Skip to main content
SpringerLink
Log in

Activation of the immune system promotes insect dispersal in the wild

  • Physiological ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Dispersal has important ecological and evolutionary consequences but is a poorly understood behaviour. We experimentally tested whether activation of the immune system affects dispersal in male damselflies, Calopteryx virgo, from three natural populations. We show that males that contained an experimentally inserted artificial pathogen, a nylon monofilament implant, had higher dispersal rates and flew further than control males, but not further than sham manipulated males. Our data suggest that dispersal may reduce the risk of further infections if immune system activation indicates high parasite infection risk in the present habitat. We, thus, suggest that parasites may play an important role in the evolution of host dispersal.

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
Fig. 2

Similar content being viewed by others

References

  • Åbro A (1996) Gregarine infection of adult Calopteryx virgo L. (Odonata: Zygoptera). J Nat Hist 30:855–859

    Article  Google Scholar 

  • Ahlroth P, Alatalo RV, Suhonen J (2009) Reduced dispersal propensity in the wingless waterstrider Aquarius najas in a highly fragmented landscape. Oecologia. doi:10.1007/s00442-009-1457-z

  • Andres JA, Cordero A (1998) Effects of water mites on the damselfly Ceriagrion tenellum. Ecol Entomol 23:103–109

    Article  Google Scholar 

  • Askew RR (1988) The dragonflies of Europe. Harley, London

    Google Scholar 

  • Boulinier T, McCoy K, Sorci G (2001) Dispersal and parasitism. In: Clobert J, Danchin E, Dhondt AA, Nichols JD (eds) Dispersal. Oxford University Press, Oxford, pp 169–179

    Google Scholar 

  • Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225

    Article  PubMed  Google Scholar 

  • Brown CR, Brown MB (1992) Ectoparasitism as a cause of natal dispersal in cliff swallows. Ecology 73:1718–1723

    Article  Google Scholar 

  • Clobert J, Danchin E, Dhondt AA, Nichols JD (2001) Dispersal. Oxford University Press, Oxford

    Google Scholar 

  • Comins HN, Hamilton WD, May RM (1980) Evolutionarily stable dispersal strategies. J Theor Biol 82:205–230

    Article  CAS  PubMed  Google Scholar 

  • Conrad KF, Willson KH, Whitfield K, Harvey IF, Thomas CJ, Sherratt TN (2002) Characteristics of dispersing Ischnura elegans and Coenagrion puella (Odonata): age, sex, size, morph and ectoparasitism. Ecography 25:439–445

    Article  Google Scholar 

  • Contreras-Garduno J, Cordoba-Aguilar A, Lanz-Mendoza H, Cordero-Rivera A (2009) Territorial behaviour and immunity are mediated by juvenile hormone: the physiological basis of honest signalling? Funct Ecol 23:157–163. doi:10.1111/j.1365-2435.2008.01485.x

    Article  Google Scholar 

  • Corbet PS (1999) Dragonflies: behaviour and ecology of Odonata. Harley, Essex

    Google Scholar 

  • Córdoba-Aguilar A, Cordero-Rivera A (2005) Evolution and ecology of calopterygidae (Zygoptera: Odonata): status of knowledge and research perspectives. Neotrop Entomol 34:861–879

    Article  Google Scholar 

  • Dixon AFG, Agarwala BK (1999) Ladybird-induced life-history changes in aphids. Proc R Soc Lond B 266:1549–1553

    Article  Google Scholar 

  • Forbes MR, Robb T (2008) Testing hypotheses about parasite-mediated selection using odonate hosts. In: Córdoba-Aguilar A (ed) Dragonflies and damselflies. Model organism for ecological and evolutionary research. Oxford University Press, Oxford, pp 175–188

    Chapter  Google Scholar 

  • Forbes MR, Muma KE, Smith BP (2004) Recapture of male and female dragonflies in relation to parasitism by mites, time of season, wing length and wing cell symmetry. Exp Appl Acarol 34:79–93

