Skip to main content
SpringerLink
Log in

The Evolution of Taxonomic Diversity in Helminth Assemblages of Mammalian Hosts

  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Several studies have searched for the key forces behind the diversification of parasite assemblages over evolutionary time. All of these studies have used parasite species richness as their measure of diversity, thus ignoring the relatedness among parasite species and the taxonomic structure of the assemblages. This information is essential, however, if we want to elucidate which processes have caused an assemblage of parasites to acquire new species. Here, we performed a comparative analysis across 110 species of mammalian hosts in which we evaluated the effects of four host traits (body mass, population density, geographic range, and basal metabolic rate) on the diversity of their assemblages of helminth endoparasites. As measures of diversity, we used parasite species richness, as well as the average taxonomic distinctness of the assemblage and its variance; the latter measures are based on the taxonomic distance between two parasite species, computed across all possible species pairs in an assemblage. Unlike parasite species richness, both the average taxonomic distinctness and its variance were unaffected by the number of hosts examined. These two measures of parasite diversity also proved highly repeatable among host populations of the same mammalian species; in contrast, parasite species richness was unreliable as a species character, as it varied as much within a host species than among different host species. Using phylogenetically independent contrasts, and correcting for potential confounding variables, we found that host population density correlated positively with parasite species richness. There were, however, no other relationships between any of the four host traits investigated and either of our measures of parasite diversity. The processes facilitating the taxonomic diversification of parasite assemblages thus remain unclear, but their elucidation will be necessary if we are to fully understand parasite evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Amin, O.M. (1985) Classification. In D.W.T. Crompton and B.B. Nickol (eds) Biology of the Acanthocephala. Cambridge University Press, Cambridge, pp. 27–72.

    Google Scholar 

  • Anderson, R.C. (2000) Nematodes Parasites of Vertebrates. 2nd edn. CABI Publishing, Wallingford, UK.

    Google Scholar 

  • Arneberg, P. (2002) Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25, 88–94.

    Article  Google Scholar 

  • Arneberg, P., Skorping, A. and Read, A.F. (1997) Is population density a species character? Comparative analyses of the nematode parasites of mammals. Oikos 80, 289–300.

    Google Scholar 

  • Bell, G. and Burt, A. (1991) The comparative biology of parasite species diversity: internal helminths of freshwater fish. J. Anim. Ecol. 60, 1047–1064.

    Google Scholar 

  • Beveridge, I., Chilton, N.B. and Spratt, D.M. (2002) The occurrence of species flocks in the nematode genus Cloacina (Strongyloidea: Cloacininae), parasitic in the stomachs of kangaroos and wallabies. Aust. J. Zool. 50, 597–620.

    Article  Google Scholar 

  • Bininda-Emonds, O.R.P., Gittleman, J.L. and Purvis, A. (1999) Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biol. Rev. 74, 143–175.

    Article  CAS  PubMed  Google Scholar 

  • Clarke, K.R. and Warwick, R.M. (1998) A taxonomic distinctness index and its statistical properties. J. Appl. Ecol. 35, 523–531.

    Article  Google Scholar 

  • Clarke, K.R. and Warwick, R.M. (1999) The taxonomic distinctness measure of biodiversity: weighting of step lengths between hierarchical levels. Mar. Ecol. Prog. Ser. 184, 21–29.

    Google Scholar 

  • Clarke, K.R. and Warwick, R.M. (2001) A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Mar. Ecol. Prog. Ser. 216, 265–278.

    Google Scholar 

  • Damuth, J. (1987) Interspecific allometry of population density in mammals and other animals: the independence of body mass and population energy-use. Biol. J. Linn. Soc. 31, 193–246.

    Google Scholar 

  • DeBry, R.W. and Sagel, R.M. (2001) Phylogeny of Rodentia (Mammalia) inferred from the nuclear-encoded gene IRBP. Mol. Phyl. Evol. 19, 290–301.

    Article  CAS  Google Scholar 

  • Diniz-Filho, J.A.F. and Torres, N.M. (2002) Phylogenetic comparative methods and the geographic range size - body size relationship in new world terrestrial Carnivora. Evol. Ecol. 16, 351–367.

    Article  Google Scholar 

  • Dobson, A.P. and Roberts, M. (1994) The population dynamics of parasitic helminth communities. Parasitology 109, S97-S108.

    Google Scholar 

  • Elgar, M.A. and Harvey, P.H. (1987) Basal metabolic rates in mammals: allometry, phylogeny and ecology. Funct. Ecol. 1, 25–36.

    Google Scholar 

  • Enquist, B.J., Haskell, J.P. and Tiffney, B.H. (2002) General patterns of taxonomic and biomass partitioning in extant and fossil plant communities. Nature 419, 610–613.

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein, J. (1985) Phylogenies and the comparative method. Am. Nat. 125, 1–15.

    Article  Google Scholar 

  • Garland, T. Jr., Harvey, P.H. and Ives, A.R. (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41, 18–32.

