Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-18T14:19:50.189Z Has data issue: false hasContentIssue false

Experimental test of host specificity in a behaviour-modifying trematode

Published online by Cambridge University Press:  23 September 2015

R. N. HERNANDEZ
Affiliation:
Department of Biology and Center for Subtropical Studies, The University of Texas-Pan American, 1201 W University Drive, Edinburg, Texas 78539, USA
B. L. FREDENSBORG*
Affiliation:
Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark
*
*Corresponding author. Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark. E-mail: [email protected]

Summary

Host behavioural modification by parasites is a common and well-documented phenomenon. However, knowledge on the complexity and specificity of the underlying mechanisms is limited, and host specificity among manipulating parasites has rarely been experimentally verified. We tested the hypothesis that the ability to infect and manipulate host behaviour is restricted to phylogenetically closely related hosts. Our model system consisted of the brain-encysting trematode Euhaplorchis sp. A and six potential fish intermediate hosts from the Order Cyprinodontiformes. Five co-occurring cyprinids were examined for naturally acquired brain infections. Then we selected three species representing three levels of taxonomic relatedness to a known host to experimentally evaluate their susceptibility to infection, and the effect of infection status on behaviours presumably linked to increased trophic transmission. We found natural brain infections of Euhaplorchis sp. A metacercariae in three cyprinids in the shallow sublittoral zone. Of the three experimentally exposed species, Fundulus grandis and Poecilia latipinna acquired infections and displayed an elevated number of conspicuous behaviours in comparison with uninfected controls. Euhaplorchis sp. A was able to infect and manipulate fish belonging to two different families, suggesting that ecological similarity rather than genetic relatedness determines host range in this species.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

