Skip to main content
SpringerLink
Log in

Life history interactions with environmental conditions in a host–parasite relationship and the parasite's mode of transmission

  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

The microsporidian parasite Edhazardia aedis is capable of vertical or horizontal transmission among individuals of its host, the mosquito Aedes aegypti, and either mode of transmission may follow the other. We show that following the horizontal infection of host larvae, the parasite's subsequent mode of transmission largely depends on host life history traits and their responses to different environmental conditions. In two experiments the intensity of larval exposure to infection and the amount of food available to them were simultaneously manipulated. One experiment followed the dynamics of host development and the parasite's production of spores while the other estimated the outcome of their relationship. Host life history traits varied widely across treatment conditions while those of the parasite did not. Of particular importance was the host's larval growth rate. Horizontal rather than vertical transmission by the parasite was more likely as low food and high dose conditions favoured slower larval growth rates. This pattern of transmission behaviour with host growth rate can be considered in terms of reproductive value: the potential vertical transmission success that female mosquitoes offer the parasite decreases as larval growth rates slow and makes them more attractive to exploitation for horizontal transmission (requiring host mortality). However, the lack of variation in the parasite's life history traits gave rise in some conditions to low estimates for both its vertical and horizontal transmission success. We suggest that the unresponsive behaviour of the parasite's life history traits reflects a bet-hedging strategy to reduce variance in its overall transmission success in the unpredictable environmental conditions and host larval growth rates that this parasite encounters in nature.

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

Similar content being viewed by others

References

  • Agnew, P. and Koella, J.C. (1997) Virulence, parasite mode of transmission, and host fluctuating asymmetry. Proc. R. Soc. Lond. B 264, 9–15.

    Google Scholar 

  • Anderson, R.M. and May, R.M. (1991) Infectious diseases of humans: dynamics and control. Oxford University Press, Oxford.

    Google Scholar 

  • Antia, R., Levin, B.R. and May, R.M. (1994) Within-host population dynamics and the evolution and maintenance of microparasite virulence. Am. Nat. 144, 457–472.

    Google Scholar 

  • Apostol, B.L., Black, W.C.I., Reiter, P. and Miller, B.R. (1994) Use of randomly amplified polymorphic DNA amplified by polymerase chain reaction markers to estimate the number of Aedes aegypti families at oviposition sites in San Juan, Puerto Rico. Am. J. Trop. Med. Hyg. 51, 89–97.

    Google Scholar 

  • Becnel, J.J., Garcia, J.J. and Johnson, M.A. (1995) Edhazardia aedis (Microspora: Culicosporidae) effects on the reproductive capacity of Aedes aegypti (Diptera: Culicidae). J. Med. Entomol. 32, 549–553.

    Google Scholar 

  • Becnel, J.J. and Johnson, M.A. (1993) Mosquito host range and specificity of Edhazardia aedis (Microspora, Culicosporidae). J. Am. Mosq. Control Assoc. 9, 269–274.

    Google Scholar 

  • Becnel, J.J., Sprague, V., Fukuda, T. and Hazard, E.I. (1989) Development of Edhazardia aedis (Kudo, 1930) N.G., N. Comb. (Microsporida: Amblyosporidae) in the mosquito Aedes aegypti (L.) (Diptera: Culicidae). J. Protozool. 36, 119–130.

    Google Scholar 

  • Berrigan, D. and Koella, J.C. (1994) The evolution of reaction norms: simple models for age and size at maturity. J. evol. Biol. 7, 549–566.

    Google Scholar 

  • Briegel, H. (1990) Metabolic relationship between female body size, reserves, and fecundity of Aedes aegypti. J. Insect Physiol. 36, 165–172.

    Google Scholar 

  • Bull, J.J. (1994) Perspective: Virulence. Evolution 48, 1423–1437.

