Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-26T08:54:26.809Z Has data issue: false hasContentIssue false
  • English
  • Français

Positive density-dependent growth supports costs sharing hypothesis and population density sensing in a manipulative parasite

Published online by Cambridge University Press:  27 June 2017

MIKHAIL GOPKO Open the ORCID record for MIKHAIL GOPKO [Opens in a new window] ,
VICTOR N. MIKHEEV  and
JOUNI TASKINEN
MIKHAIL GOPKO*
Affiliation:
A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 33 Leninsky Prospekt, 119071 Moscow, Russia
VICTOR N. MIKHEEV
Affiliation:
A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 33 Leninsky Prospekt, 119071 Moscow, Russia
JOUNI TASKINEN
Affiliation:
Department of Biological and Environmental Science, University of Jyväskylä, P.O. Box 35 (YAC-315.2), FI-40014 Jyväskylä, Finland
*
*Corresponding author: Laboratory for Behaviour of Lower Vertebrates, Institute of Ecology and Evolution, RAS, 33 Leninskij prospect, Moscow 119071, Russia. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Parasites manipulate their hosts’ phenotype to increase their own fitness. Like any evolutionary adaptation, parasitic manipulations should be costly. Though it is difficult to measure costs of the manipulation directly, they can be evaluated using an indirect approach. For instance, theory suggests that as the parasite infrapopulation grows, the investment of individual parasites in host manipulation decreases, because of cost sharing. Another assumption is that in environments where manipulation does not pay off for the parasite, it can decrease its investment in the manipulation to save resources. We experimentally infected rainbow trout Oncorhynchus mykiss with the immature larvae of the trematode Diplostomum pseudospathaceum, to test these assumptions. Immature D. pseudospathaceum metacercariae are known for their ability to manipulate the behaviour of their host enhancing its anti-predator defenses to avoid concomitant predation. We found that the growth rate of individual parasites in rainbow trout increased with the infrapopulation size (positive density-dependence) suggesting cost sharing. Moreover, parasites adjusted their growth to the intensity of infection within the eye lens where they were localized suggesting population density sensing. Results of this study support the hypothesis that macroparasites can adjust their growth rate and manipulation investment according to cost sharing level and infrapopulation size.

Keywords

parasitic manipulationhost–parasite interactionsmanipulation costscost sharingpositive density-dependencepopulation density sensinginfrapopulation sizeimmature parasites
Type
Research Article
Information
Parasitology , Volume 144 , Issue 11 , September 2017 , pp. 1511 - 1518
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

