Skip to main content Accessibility help
×
Home
Hostname: page-component-99c86f546-5rzhg Total loading time: 0.269 Render date: 2021-12-01T10:42:57.902Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true, "newUsageEvents": true }

Article contents

Smelling the future: subtle life-history adjustments in response to environmental conditions and perceived transmission opportunities in a trematode

Published online by Cambridge University Press:  08 November 2016

C. LAGRUE*
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
R. RINNEVALLI
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
R. POULIN
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand
*
*Corresponding author: Department of Zoology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand. E-mail: clement.lagrue@gmail.com

Summary

A number of parasites with complex life cycles can abbreviate their life cycles to increase the likelihood of reproducing. For example, some trematodes can facultatively skip the definitive host and produce viable eggs while still inside their intermediate host. The resulting shorter life cycle is clearly advantageous when transmission probabilities to the definitive hosts are low. Coitocaecum parvum can mature precociously (progenesis), and produce eggs by selfing inside its amphipod second intermediate host. Environmental factors such as definitive host density and water temperature influence the life-history strategy adopted by C. parvum in their crustacean host. However, it is also possible that information about transmission opportunities gathered earlier in the life cycle (i.e. by cercariae-producing sporocysts in the first intermediate host) could have priming effects on the adoption of one or the other life strategy. Here we document the effects of environmental parameters (host chemical cues and temperature) on cercarial production within snail hosts and parasite life-history strategy in the amphipod host. We found that environmental cues perceived early in life have limited priming effects on life-history strategies later in life and probably account for only a small part of the variation among conspecific parasites. External cues gathered at the metacercarial stage seem to largely override potential effects of the environmental conditions experienced by early stages of the parasite.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Badets, M., Morrison, C. and Verneau, O. (2010). Alternative parasite development in transmission strategies: how time flies!. Journal of Evolutionary Biology 23, 21512162.CrossRefGoogle ScholarPubMed
Breithaupt, T. and Thiel, M. (2010). Chemical Communication in Crustaceans. Springer Science & Business Media, Berlin, Germany.Google Scholar
Dodson, S. I. (1989). The ecological role of chemical stimuli for the zooplankton predator-induced morphology of Daphnia . Oecologia 78, 361367.CrossRefGoogle ScholarPubMed
Fingerut, J. T., Zimmer, C. A. and Zimmer, R. K. (2003). Patterns and processes of larval emergence in an estuarine parasite system. The Biological Bulletin 205, 110120.CrossRefGoogle Scholar
Frank, S. A. (1996). Models of parasite virulence. Quarterly Review of Biology 71, 3778.CrossRefGoogle ScholarPubMed
Fried, B., Eyster, L. S. and Pechenik, J. A. (1998). Histochemical glycogen and neutral lipid in Echinostoma trivolvis cercariae and effects of exogenous glucose on cercarial longevity. Journal of Helminthology 72, 8385.CrossRefGoogle ScholarPubMed
Fried, B., LaTerra, R. and Kim, Y. (2002). Emergence of cercariae of Echinostoma caproni and Schistosoma mansoni from Biomphalaria glabrata under different laboratory conditions. Journal of Helminthology 76, 369371.CrossRefGoogle ScholarPubMed
Galaktionov, K. V. and Dobrovolskij, A. A. (2003). The Biology and Evolution of Trematodes. Kluwer Academic Publishers, Dordrecht, The Netherlands.CrossRefGoogle Scholar