    Google Scholar 

  • Christophers, S.R. (1960) Aedes aegypti (L.) the yellow fever mosquito. Its life history, bionomics and structure. Cambridge University Press, Cambridge.

    Google Scholar 

  • Cossentine, J.E. and Lewis, L.C. (1986) Impact of Vairimorpha necatrix and Vairimorpha sp. (Microspora: Microsporida) on Bonnetia comta (Diptera: Tachinidae) within Agrotis ipsilon (Lepidoptera: Noctuidae) hosts. J. Invertebr. Pathol. 47, 303–309.

    Google Scholar 

  • Dye, C. (1984) Competition amongst larval Aedes aegypti: the role of interference. Ecol. Entomol. 9, 355–357.

    Google Scholar 

  • Ebert, D. (1995) The ecological interaction between a microsporidian parasite and its host Daphnia magna. J. Anim. Ecol. 64, 361–369.

    Google Scholar 

  • Ewald, P.W. (1994) Evolution of Infectious Disease. Oxford University Press, New York.

    Google Scholar 

  • Fialho, R.F. and Schall, J.J. (1995) Thermal ecology of a malarial parasite and its insect vector: consquences for the parasite's transmission success. J. Anim. Ecol. 64, 553–562.

    Google Scholar 

  • Fisher, R.A. (1958) The genetical theory of natural selection. Dover Publications, Inc., New York.

    Google Scholar 

  • Focks, D.A., Haile, D.G., Daniels, E. and Mount, G.A. (1993) Dynamic life table model for Aedes aegypti (L.) (Diptera: Culicidae). Analysis of the literature and model development. J. Med. Entomol. 30, 1003–1017.

    Google Scholar 

  • Frank, S.A. (1992) A kin selection model for the evolution of virulence. Proc. R. Soc. Lond. B 250, 195–197.

    Google Scholar 

  • Frank, S.A. (1996) Models of parasite virulence. Q. Rev. Biol. 71, 37–78.

    Google Scholar 

  • Gillespie, J.H. (1974) Natural selection for within-generation variance in offspring number. Genetics 76, 601–606.

    Google Scholar 

  • Gilpin, M.E. and McClelland, G.A.H. (1979) Systems analysis of the Yellow Fever mosquito Aedes aegypti. Fortschr. Zool. 25, 355–388.

    Google Scholar 

  • Hamilton, W.D., Axelrod, A. and Tanese, R. (1990) Sexual reproduction as an adaptation to resist parasites (a review). Proc. Natl. Acad. Sci. USA 87, 3566–3573.

    Google Scholar 

  • Hembree, S.C. (1979) Preliminary report of some mosquito pathogens in Thailand. Mosq. News 39, 575–582.

    Google Scholar 

  • Hembree, S.C. and Ryan, J.R. (1982) Obervations on the vertical transmission of a new microsporidian pathogen of Aedes aegypti from Thailand. Mosq. News 42, 49–55.

    Google Scholar 

  • Hochberg, M.E., Michalakis, Y. and de Meeus, T. (1992) Parasitism as a constraint on the rate of life-history evolution. J. Evol. Biol. 5, 491–504.

    Google Scholar 

  • Johnson, M.A., Becnel, J.J. and Undeen, A.H. (1997) A new sporulation sequence in Edhazardia aedis (Microsporidia: Culicosporidiae), a parasite of the mosquito Aedes aegypti (Diptera: Culicidae). J. Invertebr. Pathol. 70, 69–75.

    Google Scholar 

  • Koella, J.C. and Agnew, P. (1997) Blood-feeding success of the mosquito Aedes aegypti depends on the transmission route of its parasite Edhazardia aedis. Oikos 78, 311–316.

    Google Scholar 

  • Koella, J.C. and Agnew, P. (1999) A correlated response of a parasite's virulence and life cycle to selection on its host's life history. J. Evol. Biol. 12, 70–79.

