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Decay of similarity with host phylogenetic distance in parasite faunas

Published online by Cambridge University Press:  23 October 2009

R. POULIN*
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56, Dunedin9054, New Zealand
*
*Corresponding author. Tel: +64 3 479 7983. Fax: +64 3 479 7584. E-mail: [email protected]

Summary

Exponential decay in community similarity as a function of distance is a ubiquitous phenomenon in biogeography. Thus, for parasite communities, pairwise similarity decreases with increasing geographical distance between host populations. This biogeographical rule should also apply along other dimensions characterizing the separation between communities. Since host-switching and phylogenetic affinities among host species affect the evolution of parasite faunas across host phylogenetic space the same way as dispersal and environmental gradients affect the assembly of local communities in geographical space, an exponential decay in similarity of parasite faunas with increasing host phylogenetic distance should be observed. This prediction is tested using data on metazoan parasites of 45 species of Canadian freshwater fishes belonging to 5 families. Across all host species, pairwise similarity in the composition of parasite faunas decayed exponentially, though not strongly, with increasing phylogenetic distance between hosts (measured as the number of substitutions per site along DNA sequences). A meta-analysis of correlations computed for separate fish families indicates only a very weak overall relationship. Data distribution indicates that phylogenetically close host species tend to share many of their parasites, while phylogenetically distant hosts have roughly equal chances of harbouring very similar or very dissimilar parasite faunas. The same pattern was seen when monogenean and trematode parasites were analysed separately, whereas no significant decay was observed for cestodes or nematodes, suggesting different patterns of host-switching and parasite colonization among these taxa. The results show that similarity in species composition decreases, though weakly, with increasing distance in the same manner in phylogenetic space as it does in geographical space.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Brooks, D. R. (1988). Macroevolutionary comparisons of host and parasite phylogenies. Annual Review of Ecology and Systematics 19, 235259.CrossRefGoogle Scholar
Brooks, D. R. and McLennan, D. A. (1993). Parascript: Parasites and the Language of Evolution. Smithsonian Institution Press, Washington, DC, USA.Google Scholar
Brouat, C. and Duplantier, J. M. (2007). Host habitat patchiness and the distance decay of similarity among gastro-intestinal nematode communities in two species of Mastomys (southeastern Senegal). Oecologia 152, 715720.CrossRefGoogle ScholarPubMed
Carney, J. P. and Dick, T. A. (2000). The historical ecology of yellow perch (Perca flavescens [Mitchill]) and their parasites. Journal of Biogeography 27, 13371347.CrossRefGoogle Scholar
Clayton, D. H. and Johnson, K. P. (2003). Linking coevolutionary history to ecological process: doves and lice. Evolution 57, 23352341.Google ScholarPubMed
Colwell, R. K. (2006). EstimateS: Statistical Estimation of Species Richness and Shared Species from Samples, version 8 (http://purl.oclc.org/estimates).Google Scholar
Desdevises, Y., Morand, S., Jousson, O. and Legendre, P. (2002). Coevolution between Lamellodiscus (Monogenea: Diplectanidae) and Sparidae (Teleostei): the study of a complex host-parasite system. Evolution 56, 24592471.Google Scholar
Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist 125, 115.CrossRefGoogle Scholar
Gotelli, N. J. and Entsminger, G. L. (2004). EcoSim: Null Models Software for Ecology, version 7. Acquired Intelligence Inc. & Kesey-Bear, Jericho, VT, USA. (http://garyentsminger.com/ecosim/index.htm).Google Scholar
