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Parasites pitched against nature: Pitch Lake water protects guppies (Poecilia reticulata) from microbial and gyrodactylid infections

  • BETTINA SCHELKLE (a1), RYAN S. MOHAMMED (a2), MICHAEL P. COOGAN (a3), MARK McMULLAN (a4), EMMA L. GILLINGHAM (a1), COCK VAN OOSTERHOUT (a4) and JOANNE CABLE (a1)...
Summary

The enemy release hypothesis proposes that in parasite depleted habitats, populations will experience relaxed selection and become more susceptible (or less tolerant) to pathogenic infections. Here, we focus on a population of guppies (Poecilia reticulata) that are found in an extreme environment (the Pitch Lake, Trinidad) and examine whether this habitat represents a refuge from parasites. We investigated the efficacy of pitch in preventing microbial infections in Pitch Lake guppies, by exposing them to dechlorinated water, and reducing gyrodactylid infections on non-Pitch Lake guppies by transferring them to Pitch Lake water. We show that (i) natural prevalence of ectoparasites in the Pitch Lake is low compared to reference populations, (ii) Pitch Lake guppies transferred into aquarium water develop microbial infections, and (iii) experimentally infected guppies are cured of their gyrodactylid infections both by natural Pitch Lake water and by dechlorinated water containing solid pitch. These results indicate a role for Pitch Lake water in the defence of guppies from their parasites and suggest that Pitch Lake guppies might have undergone enemy release in this extreme environment. The Pitch Lake provides an ideal ecosystem for studies on immune gene evolution in the absence of parasites and long-term evolutionary implications of hydrocarbon pollution for vertebrates.

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Corresponding author
*Corresponding author: School of Biosciences, Cardiff University, Cardiff CF10 3AX, UK. Tel: + + 44 (0) 20 298 76022. Fax: +44 (0)29 208 74116. E-mail: cablej@cardiff.ac.uk
References
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Ali, D., Haque, S., Ramsubhag, A., Guinan, E. and Schulze-Makuch, D. (2006). Pitch lake, Trinidad: An analog site for hydrocarbon pools on Titan. Astrobiology 6, 176.
Amils Pibernat, R., Ellies-Evans, C. and Hinghofer-Szalkay, H. G. (2007). Life in Extreme Environments. Springer, Dordrecht, The Netherlands.
Bakke, T. A., Cable, J. and Harris, P. D. (2007). The biology of gyrodactylid monogeneans: the ‘Russian-doll killers’. Advances in Parasitology 64, 161376.
Barson, N. J., Cable, J. and van Oosterhout, C. (2009). Population genetic analysis of microsatellite variation of guppies (Poecilia reticulata) in Trinidad and Tobago: evidence for a dynamic source-sink metapopulation structure, founder events and population bottlenecks. Journal of Evolutionary Biology 22, 485497.
Burgess, P., McMahon, S. and Price, D. J. (2005). Conservation of Trinidad populations of Poecilia reticulata Peters, 1859 (Poeciliidae). In Viviparous Fishes (ed. Grier, H. and Uribe, M. C.), pp. 426434. New Life Publications, Homestead, FL, USA.
Cable, J. (2011). Poeciliid Parasites. In Ecology and Evolution of Poeciliid Fishes. (ed. Evans, J. P., Pilastro, A. and Schlupp, I.), pp. 8294. Chicago University Press, Chicago IL, USA.
Cable, J. and Harris, P. D. (2002). Gyrodactylid developmental biology: historical review, current status and future trends. International Journal for Parasitology 32, 255280.
Cable, J. and van Oosterhout, C. (2007). The impact of parasites on the life history evolution of guppies (Poecilia reticulata): the effects of host size on parasite virulence. International Journal for Parasitology 37, 14491458.
Coltrain, J. B., Harris, J. M., Cerling, T. E., Ehleringer, J. R., Dearing, M. D., Ward, J. and Allen, J. (2004). Rancho La Brea stable isotope biogeochemistry and its implications for the palaeoecology of late Pleistocene, coastal Southern California. Palaeogeography, Paleoclimatology and Palaeoecology 205, 199219.