    Google Scholar 

  • Koella, J.C., Agnew, P. and Michalakis, Y. (1998) Coevolutionary interactions between host life histories and parasite life cycles. Parasitology 116, S47-S55.

    Google Scholar 

  • Koella, J.C. and Antia, R. (1995) Optimal pattern of replication and transmission for parasites with two stages in their life cycle. Theor. Popul. Biol. 47, 277–291.

    Google Scholar 

  • Kudo, R. (1930) Studies on microsporidia parasitic in mosquitoes. VIII. On a microsporidian, Nosema aedis nov. sp., parasitic in the larva of Aedes aegypti of Puerto Rico. Arch Protistenkd 69, 23–28.

    Google Scholar 

  • Lord, J.C. and Hall, D.W. (1983) Sporulation of Amblyospora (Microsporidia) in female Culex salinarius: Induction by 20-hydroxyecdysone. Parasitology 87, 377–383.

    Google Scholar 

  • Lucarotti, C.J. and Andreadis, T.G. (1995) Reproductive strategies and adaptations for survival among obligatory microsporidian and fungal parasites of mosquitoes: a comparative analysis of Amblyospora and Coelomomyces. J. Am. Mosq. Control Assoc. 11, 111–121.

    Google Scholar 

  • MacGregor, M.E. (1915) Notes on the rearing of Stegomyia fasciata in London. J. Trop. Med. (Hyg.) 18, 193–196.

    Google Scholar 

  • Michalakis, Y. and Hochberg, M.E. (1994) Parasitic effects on host life-history traits: a review of recent studies. Parasite 1, 291–294.

    Google Scholar 

  • Michalakis, Y., Olivieri, I., Renaud, F. and Raymond, M. (1992) Pleiotropic action of parasites: how to be good for the host. Trends Evol. Ecol. 7, 59–62.

    Google Scholar 

  • Müller, C.B. and Schmid-Hempel, P. (1993) Exploitation of cold temperature as defense against parasitoids in bumbleebees. Nature 363, 65–67.

    Google Scholar 

  • Philippi, T. and Seger, J. (1989) Hedging one's evolutionary bets, revisited. Trends Evol. Ecol. 4, 41–44.

    Google Scholar 

  • SAS Institute. (1994) JMP. Cary: SAS Institute Inc.

    Google Scholar 

  • Seger, J. and Brockman, H.J. (1987) What is bet-hedging? In P. Harvey and L. Partridge (ed.) Oxford Surveys of Evolutionary Biology, vol. 4, pp. 182–211. Oxford University Press, Oxford.

    Google Scholar 

  • Sokal, R.R. and Rohlf, F.J. (1995) Biometry, the principles and practice of statistics in biological research. W. H. Freeman and Company, San Fransisco.

    Google Scholar 

  • Southwood, T.R.E., Murdie, G., Yasuno, M., Tonn, R.J. and Reader, P.M. (1972) Studies on the life budget of Aedes aegypti in Wat Samphaya, Bangkok, Thailand. Bull. Wld. Hlth. Org. 46, 211–226.

    Google Scholar 

  • Undeen, A.H. and Becnel, J.J. (1992) Longevity and germination of Edhazardia aedis (Microspora, Amblyosporidae) spores. Biocontrol Sci. Technol. 2, 247–256.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Experimental Ecology, ETH-Zurich, ETH Zentrum NW, CH-8092, Zurich, Switzerland, and

    Philip Agnew & Jacob C. Koella

  2. Department of Zoology, Aarhus University, Universitetsparken B135, DK-8000, Aarhus C, Denmark

    Philip Agnew & Jacob C. Koella

Authors
  1. Philip Agnew
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jacob C. Koella
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Agnew, P., Koella, J.C. Life history interactions with environmental conditions in a host–parasite relationship and the parasite's mode of transmission. Evolutionary Ecology 13, 67–91 (1999). https://doi.org/10.1023/A:1006586131235

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006586131235

Search

Navigation