    Article  PubMed  Google Scholar 

  • Hamilton WD, May RM (1977) Dispersal in stable habitats. Nature 269:578–581

    Article  Google Scholar 

  • Hastings A (1983) Can spatial variation alone lead to selection for dispersal. Theor Popul Biol 24:244–251

    Article  Google Scholar 

  • Heeb P, Werner I, Mateman AC, Kolliker M, Brinkhof MWG, Lessells CM, Richner H (1999) Ectoparasite infestation and sex-biased local recruitment of hosts. Nature 400:63–65

    Article  CAS  PubMed  Google Scholar 

  • Holyoak M, Casagrandi R, Nathan R, Revilla E, Spiegel O (2008) Trends and missing parts in the study of movement ecology. Proc Natl Acad Sci USA 105:19060–19065. doi:10.1073/pnas.0800483105

    Article  CAS  PubMed  Google Scholar 

  • Jaenike J, Benway H, Stevens G (1995) Parasite-induced mortality in mycophagous drosophila. Ecology 76:383–391

    Article  Google Scholar 

  • Koskimäki J, Rantala MJ, Taskinen J, Tynkkynen K, Suhonen J (2004) Immunocompetence and resource holding potential in the damselfly, Calopteryx virgo L. Behav Ecol 15:169–173

    Article  Google Scholar 

  • Koskimäki J, Rantala MJ, Suhonen J (2009) Wandering males are smaller than territorial males in the damselfly Calopteryx virgo (L.) (Zygoptera: Calopterygidae). Odonatologica 38:159–165

    Google Scholar 

  • Lee KP, Cory JS, Wilson K, Raubenheimer D, Simpson SJ (2006) Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc R Soc Lond B 273:823–829. doi:10.1098/rspb.2005.3385

    Article  CAS  Google Scholar 

  • Levin SA, Cohen D, Hastings A (1984) Dispersal strategies in patchy environments. Theor Popul Biol 26:165–191

    Article  Google Scholar 

  • Marden JH, Cobb JR (2004) Territorial and mating success of dragonflies that vary in muscle power output and presence of gregarine gut parasites. Anim Behav 68:857–865

    Article  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 

  • Moret Y, Schmid-Hempel P (2000) Survival for immunity: The price of immune system activation for bumblebee workers. Science 290:1166–1168. doi:10.1126/science.290.5494.1166

    Article  CAS  PubMed  Google Scholar 

  • Pajunen VI (1966) Aggressive behaviour and territoriality in a population of Calotperyx virgo L. (Odonata: Calopterygidae). Ann Zool Fenn 3:201–214

    Google Scholar 

  • Plaistow S, Siva-Jothy MT (1996) Energetic constraints and male mate-securing tactics in the damselfly Calopteryx splendens xanthostoma (Charpentier). Proc R Soc Lond B 263:1233–1238

    Article  Google Scholar 

  • Rantala MJ, Roff DA (2007) Inbreeding and extreme outbreeding cause sex differences in immune defence and life history traits in Epirrita autumnata. Heredity 98:329–336

    Article  CAS  PubMed  Google Scholar 

  • Rantala MJ, Koskimäki J, Taskinen J, Tynkkynen K, Suhonen J (2000) Immunocompetence, developmental stability and wingspot size in the damselfly Calopteryx splendens L. Proc R Soc Lond B 267:2453–2457

    Article  CAS  Google Scholar 

  • Rantala MJ, Hovi M, Korkeamäki E, Suhonen J (2001) No trade-off between the size and timing of emergence in the damselfly, Calopteryx virgo L. Ann Zool Fenn 38:117–122

    Google Scholar 

  • Ronce O (2007) How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Evol Syst 38:231–253. doi:10.1146/annurev.ecolsys.38.091206.095611

    Article  Google Scholar 

  • Shields WM (1987) Optimal inbreeding and evolution of philopatry. In: The ecology of animal movement. Clarendon, pp 132–159