Decaestecker, E., Gaba, S., Raeymaekers, J. A. M., Stocks, R., van Kerckhoven, L., Ebert, D. and De Meester, L. (2007). Host-parasite ‘Red Queen’ dynamics archived in pond sediment. Nature, London 450, 870873.
Dybdahl, M. F. and Lively, C. M. (1998). Host-Parasite Coevolution: Evidence for Rare Advantage and Time-Lagged Selection in a Natural Population. Evolution 52, 10571066.
Dunson, W. A., Swarts, F. and Silversti, M. (1977). Exceptional tolerance of low pH of some tropical blackwater fish. Journal of Experimental Zoology 201, 157162.
Fraser, B. A. and Neff, B. D. (2010). Parasite mediated homogenizing selection at the MHC in guppies. Genetica 138, 273278.
Harris, P. D., Cable, J., Tinsley, R. C. and Lazarus, C. M. (1999). Combined ribosomal DNA and morphological analysis of individual gyrodactylid monogeneans. Journal of Parasitology 85, 188191.
Kadavy, D. R., Plantz, B., Shaw, C. A., Myatt, J., Kokjohn, T. A. and Nickerson, K. W. (1999). Microbiology of the oil fly, Helaeomyia petrolei. Applied and Environmental Microbiology 65, 14771482.
Khan, R. A. (1990). Parasitism in marine fish after chronic exposure to petroleum hydrocarbons in the laboratory and to the Exxon Valdez oil spill. Bulletin of Environmental Contamination and Toxicology 44, 759763.
Kahn, R. A. and Kiceniuk, J. W. (1988). Effect of petroleum aromatic hydrocarbons on monogeneids parasitizing Atlantic cod, Gadus morhua L. Bulletin of Environmental Contamination and Toxicology 41, 94100.
Lawrence, N. S., Davis, J. and Compton, R. G. (2000). Analytical strategies for the detection of sulfide: a review. Talanta 52, 711784.
Lindström, K. M., Foufopoulos, J., Pärn, H. and Wikelski, M. (2004) Immunological investments reflect parasite abundance in island populations of Darwin's finches. Proceedings of the Royal Society of London, B 271, 15131519.
Liu, H. and Stiling, P. (2006). Testing the enemy release hypothesis: a review and meta-analysis. Biological Invasions 8, 15351545.
Lively, C. M. (1987). Evidence from a New-Zealand snail for the maintenance of sex by parasitism. Nature, London 328, 519521.
Lively, C. M. and Jokela, J. (2002). Temporal and spatial distributions of parasites and sex in a freshwater snail. Evolutionary Ecology Research 4, 219226.
Magurran, A. E. (2005). Evolutionary Ecology: The Trinidadian Guppy. Oxford Series in Ecology and Evolution, Oxford, UK.
Marković, S., Marković, Z., McCrindle, R. I. and Simonović, B. R. (2007). Kinetics of extraction of coal-tar pitch components with supercritical carbon dioxide. Chemical Papers 61, 4650.
Martin, C. H. and Johnson, S. (2007). A field test of the Hamilton-Zuk hypothesis in the Trinidadian guppy (Poecilia reticulata). Behavioral Ecology and Sociobiology 61, 18971909.
McMullan, M. (2010). Host-parasite co-evolution and genetic variation at the Major Histocompatibility Complex in the Trinidadian guppy (Poecilia reticulata). Ph.D. thesis, University of Hull, UK.
Pan, Z. and Raftery, D. (2007). Comparing and combining NMR spectroscopy and mass spectrometry in metabolomics. Analytical and Bioanalytical Chemistry 387, 525527.
Paterson, S., Vogwill, R., Buckling, A., Benmayor, R., Spiers, A. J., Thomson, N. R., Quail, M., Smith, F., Walker, D., Libberton, B., Fenton, A., Hall, N. and Brockhurst, M. A. (2010). Antagonistic coevolution accelerates molecular evolution. Nature, London 464, 275278.