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. (2002). Modulating the modulators: parasites, neuromodulators and host behavioral change. Brain, Behavior and Evolution 60, 370377.Google Scholar
Antonovics, J., Boots, M., Ebert, D., Koskella, B., Poss, M. and Sadd, B. M. (2012). The origin of specificity by means of natural selection: evolved and nonhost resistance in host–pathogen interactions. Evolution 67, 19.CrossRefGoogle ScholarPubMed
de Bekker, C., Quevillon, L. E., Smith, P. B., Fleming, K. R., Ghosh, D., Patterson, A. D. and Hughes, D. (2014). Species-specific ant brain manipulation by a specialized fungal parasite. BMC Evolutionary Biology 14, 166.Google Scholar
Desneux, N., Blahnik, R., Delebecque, C. J. and Heimpel, G. E. (2012). Host phylogeny and specialization in parasitoids. Ecology Letters 15, 453460.Google Scholar
Ebert, D. (1998). Experimental evolution of parasites. Science 282, 14321435.Google Scholar
Fredensborg, B. L. (2014). Predictors of host specificity among behavior-manipulating parasites. Integrative and Comparative Biology 54, 149158.Google Scholar
Fredensborg, B. L. and Longoria, A. N. (2012). Increased surfacing behavior in longnose killifish infected by brain-encysting trematode. Journal of Parasitology 98, 899903.Google Scholar
Futuyma, D. J. and Moreno, G. (1988). The evolution of ecological specialization. Annual Reviews of Ecology and Systematics 19, 207233.Google Scholar
Ghedotti, M. J. and Davis, M. P. (2013). Phylogeny, Classification, and evolution of salinity tolerance of the North American topminnows and killifishes, Family Fundulidae (Teleostei: Cyprinodontiformes). Fieldiana: Life and Earth Sciences 7, 165.Google Scholar
Haas, W., Granzer, M. and Brockelman, C. R. (1990). Opisthorchis viverrini: finding and recognition of the fish host by the cercariae. Experimental Parasitology 71, 422431.Google Scholar
Haas, W., Wulff, C., Grabe, K., Meyer, V. and Haeberlein, S. (2007). Navigation within host tissues: cues for orientation of Diplostomum spathaceum (Trematoda) in fish towards veins, head and eye. Parasitology 134, 10131023.Google Scholar
Helluy, S. (2013). Parasite-induced alterations of sensorimotor pathways in gammarids: collateral damage of neuroinflammation? Journal of Experimental Biology 216, 6777.Google Scholar
Helluy, S. and Thomas, F. (2003). Effects of Microphallus papillorobustus (Platyhelminthes: Trematoda) serotonertic immunoreactivity and neuronal architecture in the brain of Gammarus insensibilis (Crustacea: Amphipoda). Proceedings of the Royal Society of London Series B 270, 563568.Google Scholar
Helluy, S. and Thomas, F. (2010). Parasitic manipulation and neuroinflammation: evidence from the system Microphallus papillorobustus (Trematoda) – Gammarus (Crustacea). Parasites and Vectors 3, 38.Google Scholar
Hendrickson, G. L. (1979). Ornithodiplostomum ptychocheilus: migration to the brain of the fish intermediate host, Pimephales promelas . Experimental Parasitology 48, 245248.Google Scholar
Hurd, H. (1990). Physiological and behavioural interactions between parasites and invertebrate hosts. Advances in Parasitology 29, 271318.Google Scholar
Lafferty, K. D. and Morris, A. K. (1996). Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77, 13901397.Google Scholar
Lafferty, K. D. and Shaw, J. C. (2013). Comparing mechanisms of host manipulation across host and parasite taxa. Journal of Experimental Biology 216, 5666.Google Scholar
Lafferty, K. D., Dobson, A. P. and Kuris, A. M. (2006). Parasites dominate foodweb links. Proceedings of the National Academy of Sciences of the USA 103, 1121111216.Google Scholar
Lefevre, T., Lebarbenchon, C., Gautier-Clerc, M., Misse, D., Poulin, R. and Thomas, F. (2009). The ecological significance of manipulative parasites. Trends in Ecology and Evolution 24, 4148.Google Scholar
Locke, S. A., McLaughlin, D. and Marcogliese, D. J. (2010). DNA barcodes show cryptic diversity and a potential physiological basis for host specificity among Diplostomoidea (Platyhelminthes: Digenea) parasitizing freshwater fishes in the St. Lawrence River, Canada. Molecular Ecology 19, 28132827.Google Scholar
Maier, S. F. and Watkins, L. R. (1999). Bidirectional communication between the brain and the immune system: implications for behaviour. Animal Behaviour 57, 741751.Google Scholar
Matisz, C., Goater, C. P. and Bray, D. (2010 a). Density and maturation of rodlet cells in brain tissue of fathead minnows (Pimephales promelas) exposed to trematode cercariae. International Journal for Parasitology 40, 307312.Google Scholar
Matisz, C., Goater, C. P. and Bray, D. (2010 b). Migration and site selection of Ornithodiplostomum ptychocheilus (Trematoda: Digenea) metacercariae in the brain of fathead minnows (Pimephales promelas). Parasitology 137, 719731.Google Scholar
McNeff, L. L. (1978). Marine cercariae from Cerithidea pliculosa Menke from Dauphin Island, Alabama; life cycles of heterophyid and opistorchiid Digenea from Cerithidea Swainson from the Eastern Gulf of Mexico. M.S. thesis. University of Alabama, Mobile, Alabama, 124 p.Google Scholar
Mollentze, N., Biek, R. and Streicker, D. G. (2014). The role of viral evolution in rabies host shifts and emergence. Current Opinion in Virology 8, 6872.Google Scholar
Moore, J. (2002). Parasites and the Behavior of Animals. Oxford University Press, Oxford, UK.Google Scholar
Moore, J. and Gotelli, N. J. (1996). Evolutionary patterns of altered behavior and susceptibility in parasitized hosts. Evolution 50, 807819.Google Scholar
Mossner, R. and Lesch, K.-P. (1998). Role of serotonin in the immune system and in neuroimmune interactions. Brain, Behavior, and Immunity 12, 249271.Google Scholar
Perlman, S. J. and Jaenike, J. (2003). Infection success in novel hosts: an experimental and phylogenetic study of Drosophila-parasitic nematodes. Evolution 57, 544557.Google Scholar
Perrot-Minnot, M.-J. and Cezilly, F. (2013). Investigating neuromodulatory systems underlying parasitic manipulation: concepts, limitations and prospects. Journal of Experimental Biology 216, 134141.Google Scholar
Poulin, R. (1992). Determinants of host-specificity in parasites of freshwater fishes. International Journal for Parasitology 22, 753758.Google Scholar
Poulin, R. (2005). Relative infection levels and taxonomic distances among the host species used by a parasite: insights into parasite specialization. Parasitology 130, 109115.Google Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton University Press, Princeton, USA.Google Scholar
Poulin, R. and Keeney, D. B. (2008). Host specificity under molecular and experimental scrutiny. Trends in Parasitology 24, 2428.Google Scholar
Schmid-Hempel, P. (2011). Evolutionary Parasitology. Oxford University Press, Oxford, UK.Google Scholar
Schneider, G. and Hohorst, W. (1971). Migration of metacercariae of Dicrocoelium-dendriticum in ants. Naturwissenschaften 58, 327328.Google Scholar
Shaw, J. C. and Overli, O. (2012). Brain-encysting trematodes and altered monoamine activity in naturally infected killifish Fundulus parvipinnis . Journal of Fish Biology 81, 22132222.Google Scholar
Shaw, J. C., Korzan, W. J., Carpenter, R. E., Kuris, A. M., Lafferty, K. D., Summers, C. H. and Overli, O. (2009). Parasite manipulation of brain monoamines in California killifish (Fundulus parvipinnis) by the trematode Euhaplorchis californiensis . Proceedings of the Royal Society of London B 276, 11371146.Google Scholar
Shaw, J. C., Hechinger, R. F., Lafferty, K. D. and Kuris, A. M. (2010). Ecology of the brain trematode Euhaplorchis californiensis and its host, the California killifish (Fundulus parvipinnis). Journal of Parasitology 96, 482490.CrossRefGoogle ScholarPubMed
Smith, N. F. (2001). Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts. Oecologia 127, 115122.Google Scholar
Straub, C. S., Ives, A. R. and Gratton, C. (2011). Evidence for a trade-off between host-range breadth and host-use efficiency in aphid parasitoids. American Naturalist 177, 389395.Google Scholar
Sukhdeo, M. V. K. and Sukhdeo, S. C. (2004). Trematode behaviours and the perceptual worlds of parasites. Canadian Journal of Zoology 82, 292315.Google Scholar
Ward, S. A. (1992). Assessing functional explanations of host-specificity. American Naturalist 139, 883891.Google Scholar
Webster, J. P. (1994). Prevalence and transmission of Toxoplasma gondii in wild brown rats, Rattus norvegicus . Parasitology 108, 407411.Google Scholar
Webster, J. P. (2001). Rats, cats, people and parasites: the impact of latent toxoplasmosis on behavior. Microbes and Infection 3, 10371045.Google Scholar
Winberg, S. and Nilsson, G. E. (1993). Roles of brain monoamine neurotransmitters in agonistic behavior and stress reactions, with particular reference to fish. Comparative Biochemistry and Physiology C 106, 597614.Google Scholar