  • Siva-Jothy MT (2000) A mechanistic link between parasite resistance and expression of a sexually selected trait in a damselfly. Proc R Soc Lond B 267:2523–2527. doi:10.1098/rspb.2000.1315

    Article  CAS  Google Scholar 

  • Sloggett JJ, Weisser WW (2002) Parasitoids induce production of the dispersal morph of the pea aphid, Acyrthosiphon pisum. Oikos 98:323–333

    Article  Google Scholar 

  • Snoeijs T, Van de Casteele T, Adriaensen F, Matthysen E, Eens M (2004) A strong association between immune responsiveness and natal dispersal in a songbird. Proc R Soc Lond B 271:S199–S201

    Article  Google Scholar 

  • Sorci G, Massot M, Clobert J (1994) Maternal parasite load increases sprint speed and philopatry in female offspring of the common lizard. Am Nat 144:153–164

    Article  Google Scholar 

  • Stettmer C (1996) Colonisation and dispersal patterns of banded (Calopteryx splendens) and beautiful demoiselles (C. virgo) (Odonata: Calopterygidae) in south-east German streams. Eur J Entomol 93:579–593

    Google Scholar 

  • Suhonen J, Rantala MJ, Honkavaara J (2008) Territoriality in odonates. In: Córdoba-Aguilar A (ed) Dragonflies and damselflies: model organisms for ecological and evolutionary research. Oxford University Press, Oxford, pp 203–217

    Google Scholar 

  • Svensson EI, Eroukhmanoff F, Friberg M (2006) Effects of natural and sexual selection on adaptive population divergence and premating isolation in a damselfly. Evolution 60:1242–1253

    PubMed  Google Scholar 

  • Taylor PD, Merriam G (1995) Wing morphology of a forest damselfly is related to landscape structure. Oikos 73:43–48

    Article  Google Scholar 

  • Taylor PD, Merriam G (1996) Habitat fragmentation and parasitism of a forest damselfly. Landsc Ecol 11:181–189

    Article  Google Scholar 

  • Tynkkynen K, Kotiaho JS, Luojumäki M, Suhonen J (2006) Interspecific territoriality in Calopteryx damselflies: the role of secondary sexual characters. Anim Behav 71:299–306

    Article  Google Scholar 

  • Van Vuren D (1996) Ectoparasites, fitness and social behaviour of yellow-bellied marmots. Ethology 102:686–694

    Article  Google Scholar 

  • Weisser WW, Braendle C, Minoretti N (1999) Predator-induced morphological shift in the pea aphid. Proc R Soc Lond B 266:1175–1181

    Article  Google Scholar 

Download references

Acknowledgments

We thank Henna Aaltonen, Jaakko Ilvonen, Katariina Kangassalo, Kari Kaunisto, Janne Kumpulainen, Topias Laaksonen, Kalle Laitila, Pipsa Lappalainen, Urzula Malinkowska, Lauri Rantanen, Eeva Rönnholm, Teijo Saikkonen, Anna Sipilä, Anssi Susilahti, Sini Tuomola and Heidi Viitaniemi for assistance in the field. Special thanks to Alexandro Cordoba-Aguilar, Andre Dhondt and Derek Dunn for comments on the manuscript. In addition, D. Dunn kindly checked the English. This study was supported by the Academy of Finland to M. J. R., J. H. and J. S.

Author information

Authors and Affiliations

  1. Section of Ecology, Department of Biology, University of Turku, 20014, Turku, Finland

    Jukka Suhonen, Johanna Honkavaara & Markus J. Rantala

Authors
  1. Jukka Suhonen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Johanna Honkavaara
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Markus J. Rantala
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jukka Suhonen.

Additional information

Communicated by Carla Caceres.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Suhonen, J., Honkavaara, J. & Rantala, M.J. Activation of the immune system promotes insect dispersal in the wild. Oecologia 162, 541–547 (2010). https://doi.org/10.1007/s00442-009-1470-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-009-1470-2

Keywords

Search

Navigation