REFERENCES

Adamo, S. A. (2012). The strings of the puppet master: how parasites change host behavior. In Host Manipulation by Parasites (ed. Hughes, D. P., Brodeur, J. and Thomas, F.), pp. 36–53. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Adamo, S. A. (2013). Parasites: evolution's neurobiologists. Journal of Experimental Biology 216, 3–10.CrossRefGoogle ScholarPubMed
Anderson, R. A., Koella, J. C. and Hurd, H. (1999). The effect of Plasmodium yoelii nigeriensis infection on the feeding persistence of Anopheles stephensi Liston throughout the sporogonic cycle. Proceedings of the Royal Society of London B 266, 1729–1733.CrossRefGoogle ScholarPubMed
Bafumi, J. and Gelman, A. E. (2006). Fitting multilevel models when predictors and group effects correlate. http://academiccommons.columbia.edu/item/ac:125243.Google Scholar
Bates, D., Maechler, M., Bolker, B. and Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.CrossRefGoogle Scholar
Bell, A. and Jones, K. (2015). Explaining fixed effects: random effects modeling of time-series cross-sectional and panel data. Political Science Research and Methods 3, 133–153.CrossRefGoogle Scholar
Benesh, D. P. (2010). What are the evolutionary constraints on larval growth in a trophically transmitted parasite? Oecologia 162, 599–608.CrossRefGoogle Scholar
Bethel, W. M. and Holmes, J. C. (1973). Altered evasive behaviour and responses to light in amphipods harboring acanthocephalan cystacanths. Journal of Parasitology 59, 945–954.CrossRefGoogle Scholar
Bethel, W. M. and Holmes, J. C. (1977). Increased vulnerability of amphipods to predation owing to altered behaviour induced by larval acanthocephalans. Canadian Journal of Zoology 55, 110–115.CrossRefGoogle Scholar
Bibby, M. C. and Rees, G. (1971). The uptake of radio-active glucose in vivo and in vitro by the metacercaria of Diplostomum phoxini (Faust) and its conversion to glycogen. Parasitology Research 37, 187–197.Google ScholarPubMed
Brown, G. E. and Smith, R. J. F. (1997). Conspecific skin extracts elicit antipredator responses in juvenile rainbow trout (Oncorhynchus mykiss). Canadian Journal of Zoology 75, 1916–1922.CrossRefGoogle Scholar
Brown, S. P. (1999). Cooperation and conflict in host-manipulating parasites. Proceedings of the Royal Society of London B 266, 1899–1904.CrossRefGoogle Scholar
Brown, S. P., De Lorgeril, J., Joly, C. and Thomas, F. (2003). Field evidence for density-dependent effects in the trematode Microphallus papillorobustus in its manipulated host, Gammarus insensibilis . Journal of Parasitology 89, 668–672.CrossRefGoogle ScholarPubMed
Candia, O. (2004). Electrolyte and fluid transport across corneal, conjunctival and lens epithelia. Experimental Eye Research 78, 527–535.CrossRefGoogle ScholarPubMed
Cézilly, F., Perrot-Minnot, M.-J. and Rigaud, T. (2014). Cooperation and conflict in host manipulation: interactions among macro-parasites and micro-organisms. Frontiers in Microbiology 5, 248.Google ScholarPubMed
Chylack, L. T. and Cheng, H. M. (1978). Sugar metabolism in the crystallin lens. Survey of Ophthalmology 23, 26–34.CrossRefGoogle Scholar
Cornet, S. (2011). Density-dependent effects on parasite growth and parasite-induced host immunodepression in the larval helminth Pomphorhynchus laevis . Parasitology 138, 257–265.CrossRefGoogle ScholarPubMed
Dawkins, R. (1982). The Extended Phenotype. Oxford University Press, Oxford, UK.Google Scholar
De Block, M. and Stoks, R. (2005). Fitness effects from egg to reproduction: bridging the life-history transition. Ecology 86, 185–197.CrossRefGoogle Scholar
Désilets, H. D., Locke, S. A., McLaughlin, J. D. and Marcogliese, D. J. (2013). Community structure of Diplostomum spp. (Digenea: Diplostomidae) in eyes of fish: main determinants and potential interspecific interactions. International Journal for Parasitology 43, 929–939.CrossRefGoogle ScholarPubMed
Dezfuli, B. S., Giari, L. and Poulin, R. (2001). Costs of intraspecific and interspecific host sharing in acanthocephalan cystacanths. Parasitology 122, 483–489.CrossRefGoogle ScholarPubMed
Dianne, L., Perrot-Minnot, M.-J., Bauer, A., Gaillard, M., Léger, E. and Rigaud, T. (2011). Protection first then facilitation: a manipulative parasite modulates the vulnerability to predation of its intermediate host according to its own developmental stage. Evolution 65, 2692–2698.CrossRefGoogle ScholarPubMed
Dianne, L., Bollache, L., Lagrue, C., Franceschi, N. and Rigaud, T. (2012). Larval size in acanthocephalan parasites: influence of intraspecific competition and effects on intermediate host behavioural changes. Parasites and Vectors 5, 166.CrossRefGoogle ScholarPubMed