Graham, A. L. (2003). Effects of snail size and age on the prevalence and intensity of avian schistosome infection: relating laboratory to field studies. Journal of Parasitology 89, 458463.CrossRefGoogle ScholarPubMed
Hay, K. B., Fredensborg, B. L. and Poulin, R. (2005). Trematode induced alterations in shell shape of the mud snail Zeacumantus subcarinatus (Prosobranchia: Batillariidae). Journal of the marine Biological association of the united Kingdom 85, 989992.CrossRefGoogle Scholar
Holomuzki, J. R. and Biggs, B. J. F. (2006). Habitat-specific variation and performance trade-offs in shell armature of New Zealand mudsnails. Ecology 87, 10381047.CrossRefGoogle ScholarPubMed
Holton, A. L. (1984). A redescription of Coitocaecum parvum Crowcroft, 1945 (Digenea: Allocreadiidae) from crustacean and fish hosts in Canterbury. New Zealand Journal of Zoology 11, 18.CrossRefGoogle Scholar
Kats, L. B. and Dill, L. M. (1998). The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5, 361394.CrossRefGoogle Scholar
Koehler, A. V., Brown, B., Poulin, R., Thieltges, D. W. and Fredensborg, B. L. (2012). Disentangling phylogenetic constraints from selective forces in the evolution of trematode transmission strategies. Evolutionary Ecology 26, 14971512.CrossRefGoogle Scholar
Lagrue, C. and Poulin, R. (2007). Life cycle abbreviation in the trematode Coitocaecum parvum: can parasites adjust to variable conditions? Journal of Evolutionary Biology 20, 11891195.CrossRefGoogle ScholarPubMed
Lagrue, C. and Poulin, R. (2008 a). Lack of seasonal variation in the life-history strategies of the trematode Coitocaecum parvum: no apparent environmental effect. Parasitology 135, 19.CrossRefGoogle ScholarPubMed
Lagrue, C. and Poulin, R. (2008 b). Intra- and interspecific competition among helminth parasites: effects on Coitocaecum parvum life-history strategy, size and fecundity. International Journal for Parasitology 38, 14351444.CrossRefGoogle ScholarPubMed
Lagrue, C. and Poulin, R. (2009 a). Life cycle abbreviation in trematode parasites and the developmental time hypothesis: is the clock ticking? Journal of Evolutionary Biology 22, 17271738.CrossRefGoogle ScholarPubMed
Lagrue, C. and Poulin, R. (2009 b). Heritability and short-term effects of inbreeding in the progenetic trematode Coitocaecum parvum: is there a need for the definitive host? Parasitology 136, 231240.CrossRefGoogle Scholar
Lagrue, C., McEwan, J., Poulin, R. and Keeney, D. B. (2007). Co-occurrences of parasite clones and altered host phenotype in a snail–trematode system. International Journal for Parasitology 37, 14591467.CrossRefGoogle Scholar
Lagrue, C., Poulin, R. and Keeney, D. B. (2009). Effects of clonality in multiple infections on the life-history strategy of the trematode Coitocaecum parvum in its amphipod intermediate host. Evolution 63, 14171426.CrossRefGoogle ScholarPubMed
Lagrue, C., Joannes, A., Poulin, R. and Blasco-Costa, I. (2016). Genetic structure and host-parasite co-divergence: evidence for trait-specific local adaptation. Biological Journal of the Linnean Society 118, 344358.CrossRefGoogle Scholar
Lawson, J. R. and Wilson, R. A. (1980). The survival of the cercariae of Schistosoma mansoni in relation to water temperature and glycogen utilization. Parasitology 81, 337348.CrossRefGoogle ScholarPubMed
Lo, C.-T. and Lee, K.-M. (1996). Pattern of emergence and the effects of temperature and light on the emergence and survival of heterophyid cercariae (Centrocestus formosanus and Haplorchis pumilio). Journal of Parasitology 82, 347350.CrossRefGoogle Scholar
Loker, E. S. (1983). A comparative study of the life-histories of mammalian schistosomes. Parasitology 87, 343369.CrossRefGoogle ScholarPubMed
McCarthy, H. O., Fitzpatrick, S. and Irwin, S. W. B. (2002). Life history and life cycles: production and behaviour of trematode cercariae in relation to host exploitation and next-host characteristics. Journal of Parasitology 88, 910918.CrossRefGoogle ScholarPubMed