Peckham, S. F. (1895). V. – On the Pitch Lake of Trinidad. Geological Magazine 2, 452458.
Ponnamperuma, C. and Pering, K. L. (1967). Aliphatic and alicyclic hydrocarbons isolated from Trinidad Lake asphalt. Geochimica et Cosmochimica Acta 31, 13501354.
Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton University Press, Princeton, NJ, USA.
R Development Core Team (2011). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria. URL: http://www.r-project.org.
Schelkle, B., Doetjes, R. and Cable, J. (2010). The salt myth revealed: treatment of gyrodactylid infections on ornamental guppies, Poecilia reticulata. Aquaculture 311, 7479.
Schelkle, B., Paladini, G., Shinn, A. P., King, S., Johnson, M., van Oosterhout, C., Mohammed, R. S. and Cable, J. (2011). Ieredactylus rivuli n. gen. et sp. (Monogenea: Gyrodactylidae) from Rivulus hartii (Cyprinodontiformes: Rivulidae) in Trinidad. Acta Parasitologica 56, 360370.
Schelkle, B., Shinn, A. P., Peeler, E. and Cable, J. (2009). Treatment of gyrodactylid infections in fish. Diseases of Aquatic Organisms 86, 6575.
Schulze-Makuch, D., Haque, S., Resendes de Sousa, Antonio M., Ali, D., Hosein, R., Song, Y. C., Yang, J., Zaikova, E., Beckles, D. M., Guinan, E., Lehto, H. J. and Hallam, S. J. (2010). Microbial Life in a Liquid Asphalt Desert. arXiv:1004·2047v1 [q-bio.GN]. Available online: http://arxiv.org/abs/1004·2047v1, accessed: 11 April 2012.
Scott, M. E. and Anderson, R. M. (1984). The population dynamics of Gyrodactylus bullatarudis (Monogenea) within laboratory populations of the fish host Poecilia reticulata. Parasitology 89, 159194.
Shephard, K. L. (1994). Functions for fish mucus. Reviews in Fish Biology and Fisheries 4, 401429.
Tezuka, A., Yamamoto, H., Yokoyama, J., van Oosterhout, C. and Kawata, M. (2011) The MC1R gene in the guppy (Poecilia reticulata): Genotypic and phenotypic polymorphisms. BMC Research Notes 4, 31.
Tobler, M., Schlupp, I., García de León, F. J., Glaubrecht, M. and Plath, M. (2007). Extreme habitats as refuge from parasite infections? Evidence from an extremophile fish. Acta Oecologica 31, 270275.
van Oosterhout, C., Harris, P. D. and Cable, J. (2003). Marked variation in parasite resistance between two wild populations of the Trinidadian guppy, Poecilia reticulata (Pisces: Poeciliidae). Biological Journal of the Linnean Society 79, 645651.
van Oosterhout, C., Mohammed, R. S., Hansen, H., Archard, G. A., McMullan, M., Weese, D. J. and Cable, J. (2007). Selection by parasites in spate conditions in a wild Trinidadian guppies (Poecilia reticulata). International Journal for Parasitology 37, 805812.
Willing, E. M., Bentzen, P., Hoffmann, M., van Oosterhout, C., Cable, J., Breden, F., Weigel, D. and Dreyer, C. (2010). Genome-wide single nucleotide polymorphisms reveal population history and adaptive divergence in wild guppies. Molecular Ecology 19, 968984.
Woolhouse, M. E. J., Webster, J. P., Domingo, E., Charlesworth, B. and Levin, B. R. (2002). Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nature Genetics 32, 569577.
World Health Organization Concise International Chemical Assessment Documents (2005). Asphalt (Bitumen). Available online: http://www.who.int/ipcs/publications/cicad/cicad59_rev_1.pdf. Accessed: 11 April 2012.
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Parasitology
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