    Google Scholar 

  • Gibson, D.I., Jones, A. and Bray, R.A. (2002) Keys to the Trematoda, Vol 1. CABI Publishing, Wallingford, UK.

    Google Scholar 

  • Gotelli, N.J. (2002) Biodiversity in the scales. Nature 419, 575–576.

    Article  CAS  PubMed  Google Scholar 

  • Gregory, R.D. (1990) Parasites and host geographic range as illustrated by waterfowl. Funct. Ecol. 4, 645–654.

    Google Scholar 

  • Gregory, R.D., Keymer, A.E. and Harvey, P.H. (1991) Life history, ecology and parasite community structure in Soviet birds. Biol. J. Linn. Soc. 43, 249–262.

    Google Scholar 

  • Gregory, R.D., Keymer, A.E. and Harvey, P.H. (1996) Helminth parasite richness among vertebrates. Biodiv. Conserv. 5, 985–997.

    Article  Google Scholar 

  • Grzimek, B. (1990) Encyclopedia of Mammals, five volumes. McGraw-Hill, New York.

    Google Scholar 

  • Harkema, R. and Miller, G.C. (1964) Helminth parasites of the raccoon, Procyon lotor, in the Southeastern United States. J. Parasitol. 50, 60–66.

    CAS  PubMed  Google Scholar 

  • Harvey, P.H. and Pagel, M.D. (1991) The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford.

    Google Scholar 

  • Huston, M.A. (1992) Biological Diversity: The Coexistence of Species on Changing Landscapes. Cambridge University Press, Cambridge.

    Google Scholar 

  • Jones, K.E., Purvis, A., MacLarnon, A., Bininda-Emonds, O.R.P. and Simmons, N.B. (2002) A phylogenetic supertree of the bats (Mammalia: Chiroptera). Biol. Rev. 77, 223–259.

    Article  PubMed  Google Scholar 

  • Jordan, H.E. and Hayes, F.A. (1959) Gastrointestinal helminths of raccoons (Procyon lotor) from Ossabaw Island, Georgia. J. Parasitol. 45, 249–252.

    CAS  PubMed  Google Scholar 

  • Kennedy, C.R. and Bush, A.O. (1992) Species richness in helminth communities: the importance of multiple congeners. Parasitology 104, 189–197.

    PubMed  Google Scholar 

  • Kennedy, C.R. and Bush, A.O. (1994) The relationship between pattern and scale in parasite communities: a stranger in a strange land. Parasitology 109, 187–196.

    Article  PubMed  Google Scholar 

  • Khalil, L.F., Jones, A. and Bray, R.A. (1994) Keys to the Cestode Parasites of Vertebrates. CABI International, Wallingford, UK.

    Google Scholar 

  • Koteja, P. (1991) On the relation between basal and field metabolic rates in birds and mammals. Funct. Ecol. 5, 56–64.

    Google Scholar 

  • Kuris, A.M., Blaustein, A.R. and Alió, J.J. (1980) Hosts as islands. Am. Nat. 116, 570–586.

    Article  Google Scholar 

  • MacArthur, R.H. and Wilson, E.O. (1967) The Theory of Island Biogeography. Princeton University Press, Princeton.

  • Matthee, C.A., Burzlaff, J.D., Taylor, J.F. and Davis, S.K. (2001) Mining the mammalian genome for artiodactyl systematics. Syst. Biol. 50, 367–390.

    Article  CAS  PubMed  Google Scholar 

  • McKenna, M.C., Bell, S.K. and Simpson, G.G. (1997) Classification of Mammals Above the Species Level. Columbia University Press, New York.

    Google Scholar 

  • McNab, B.K. (1988) Complications inherent in scaling the basal rate of metabolism in mammals. Q. Rev. Biol. 63, 25–54.

    Article  CAS  PubMed  Google Scholar 

  • McNab, B.K. (1992) The comparative energetics of rigid endothermy: the Arvicolidae. J. Zool. 227, 585–606.

    Article  Google Scholar 

  • Morand, S. (2000) Wormy world: comparative tests of theoretical hypotheses on parasite species richness. In R. Poulin, S. Morand and A. Skorping (eds) Evolutionary Biology of Host-Parasite Relationships: Theory Meets Reality, Elsevier Science, Amsterdam, pp. 63–79.

    Google Scholar 

  • Morand, S. and Harvey, P.H. (2000) Mammalian metabolism, longevity and parasite species richness. Proc. Roy. Soc. London B 267, 1999–2003.

    Article  CAS  Google Scholar 

  • Morand, S. and Poulin, R. (1998) Density, body mass and parasite species richness of terrestrial mammals. Evol. Ecol. 12, 717–727.

    Article  Google Scholar 

  • Mouillot, D. and Poulin, R. (2004) Taxonomic partitioning shedding light on the diversification of parasite communities. Oikos 104, 205–207.

    Article  Google Scholar 

  • Murphy, W.J., Eizirik, E., Johnson, W.E., Zhang, Y.P., Ryder, O.A. and O’Brien, S.J. (2001) Molecular phylogenetics and the origins of placental mammals. Nature 409, 614–618.

    Article  CAS  PubMed  Google Scholar 

  • Page, R.D.M. (2003) Tangled Trees: Phylogeny, Cospeciation, and Coevolution. University of Chicago Press, Chicago.

    Google Scholar 

  • Paterson, A.M. and Gray, R.D. (1997) Host-parasite cospeciation, host switching, and missing the boat. In D.H. Clayton and J. Moore (eds) Host-Parasite Evolution: General Principles and Avian Models. Oxford University Press, Oxford, pp. 236–250.

    Google Scholar 

  • Poulin, R. (1995) Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecol. Monogr. 65, 283–302.

    Google Scholar 

  • Poulin, R. (1997) Species richness of parasite assemblages: evolution and patterns. Annu. Rev. Ecol. Syst. 28, 341–358.

    Article  Google Scholar 

  • Poulin, R. (1998) Evolutionary Ecology of Parasites: From Individuals to Communities. Chapman & Hall, London.

    Google Scholar 

  • Poulin, R. (1999) Speciation and diversification of parasite lineages: an analysis of congeneric parasite species in vertebrates. Evol. Ecol. 13, 455–467.

    Article  Google Scholar 

  • Poulin, R. and Morand, S. (2000) The diversity of parasites. Q. Rev. Biol. 75, 277–293.

    Article  CAS  PubMed  Google Scholar 

  • Poulin, R. and Mouillot, D. (2003) Host introductions and the geography of parasite taxonomic diversity. J. Biogeogr. 30, 837–845.

    Article  Google Scholar 

  • Purvis, A. and Hector, A. (2000) Getting the measure of biodiversity. Nature 405, 212–219.

    Article  CAS  PubMed  Google Scholar 

  • Purvis, A. and Rambaut, A. (1994) Comparative Analysis by Independent Contrasts, CAIC version 2.0. Oxford University, Oxford.

  • Roberts, M.G., Dobson, A.P., Arneberg, P., de Leo, G.A., Krecek, R.C., Manfredi, M.T., Lanfranchi, P. and Zaffaroni, E. (2002) Parasite community ecology and biodiversity. In P.J. Hudson, A. Rizzoli, B.T. Grenfell, H. Heesterbeek and A.P. Dobson (eds) The Ecology of Wildlife Diseases. Oxford University Press, Oxford, pp. 63–82.

    Google Scholar 

  • Rogers, S.I., Clarke, K.R. and Reynolds, J.D. (1999) The taxonomic distinctness of coastal bottom-dwelling fish communities of the North-east Atlantic. J. Anim. Ecol. 68, 769–782.

    Article  Google Scholar 

  • Rosenzweig, M.L. (1995) Species Diversity in Space and Time. Cambridge University Press, Cambridge.

    Google Scholar 

  • Schad, G.A. (1963) Niche diversification in a parasite species flock. Nature 198, 404–406.

    Google Scholar 

  • Shimatani, K. (2001) On the measurement of species diversity incorporating species differences. Oikos 93, 135–147.

    Article  Google Scholar 

  • Snyder, D.E. and Fitzgerald, P.R. (1985) Helminth parasites from Illinois raccoons (Procyon lotor). J. Parasitol. 71, 274–278.

    Google Scholar 

  • Sokal, R.R. and Rohlf, F.J. (1995) Biometry, 3rd edn. W. H. Freeman and Co., New York.

    Google Scholar 

  • Stanko, M., Miklisova, D., Goüy de Bellocq, J. and Morand, S. (2002) Mammal density and patterns of ectoparasite species richness and abundance. Oecologia 131, 289–295.

    Article  Google Scholar 

  • Tokeshi, M. (1999) Species Coexistence: Ecological and Evolutionary Perspectives. Blackwell Science, Oxford.

  • Walther, B.A., Cotgreave, P., Price, R.D., Gregory, R.D. and Clayton, D.H. (1995) Sampling effort and parasite species richness. Parasitol. Today 11, 306–310.

    Article  CAS  PubMed  Google Scholar 

  • Warwick, R.M. and Clarke, K.R. (2001) Practical measures of marine biodiversity based on relatedness of species. Oceanogr. Mar. Biol. Annu. Rev. 39, 207–231.

    Google Scholar 

  • Webb, C.O., Ackerly, D.D., McPeek, M.A. and Donoghue, M.J. (2002) Phylogenies and community ecology. Annu. Rev. Ecol. Syst. 33, 475–505.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand

    Robert Poulin

  2. UMR CNRS-UMII 5119 Ecosystèmes Lagunaires, Université Montpellier II, CC 093, 34095 Montpellier Cedex 5, France

    David Mouillot

Authors
  1. Robert Poulin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David Mouillot
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Poulin, R., Mouillot, D. The Evolution of Taxonomic Diversity in Helminth Assemblages of Mammalian Hosts. Evol Ecol 18, 231–247 (2004). https://doi.org/10.1023/B:EVEC.0000035029.55952.68

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:EVEC.0000035029.55952.68

Search

Navigation