Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-23T04:31:24.709Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  26 July 2012

BETTINA SCHELKLE ,
RYAN S. MOHAMMED ,
MICHAEL P. COOGAN ,
MARK McMULLAN ,
EMMA L. GILLINGHAM ,
COCK VAN OOSTERHOUT  and
JOANNE CABLE
BETTINA SCHELKLE
Affiliation:
School of Biosciences, Cardiff University, Cardiff CF10 3AX, UK
RYAN S. MOHAMMED
Affiliation:
Department of Life Sciences, University of the West Indies, St Augustine, Trinidad, West Indies
MICHAEL P. COOGAN
Affiliation:
School of Chemistry, Cardiff University, Cardiff CF10 3AT, UK
MARK McMULLAN
Affiliation:
School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK
EMMA L. GILLINGHAM
Affiliation:
School of Biosciences, Cardiff University, Cardiff CF10 3AX, UK
COCK VAN OOSTERHOUT
Affiliation:
School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK
JOANNE CABLE*
Affiliation:
School of Biosciences, Cardiff University, Cardiff CF10 3AX, UK
*
*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: [email protected]
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

antihelminthicasphaltPitch LakeGyrodactylusPoecilia reticulataenemy release
Type
Research Article
Information
Parasitology , Volume 139 , Issue 13 , November 2012 , pp. 1772 - 1779
Copyright
Copyright © Cambridge University Press 2012

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

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.Google Scholar
Amils Pibernat, R., Ellies-Evans, C. and Hinghofer-Szalkay, H. G. (2007). Life in Extreme Environments. Springer, Dordrecht, The Netherlands.CrossRefGoogle Scholar
Bakke, T. A., Cable, J. and Harris, P. D. (2007). The biology of gyrodactylid monogeneans: the ‘Russian-doll killers’. Advances in Parasitology 64, 161–376.CrossRefGoogle ScholarPubMed
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, 485–497.CrossRefGoogle ScholarPubMed
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. 426–434. New Life Publications, Homestead, FL, USA.Google Scholar
Cable, J. (2011). Poeciliid Parasites. In Ecology and Evolution of Poeciliid Fishes. (ed. Evans, J. P., Pilastro, A. and Schlupp, I.), pp. 82–94. Chicago University Press, Chicago IL, USA.Google Scholar
Cable, J. and Harris, P. D. (2002). Gyrodactylid developmental biology: historical review, current status and future trends. International Journal for Parasitology 32, 255–280.CrossRefGoogle ScholarPubMed
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, 1449–1458.CrossRefGoogle ScholarPubMed
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, 199–219.CrossRefGoogle Scholar
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, 870–873.CrossRefGoogle ScholarPubMed
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, 1057–1066.CrossRefGoogle Scholar
Dunson, W. A., Swarts, F. and Silversti, M. (1977). Exceptional tolerance of low pH of some tropical blackwater fish. Journal of Experimental Zoology 201, 157–162.CrossRefGoogle Scholar
Fraser, B. A. and Neff, B. D. (2010). Parasite mediated homogenizing selection at the MHC in guppies. Genetica 138, 273–278.CrossRefGoogle ScholarPubMed
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, 188–191.CrossRefGoogle ScholarPubMed
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, 1477–1482.CrossRefGoogle ScholarPubMed
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, 759–763.CrossRefGoogle Scholar
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, 94–100.CrossRefGoogle Scholar
Lawrence, N. S., Davis, J. and Compton, R. G. (2000). Analytical strategies for the detection of sulfide: a review. Talanta 52, 711–784.CrossRefGoogle ScholarPubMed
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, 1513–1519.CrossRefGoogle ScholarPubMed
Liu, H. and Stiling, P. (2006). Testing the enemy release hypothesis: a review and meta-analysis. Biological Invasions 8, 1535–1545.CrossRefGoogle Scholar
Lively, C. M. (1987). Evidence from a New-Zealand snail for the maintenance of sex by parasitism. Nature, London 328, 519–521.CrossRefGoogle Scholar
Lively, C. M. and Jokela, J. (2002). Temporal and spatial distributions of parasites and sex in a freshwater snail. Evolutionary Ecology Research 4, 219–226.Google Scholar
Magurran, A. E. (2005). Evolutionary Ecology: The Trinidadian Guppy. Oxford Series in Ecology and Evolution, Oxford, UK.CrossRefGoogle Scholar
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, 46–50.CrossRefGoogle Scholar
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, 1897–1909.CrossRefGoogle Scholar
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.Google Scholar
Pan, Z. and Raftery, D. (2007). Comparing and combining NMR spectroscopy and mass spectrometry in metabolomics. Analytical and Bioanalytical Chemistry 387, 525–527.CrossRefGoogle ScholarPubMed
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, 275–278.CrossRefGoogle ScholarPubMed
Peckham, S. F. (1895). V. – On the Pitch Lake of Trinidad. Geological Magazine 2, 452–458.CrossRefGoogle Scholar
Ponnamperuma, C. and Pering, K. L. (1967). Aliphatic and alicyclic hydrocarbons isolated from Trinidad Lake asphalt. Geochimica et Cosmochimica Acta 31, 1350–1354.CrossRefGoogle Scholar
Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton University Press, Princeton, NJ, USA.Google ScholarPubMed
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.Google Scholar
Schelkle, B., Doetjes, R. and Cable, J. (2010). The salt myth revealed: treatment of gyrodactylid infections on ornamental guppies, Poecilia reticulata. Aquaculture 311, 74–79.CrossRefGoogle Scholar
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, 360–370.CrossRefGoogle Scholar
Schelkle, B., Shinn, A. P., Peeler, E. and Cable, J. (2009). Treatment of gyrodactylid infections in fish. Diseases of Aquatic Organisms 86, 65–75.CrossRefGoogle ScholarPubMed
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.Google Scholar
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, 159–194.CrossRefGoogle ScholarPubMed
Shephard, K. L. (1994). Functions for fish mucus. Reviews in Fish Biology and Fisheries 4, 401–429.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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, 270–275.CrossRefGoogle Scholar
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, 645–651.CrossRefGoogle Scholar
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, 805–812.CrossRefGoogle Scholar
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, 968–984.CrossRefGoogle ScholarPubMed
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, 569–577.CrossRefGoogle ScholarPubMed
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.Google Scholar