Ferrari, M. C. O., Wisenden, B. D. and Chivers, D. P. (2010). Chemical ecology of predator–prey interactions in aquatic ecosystems: a review and prospectus. Canadian Journal of Zoology 88, 698–724.CrossRefGoogle Scholar
Gopko, M. V., Mikheev, V. N. and Taskinen, J. (2015). Changes in host behaviour caused by immature larvae of the eye fluke: evidence supporting the predation suppression hypothesis. Behavioral Ecology and Sociobiology 69, 1723–1730.CrossRefGoogle Scholar
Gopko, M. V., Mikheev, V. N. and Taskinen, J. (2017). Deterioration of basic components of the anti-predator behavior in fish harboring eye fluke larvae. Behavioral Ecology and Sociobiology 71, 68.CrossRefGoogle Scholar
Hafer, N. (2016). Conflicts over host manipulation between different parasites and pathogens: investigating the ecological and medical consequences. BioEssays 38, 1027–1037.CrossRefGoogle ScholarPubMed
Hafer, N. and Benesh, D. P. (2015). Does resource availability affect host manipulation? – an experimental test with Schistocephalus solidus . Parasitology Open 1, e3.CrossRefGoogle Scholar
Hafer, N. and Milinski, M. (2015). When parasites disagree: evidence for parasite-induced sabotage of host manipulation. Evolution 69, 611–620.CrossRefGoogle ScholarPubMed
Hafer, N. and Milinski, M. (2016). Inter- and intraspecific conflicts between parasites over host manipulation. Proceedings of the Royal Society of London B 283, 20152870.Google ScholarPubMed
Hammerschmidt, K., Koch, K., Milinski, M., Chubb, J. C. and Parker, G. A. (2009). When to go: optimization of host switching in parasites with complex life cycles. Evolution 63, 1976–1986.CrossRefGoogle ScholarPubMed
Höglund, J. and Thuvander, A. (1990). Indications of nonspecific protective mechanisms in rainbow trout Oncorhynchus mykiss with diplostomosis. Diseases of Aquatic Organisms 8, 91–97.CrossRefGoogle Scholar
Karvonen, A., Seppälä, O. and Valtonen, E. T. (2004). Eye fluke-induced cataract formation in fish: quantitative analysis using an ophthalmological microscope. Parasitology 129, 473–478.CrossRefGoogle ScholarPubMed
Kingsolver, J. G. and Huey, R. B. (2008). Size, temperature, and fitness: three rules. Evolutionary Ecology Research 10, 251–268.Google Scholar
Lafferty, K. D. and Morris, A. K. (1996). Altered behaviour of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77, 1390–1397.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, 1189–1195.CrossRefGoogle ScholarPubMed
Langerhans, R. B. (2006). Evolutionary consequences of predation: avoidance, escape, reproduction, and diversification. In Predation in Organisms: a Distinct Phenomenon (ed. Elewa, A. M. T.), pp. 177–220. Springer-Verlag, Heidelberg, Germany.Google Scholar
Marcogliese, D. J., Dumont, P., Gendron, A. D., Mailhot, Y., Bergeron, E. and McLaughlin, J. D. (2001). Spatial and temporal variation in abundance of Diplostomum spp. in walleye (Stizostedion vitreum) and white suckers (Catostomus commersoni) from the St. Lawrence River. Canadian Journal of Zoology 79, 355–369.CrossRefGoogle Scholar
Maure, F., Brodeur, J., Ponlet, N., Doyon, J., Firlej, A., Elguero, E. and Thomas, F. (2011). The cost of a bodyguard. Biology Letters 7, 843–846.CrossRefGoogle ScholarPubMed
Mikheev, V. N., Pasternak, A. F., Taskinen, J. and Valtonen, E. T. (2010). Parasite-induced aggression and impaired contest ability in a fish host. Parasites and Vectors 3, 17.CrossRefGoogle Scholar
Mirza, R. S. and Chivers, D. P. (2001). Are chemical alarm cues conserved within salmonid fishes? Journal of Chemical Ecology 27, 1641–1655.CrossRefGoogle ScholarPubMed
Ng, W. L. and Bassler, B. L. (2009). Bacterial quorum-sensing network architectures. Annual Review of Genetics 43, 197–222.CrossRefGoogle ScholarPubMed
Parker, G. A., Ball, M. A., Chubb, J. C., Hammerschmidt, K. and Milinski, M. (2009). When should a trophically transmitted parasite manipulate its host? Evolution 63, 448–458.CrossRefGoogle ScholarPubMed
Poulin, R. (1994). The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology 109, S109–S118.CrossRefGoogle ScholarPubMed
Poulin, R. (2010). Parasite manipulation of host behaviour: an update and frequently asked questions. Advances in the Study of Behavior 41, 151–186.CrossRefGoogle Scholar
Poulin, R., Fredensborg, B. L., Hansen, E. and Leung, T. L. F. (2005). The true cost of host manipulation by parasites. Behavioural Processes 68, 241–244.CrossRefGoogle ScholarPubMed