Gregory, R. D. (1990). Parasites and host geographic range as illustrated by waterfowl. Functional Ecology 4, 645654.CrossRefGoogle Scholar
Hafner, M. S. and Nadler, S. A. (1988). Phylogenetic trees support the coevolution of parasites and their hosts. Nature, London 332, 258259.CrossRefGoogle ScholarPubMed
Hardman, M. (2004). The phylogenetic relationships among Noturus catfishes (Siluriformes: Ictaluridae) as inferred from mitochondrial gene cytochrome b and nuclear recombination activating gene 2. Molecular Phylogenetics and Evolution 30, 395408.CrossRefGoogle ScholarPubMed
Hardman, M. and Page, L. M. (2003). Phylogenetic relationships among bullhead catfishes of the genus Ameiurus (Siluriformes: Ictaluridae). Copeia 2003, 2033.CrossRefGoogle Scholar
Harvey, P. H. and Pagel, M. D. (1991). The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Huyse, T. and Volckaert, F. A. M. (2005). Comparing host and parasite phylogenies: Gyrodactylus flatworms jumping from goby to goby. Systematic Biology 54, 710718.CrossRefGoogle ScholarPubMed
Lambert, A. and El Gharbi, S. (1995). Monogenean host specificity as a biological and taxonomic indicator for fish. Biological Conservation 72, 227235.CrossRefGoogle Scholar
Magurran, A. E. (1988). Ecological Diversity and its Measurement. Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Manly, B. F. J. (1997). Randomization, Bootstrap and Monte Carlo Methods in Biology, 2nd edition. Chapman and Hall, London, UK.Google Scholar
Margolis, L. and Arthur, J. R. (1979). Synopsis of the Parasites of Fishes of Canada. Bulletin of the Fisheries Research Board of Canada no. 199, Department of Fisheries and Oceans Canada, Ottawa, Canada.Google Scholar
McDonald, T. E. and Margolis, L. (1995). Synopsis of the Parasites of Fishes of Canada: Supplement (1978–1993). Canadian Special Publication of Fisheries and Aquatic Sciences no. 122, National Research Council of Canada, Ottawa, Canada.Google Scholar
Morlon, H., Chuyong, G., Condit, R., Hubbell, S., Kenfack, D., Thomas, D., Valencia, R. and Green, J. L. (2008). A general framework for the distance-decay of similarity in ecological communities. Ecology Letters 11, 904917.CrossRefGoogle ScholarPubMed
Near, T. J., Bolnick, D. I. and Wainwright, P. C. (2004). Investigating phylogenetic relationships of sunfishes and black basses (Actinopterygii: Centrarchidae) using DNA sequences from mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution 32, 344357.Google ScholarPubMed
Nekola, J. C. and White, P. S. (1999). The distance decay of similarity in biogeography and ecology. Journal of Biogeography 26, 867878.CrossRefGoogle Scholar
Nunn, C. L., Altizer, S., Jones, K. E. and Sechrest, W. (2003). Comparative tests of parasite species richness in primates. American Naturalist 162, 597614.CrossRefGoogle ScholarPubMed
Oliva, M. E. and González, M. T. (2005). The decay of similarity over geographical distance in parasite communities of marine fishes. Journal of Biogeography 32, 13271332.CrossRefGoogle Scholar
Pérez-del-Olmo, A., Fernández, M., Raga, J. A., Kostadinova, A. and Morand, S. (2009). Not everything is everywhere: the distance decay of similarity in a marine host-parasite system. Journal of Biogeography 36, 200209.CrossRefGoogle Scholar
Poulin, R. (1992). Determinants of host-specificity in parasites of freshwater fishes. International Journal for Parasitology 22, 753758.CrossRefGoogle ScholarPubMed
Poulin, R. (1995). Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecological Monographs 65, 283302.CrossRefGoogle Scholar
Poulin, R. (1997). Species richness of parasite assemblages: evolution and patterns. Annual Review of Ecology and Systematics 28, 341358.CrossRefGoogle Scholar
