) Crustacean hemocytes and haematopoiesis. Aquaculture 191:45–52CrossRefGoogle Scholar
  11. Kalbe M, Kurtz J (2006) Local differences in immunocompetence reflect resistance of sticklebacks against the eye fluke Diplostomum pseudospathaceum. Parasitology 132:105–116CrossRefGoogle Scholar
  12. Karvonen A, Seppälä O, Valtonen ET (2004) Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish. Parasitology 129:159–164CrossRefGoogle Scholar
  13. Kostadinova A, Mavrodieva RS (2005) Microphallids in Gammarus insensibilis Stock, 1966 from a Black Sea lagoon: host response to infection. Parasitology 131:347–354CrossRefGoogle Scholar
  14. Kraaijeveld AR, Ferrari J, Godfray HCJ (2002) Costs of resistance in insect-parasite and insect–parasitoid interactions. Parasitology 125:S71–S82CrossRefGoogle Scholar
  15. Kurtz J, Franz K (2003) Evidence for memory in invertebrate immunity. Nature 425:37–38CrossRefGoogle Scholar
  16. Langand J, Jourdane J, Coustau C, Delay B, Morand S (1998) Cost of resistance, expressed as a delayed maturity, detected in the host–parasite system Biomphalaria glabrata/Echinostoma caproni. Heredity 80:320–325CrossRefGoogle Scholar
  17. Leung TLF, Poulin R (2006) Effects of the trematode Maritrema novaezealandensis on the behaviour of its amphipod host: adaptive or not? J Helminthol 80:271–275PubMedGoogle Scholar
  18. Lindstrom KM, Foufopoulos J, Parn H, Wikelski M (2004) Immunological investments reflect abundance in island populations of Darwin finches. Proc R Soc Lond B 271:1513–1519CrossRefGoogle Scholar
  19. Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98CrossRefGoogle Scholar
  20. Loker ES (1994) On being a parasite in an invertebrate host: a short survival course. J Parasitol 80:728–747CrossRefGoogle Scholar
  21. Martorelli SR, Fredensborg BL, Mouritsen KN, Poulin R (2004) Description and proposed life cycle of Maritrema novaezealandensis n. sp. (Microphallidae) parasitic in red-billed gulls, Larus novaehollandiae scopulinus, from Otago Harbor, South Island, New Zealand. J Parasitol 90:272–277CrossRefGoogle Scholar
  22. Mooring MS, Blumstein DT, Stoner CJ (2004) The evolution of parasite-defence grooming in ungulates. Biol J Linnean Soc 81:17–37CrossRefGoogle Scholar
  23. Moret Y, Schmid-Hempel P (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290:1166–1168CrossRefGoogle Scholar
  24. Plaistow SJ, Outreman Y, Moret Y, Rigaud T (2003) Variation in the risk of being wounded: an overlooked factor in studies of invertebrate immune function? Ecol Lett 6:489–494CrossRefGoogle Scholar
  25. Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17:462–468CrossRefGoogle Scholar
  26. Rigby MC, Moret Y (2000) Life history trade-offs with immune defenses. In: Poulin R, Morand S, Skorping A (eds) Evolutionary biology of host-parasite relationships: theory meets reality. Elsevier, Amsterdam, pp 129–142Google Scholar
  27. Rigby MC, Hechinger RF, Stevens L (2002) Why should parasite resistance be costly? Trends Parasitol 18:116–120CrossRefGoogle Scholar
  28. Rolff J, Siva-Jothy MT (2003) Invertebrate ecological immunology. Science 301:472–475CrossRefGoogle Scholar
  29. Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond B 270:257–366CrossRefGoogle Scholar
  30. Schwarzenbach GA, Ward PI (2006) Responses to selection on phenoloxidase activity in yellow dung flies. Evolution 60:1612–1621CrossRefGoogle Scholar
  31. Sheldon BC, Verhulst S (1996) Ecological immunity: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321CrossRefGoogle Scholar
  32. Sheridan LAD, Poulin R, Ward DF, Zuk M (2000) Sex differences in parasitic infections among arthropod hosts: is there a male bias? Oikos 88:327–334CrossRefGoogle Scholar
  33. Soderhall K, Cerenius L (1998) Role of the prophenoloxidase-activating system in invertebrate immunity. Curr Opin Immunol 10:23–28CrossRefGoogle Scholar
  34. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  35. Thomas F, Guldner E, Renaud F (2000) Differential parasite (Trematoda) encapsulation in Gammarus aequicauda (Amphipoda). J Parasitol 86:650–654CrossRefGoogle Scholar
  36. Tschirren B, Richner H (2006) Parasites shape the optimal investment in immunity. Proc R Soc Lond B 273:1773–1777CrossRefGoogle Scholar
  37. Wedekind C, Jakobsen PJ (1998) Male-biased susceptibility to helminth infection: an experimental test with a copepod. Oikos 81:458–462CrossRefGoogle Scholar
  38. Zuk M, Stoehr AM (2002) Immune defense and host life history. Am Nat 160:S9–S22CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Kim Bryan-Walker
    • 1
  • Tommy L. F. Leung
    • 1
  • Robert Poulin
    • 1
    Email author
  1. 1.Department of ZoologyUniversity of OtagoDunedinNew Zealand

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