R Core Team (2015). R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.Google Scholar
Saldanha, I., Leung, T. L. F. and Poulin, R. (2009). Causes of intraspecific variation in body size among trematode metacercariae. Journal of Helminthology 83, 289–293.CrossRefGoogle ScholarPubMed
Sandland, G. T. and Goater, C. P. (2000). Development and intensity-dependence of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas). Journal of Parasitology 86, 1056–1060.CrossRefGoogle ScholarPubMed
Seppälä, O., Karvonen, A. and Valtonen, E. T. (2004). Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke–fish interaction. Animal Behaviour 68, 257–263.CrossRefGoogle Scholar
Seppälä, O., Karvonen, A. and Valtonen, E. T. (2005). Manipulation of fish host by eye flukes in relation to cataract formation and parasite infectivity. Animal Behaviour 70, 889–894.CrossRefGoogle Scholar
Seppälä, O., Karvonen, A. and Valtonen, E. T. (2008 a). Shoaling behavior of fish under parasitism and predation risk. Animal Behaviour 75, 145–150.CrossRefGoogle Scholar
Seppälä, O., Valtonen, E. T. and Benesh, D. P. (2008 b). Host manipulation by parasites in the world of dead-end predators: adaptation to enhance transmission? Proceedings of the Royal Society of London B 275, 1611–1615.Google ScholarPubMed
Seppälä, O., Karvonen, A. and Valtonen, E. T. (2012). Behavioural mechanisms underlying ‘specific’ host manipulation by a trophically transmitted parasite. Evolutionary Ecology Research 14, 73–81.Google Scholar
Sokolov, S. G. (2010). Parasites of underyearling kamchatka mykiss Parasalmo mykiss mykiss (Osteichithyes: Salmonidae) in the Utkholok River (North-Western Kamchatka). Parazitologiia 44, 336–342 (in Russian).Google ScholarPubMed
Sovová, T., Boyle, D., Sloman, K. A., Pérez, C. V. and Handy, R. H. (2014). Impaired behavioural response to alarm substance in rainbow trout exposed to copper nanoparticles. Aquatic Toxicology 152, 195–204.CrossRefGoogle ScholarPubMed
Sweeting, R. (1974). Investigations into natural and experimental infections of freshwater fish by the common eye-fluke Diplostomum spathaceum Rud. Parasitology 69, 291–300.CrossRefGoogle ScholarPubMed
Thomas, F., Adamo, S. and Moore, J. 2005. Parasitic manipulation: where are we and where should we go? Behavioural Processes 68, 185–199.CrossRefGoogle ScholarPubMed
Turner, P. E. and Chao, L. (1999). Prisoners’ dilemma in an RNA virus. Nature 398, 441–443.CrossRefGoogle Scholar
Valtonen, E. T. and Gibson, D. I. (1997). Aspects of the biology of diplostomid metacercarial (Digenea) populations occurring in fishes in different localities of northern Finland. Annales Zoologici Fennici 34, 47–59.Google Scholar
Vickery, W. L. and Poulin, R. (2010). The evolution of host manipulation by parasites: a game theory analysis. Evolutionary Ecology 24, 773–788.CrossRefGoogle Scholar
Vik, J. O., Borgstrom, R. and Skaala, O. (2001). Cannibalism governing mortality of juvenile brown trout, Salmo trutta, in a regulated stream. Regulated Rivers-Research & Management 17, 583–594.CrossRefGoogle Scholar
Voutilainen, A., Huuskonen, H. and Taskinen, J. (2010). Penetration and migration success of Diplostomum spp. cercariae in arctic charr. Journal of Parasitology 96, 232–235.CrossRefGoogle ScholarPubMed
Vyas, A., Kim, S. K. and Sapolsky, R. M. (2007). The effects of Toxoplasma infection on rodent behavior are dependent on dose of the stimulus. Neuroscience 148, 342–348.CrossRefGoogle ScholarPubMed
Warkentin, K. M. (1995). Adaptive plasticity in hatching age: a response to predation risk trade-offs. Proceedings of the National Academy of Sciences of the United States of America 92, 3507–3510.CrossRefGoogle ScholarPubMed
Wedekind, C. (2002). Induced hatching to avoid infectious egg disease in whitefish. Current Biology 12, 69–71.CrossRefGoogle ScholarPubMed
Wegner, K. M., Kalbe, M. and Reusch, T. B. H. (2007). Innate versus adaptive immunity in sticklebacks: evidence for trade-offs from a selection experiment. Evolutionary Ecology 21, 473–483.CrossRefGoogle Scholar
Weinersmith, K. L., Warinner, C. B., Tan, V., Harris, D. J., Mora, A. B., Kuris, A. M., Lafferty, K. D. and Hechinger, R. F. (2014). A lack of crowding? Body size does not decrease with density for two behavior-manipulating parasites. Integrative and Comparative Biology 54, 184–192.CrossRefGoogle Scholar
Weinreich, F., Benesh, D. P. and Milinski, M. (2013). Suppression of predation on the intermediate host by two trophically-transmitted parasites when uninfective. Parasitology 140, 129–135.CrossRefGoogle ScholarPubMed