Poulin, R. (1998). Comparison of three estimators of species richness in parasite component communities. Journal of Parasitology 84, 485490.CrossRefGoogle ScholarPubMed
Poulin, R. (2003). The decay of similarity with geographical distance in parasite communities of vertebrate hosts. Journal of Biogeography 30, 16091615.CrossRefGoogle Scholar
Poulin, R. (2004). Parasite species richness in New Zealand fishes: a grossly underestimated component of biodiversity? Diversity and Distributions 10, 3137.CrossRefGoogle Scholar
Poulin, R. (2006). Variation in infection parameters among populations within parasite species: intrinsic properties versus local factors. International Journal for Parasitology 36, 877885.CrossRefGoogle ScholarPubMed
Poulin, R. and Keeney, D. B. (2008). Host specificity under molecular and experimental scrutiny. Trends in Parasitology 24, 2428.CrossRefGoogle ScholarPubMed
Poulin, R. and Mouillot, D. (2003). Parasite specialization from a phylogenetic perspective: a new index of host specificity. Parasitology 126, 473480.CrossRefGoogle ScholarPubMed
Scott, W. B. and Crossman, E. J. (1973). Freshwater Fishes of Canada. Bulletin of the Fisheries Research Board of Canada no. 184, Department of Fisheries and Oceans Canada, Ottawa, Canada.Google Scholar
Seifertova, M., Vyskocilova, M., Morand, S. and Simkova, A. (2008). Metazoan parasites of freshwater cyprinid fish (Leuciscus cephalus): testing biogeographical hypotheses of species diversity. Parasitology 135, 14171435.CrossRefGoogle ScholarPubMed
Simons, A. M., Berendzen, P. B. and Mayden, R. L. (2003). Molecular systematics of North American phoxinin genera (Actinopterygii: Cyprinidae) inferred from mitochondrial 12S and 16S ribosomal RNA sequences. Zoological Journal of the Linnean Society 139, 6380.CrossRefGoogle Scholar
Skerikova, A., Hypsa, V. and Scholz, T. (2001). Phylogenetic analysis of European species of Proteocephalus (Cestoda: Proteocephalidea): compatibility of molecular and morphological data, and parasite-host coevolution. International Journal for Parasitology 31, 11211128.CrossRefGoogle ScholarPubMed
Sloss, B. L., Billington, N. and Burr, B. M. (2004). A molecular phylogeny of the Percidae (Teleostei, Perciformes) based on mitochondrial DNA sequence. Molecular Phylogenetics and Evolution 32, 545562.CrossRefGoogle ScholarPubMed
Soininen, J., McDonald, R. and Hillebrand, H. (2007). The distance decay of similarity in ecological communities. Ecography 30, 3–12.CrossRefGoogle Scholar
Steinitz, O., Heller, J., Tsoar, A., Rotem, D. and Kadmon, R. (2006). Environment, dispersal and patterns of species similarity. Journal of Biogeography 33, 10441054.CrossRefGoogle Scholar
Sun, Y. H., Xie, C. X., Wang, W. M., Liu, S. Y., Treer, T. and Chang, M. M. (2007). The genetic variation and biogeography of catostomid fishes based on mitochondrial and nucleic DNA sequences. Journal of Fish Biology 70 (Suppl. C), 291309.CrossRefGoogle Scholar
Thieltges, D. W., Ferguson, M. A. D., Jones, C. S., Krakau, M., de Montaudouin, X., Noble, L. R., Reise, K. and Poulin, R. (2009). Distance decay of similarity among parasite communities of three marine invertebrate hosts. Oecologia 160, 163173.CrossRefGoogle ScholarPubMed
Vinarski, M. V., Korallo, N. P., Krasnov, B. R., Shenbrot, G. I. and Poulin, R. (2007). Decay of similarity of gamasid mite assemblages parasitic on Palaearctic small mammals: geographic distance, host species composition or environment? Journal of Biogeography 34, 16911700.CrossRefGoogle Scholar
Walther, B. A., Cotgreave, P., Price, R. D., Gregory, R. D. and Clayton, D. H. (1995). Sampling effort and parasite species richness. Parasitology Today 11, 306310.CrossRefGoogle ScholarPubMed
Wright, D. H., Patterson, B. D., Mikkelson, G. M., Cutler, A. and Atmar, W. (1998). A comparative analysis of nested subset patterns of species composition. Oecologia 113, 120.CrossRefGoogle Scholar