Morand, S. and Sorci, G. (1998). Determinants of life-history evolution in nematodes. Parasitology Today 14, 193196.CrossRefGoogle ScholarPubMed
Mouritsen, K. N. (2002). The Hydrobia UlvaeMaritrema subdolum association: influence of temperature, salinity, light, water pressure and secondary host exudates on cercarial emergence and longevity. Journal of Helminthology 76, 341347.CrossRefGoogle ScholarPubMed
Parker, G. A., Chubb, J. C., Roberts, G. N., Michaud, M. and Milinski, M. (2003). Optimal growth of larval helminths in their intermediate host. Journal of Evolutionary Biology 16, 4754.CrossRefGoogle Scholar
Pechenik, J. A. and Fried, B. (1995). Effect of temperature on survival and infectivity of Echinostoma trivolvis cercariae: a test of the energy limitation hypothesis. Parasitology 111, 373378.CrossRefGoogle Scholar
Poulin, R. (1996). The evolution of life history strategies in parasitic animals. Advances in Parasitology 37, 107134.CrossRefGoogle ScholarPubMed
Poulin, R. (2003). Information about transmission opportunities triggers a life-history switch in a parasite. Evolution 57, 28992903.CrossRefGoogle Scholar
Poulin, R. (2006). Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143151.CrossRefGoogle ScholarPubMed
Poulin, R. and Cribb, T. H. (2002). Trematode life cycles: short is sweet? Trends in Parasitology 18, 176183.CrossRefGoogle ScholarPubMed
Rowe, D. K., Nichols, S. and Kelly, G. R. (2001). Depth distribution and abundance of the common bully, Gobiomorphus cotidianus (Eleotridae), in three oligotrophic New Zealand lakes, one of which is turbid. Environmental Biology of Fishes 61, 407418.CrossRefGoogle Scholar
Seppälä, O., Liljeroos, K., Karvonen, A. and Jokela, J. (2008). Host condition as a constraint for parasite reproduction. Oikos 117, 749753.CrossRefGoogle Scholar
Shostak, A. W. and Esch, G. W. (1990). Photocycle-dependent emergence by cercariae of Halipegus occidualis from Helisoma anceps, with special reference to cercarial emergence patterns as adaptations for transmission. Journal of Parasitology 76, 790795.CrossRefGoogle Scholar
Thieltges, D. W., de Montaudouin, X., Fredensborg, B. L., Jensen, K. T., Koprivnikar, J. and Poulin, R. (2008). Production of marine trematode cercariae: a potentially overlooked path of energy flow in benthic systems. Marine Ecology Progress Series 372, 147155.CrossRefGoogle Scholar
Thomas, F., Brown, S. P., Sukhdeo, M. and Renaud, F. (2002). Understanding parasite strategies: a state-dependent approach? Trends in Parasitology 18, 387390.CrossRefGoogle ScholarPubMed
Tseng, M. (2006). Interactions between the parasite's previous and current environment mediate the outcome of parasite infection. The American Naturalist 168, 565571.CrossRefGoogle ScholarPubMed
Viney, M. and Cable, J. (2011). Macroparasite life histories. Current Biology 21, R767R774.CrossRefGoogle ScholarPubMed
Xu, X., Stack, R. J., Rao, N. and Caulfield, J. P. (1994). Schistosoma mansoni: fractionation and characterization of the glycocalyx and glycogen-like material from cercariae. Experimental Parasitology 79, 399409.CrossRefGoogle ScholarPubMed
1
Cited by

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Smelling the future: subtle life-history adjustments in response to environmental conditions and perceived transmission opportunities in a trematode
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Smelling the future: subtle life-history adjustments in response to environmental conditions and perceived transmission opportunities in a trematode
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Smelling the future: subtle life-history adjustments in response to environmental conditions and perceived transmission opportunities in a trematode
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *