Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-10T09:53:07.784Z Has data issue: false hasContentIssue false
  • English
  • Français

Incorporating parasite systematics in comparative analyses of variation in spleen mass and testes sizes of rodents

Published online by Cambridge University Press:  20 April 2011

NICOLAS PONLET ,
KITIPONG CHAISIRI ,
JULIEN CLAUDE  and
SERGE MORAND
NICOLAS PONLET
Affiliation:
Institut des Sciences de l'Evolution, UMR 5554/226 UM2-CNRS-IRD, CC65, Université de Montpellier 2, F-34095 Montpellier, France
KITIPONG CHAISIRI
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Bangkok 10400, Thailand
JULIEN CLAUDE
Affiliation:
Institut des Sciences de l'Evolution, UMR 5554/226 UM2-CNRS-IRD, CC65, Université de Montpellier 2, F-34095 Montpellier, France
SERGE MORAND*
Affiliation:
Institut des Sciences de l'Evolution, UMR 5554/226 UM2-CNRS-IRD, CC65, Université de Montpellier 2, F-34095 Montpellier, France
*
*Corresponding author: E-mail: serge.morand@univ-montp2.fr
Get access Rights & Permissions [Opens in a new window]

Summary

Parasite diversity is hypothesized to act on host life-history traits through investment in immunity. In order to incorporate the diversity of the parasite community that an individual host or a host species may face, two indices can be used: Taxonomic Species Richness and Taxonomic Entropy, where the taxonomic information is incorporated with the taxonomic weight. We tested whether these indices correlate with several morphological traits potentially implicated in immune defence and in reproduction, using data on gastrointestinal helminths and their rodent hosts sampled in Southeast Asia. We found no relationship between parasite diversity indices and either spleen mass or testes size at the intraspecific level, i.e. at the level of individuals. At the interspecific level, we found no relationship between the parasite diversity indices and testes size. However, we found that female spleen mass is significantly influenced by the specific species richness of parasites, whereas male spleen mass is influenced by individual mean parasite diversity indices. We concluded that female spleen mass may have evolved in response to gastrointestinal helminth pressure acting at species levels, while in males, the individual spleen mass could be constrained by other factors, such as the blood storage function of the spleen.

Keywords

RodentsSoutheast Asiagastrointestinal helminthsparasite species richnesstaxonomic indextaxonomic weightcomparative analysisspleen masstestes size
Type
Research Article
Information
Parasitology , Volume 138 , Special Issue 13: Systematics as a cornerstone of parasitology , November 2011 , pp. 1804 - 1814
Copyright
Copyright © Cambridge University Press 2011

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

Agnew, P., Koella, J. C. and Michalakis, Y. (2000). Host life history responses to parasitism. Microbes and Infections 2, 891–896.CrossRefGoogle ScholarPubMed
Bordes, F. and Morand, S. (2009). Parasite diversity: an overlooked metric of parasite pressures? Oikos 118, 801–806.CrossRefGoogle Scholar
Brooker, S. and Clements, A. C. A. (2009). Spatial heterogeneity of parasite co-infection: Determinants and geostatistical prediction at regional scales. International Journal for Parasitology 39, 591–597.CrossRefGoogle ScholarPubMed
Brown, C. R. and Brown, M. B. (2002). Spleen volume varies with colony size and parasite load in a colonial bird. Proceedings of the Royal Society of London Series B-Biological Sciences 269, 1367–1373.CrossRefGoogle Scholar
Calvete, C., Blanco-Aguiar, J. A., Virgos, E., Cabezas-Diaz, S. and Villafuerte, R. (2004). Spatial variation in helminth community structure in the red-legged partridge (Alectoris rufa L.): effects of definitive host density. Parasitology 129, 101–113.CrossRefGoogle Scholar
Chaisiri, K., Chaeychomsri, W., Siruntawineti, J., Ribas, A., Herbreteau, V. and Morand, S. (2010 b). Gastrointestinal helminth infection in Asian house rat (Rattus tanezumi) from Northern and Northeastern Thailand. Journal of Tropical Medicine and Parasitology 33, 29–35.Google Scholar
Chaisiri, K., Herbreteau, V., Ribas, A. and Morand, S. (2010 a). A study of great bandicoot (Bandicota indica) and their gastrointestinal helminths from northern and northeastern Thailand. Sciences Pages of the Year (Bangkok) 10, 2553.Google Scholar
Clarke, K. R. and Warwick, R. M. (2001). A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Marine Ecology – Progress Series 216, 265–278.CrossRefGoogle Scholar
Combes, C. (2001). Parasitism. The Ecology and Evolution of Intimate Interactions. Chicago: University of Chicago Press.Google Scholar
Corbin, E., Vicente, J., Martin-Hernando, M. P., Acevedo, P., Perez-Rodriguez, L. and Gortazar, C. (2008). Spleen mass as a measure of immune strength in mammals. Mammal Review 38, 108–115.CrossRefGoogle Scholar
Crivellato, E., Vacca, A. and Ribatti, D. (2004). Setting the stage: and anatomist's view of the immune system. Trends in Immunology 25, 210–217.CrossRefGoogle ScholarPubMed
Enstrom, D. A., Ketterson, E. D. and Nolan, V. (1997). Testosterone and mate choice in the dark-eyed junco. Animal Behaviour 54, 1135–1146.CrossRefGoogle Scholar
Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist 125, 1–15.CrossRefGoogle Scholar
Fernández-Llario, P., Parra, A., Cerrato, R. and Hermoso de Mendoza, J. (2004). Spleen size variations and reproduction in a Mediterranean population of wild boar (Sus scrofa). European Journal of Wildlife Research 50, 13–17.CrossRefGoogle Scholar
Folstad, I. and Karter, A. J. (1992). Parasites, bright males, and the immunocompetence handicap. American Naturalist 139, 603–622.CrossRefGoogle Scholar
French, S. S., DeNardo, D. F. and Moore, M. C. (2007). Trade-offs between the reproductive and immune systems: Facultative responses to resources or obligate responses to reproduction? American Naturalist 170, 79–89.CrossRefGoogle ScholarPubMed
Garamszegi, L. Z., Eens, M., Hurtrez-Bousses, S. and Møller, A. P. (2005). Testosterone, testes size, and mating success in birds: a comparative study. Hormones and Behavior 47, 389–409.CrossRefGoogle ScholarPubMed
Garside, P., Behnke, J. M. and Rose, R. A. (1989). The immune-response of male dsn hamsters to a primary infection with Ancylostoma ceylanicum. Journal of Helminthogy 63, 251–260.CrossRefGoogle ScholarPubMed
Getty, T. (2002). Signaling health versus parasites. American Naturalist 159, 363–371.CrossRefGoogle ScholarPubMed
Goüy de Bellocq, J., Ribas, A., Casanova, J.-C. and Morand, S. (2007). Immunocompetence and helminth community of the white-toothed shrew, Crocidura russula from the Montseny Natural Park, Spain. European Journal of Wildlife Research 53, 315–320.CrossRefGoogle Scholar
Hagelin, J. C. and Ligon, J. D. (2001). Female quail prefer testosterone-mediated traits, rather than the ornate plumage of males. Animal Behaviour 61, 465–476.CrossRefGoogle Scholar
Herbreteau, V., Rerkamnuaychoke, W., Jittapalapong, S. and Morand, S. (2011). Field and Laboratory Protocols for Rodent Studies. Kasetsart University Press, Bangkok, (in press).Google Scholar
Horak, P., Tummeleht, L. and Talvik, H. (2006). Predictors and markers of resistance to neurotropic nematode infection in rodent host. Parasitology Research 98, 396–402.CrossRefGoogle ScholarPubMed
Hunt, K. E., Hahn, T. P. and Wingfield, J. C. (1997). Testosterone implants increase song but not aggression in male Lapland longspurs. Animal Behaviour 54, 1177–1192.CrossRefGoogle Scholar
Janeway, C. A., Travers, P., Walport, M. and Capra, J. D. (1999). Immunobiology: The Immune System in Health and Disease, Fourth Edition. Current Biology Publications, New York.Google Scholar
Klasing, K. C. (1998). Nutritional modulation of resistance to infectious diseases. Poultry Science 77, 1119–1125.CrossRefGoogle ScholarPubMed
Kopp, W. C. (1990). The immune functions of the spleen. In The Spleen: Structure, Function and Clinical Significance (ed. Bowdler, A. J.), pp. 103–126. Chapman & Hall Medical, London, UK.Google Scholar
Lee, K. A. (2006). Linking immune defenses and life history at the level of the individual and the species. Integrative and Comparative Biology 46, 1000–1015.CrossRefGoogle ScholarPubMed
Lutermann, H. and Bennett, N. C. (2008). Strong immune function: a benefit promoting the evolution of sociality? Journal of Zoology 275, 26–32.CrossRefGoogle Scholar
MacLeod, C. D. (2010). Assessing the shape and topology of allometric relationships with body mass: a case study using testes mass allometry. Methods in Ecology and Evolution 1, 359–370.CrossRefGoogle Scholar
Magurran, A. E. (2004). Measuring Biological Diversity. Princeton University Press, Princeton.Google Scholar
Malo, A. F., Roldan, E. R. S., Garde, J. J., Soler, A. J., Vicente, J., Gortazar, C. and Gomendio, M. (2009). What does testosterone do for red deer males? Proceedings of the Royal Society B-Biological Sciences 276, 971–980.CrossRefGoogle ScholarPubMed
Martin, L. B., Scheuerlein, A. and Wikelski, M. (2003). Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proceedings of the Royal Society London B 270, 153–158.CrossRefGoogle ScholarPubMed
Martin, T. E., Møller, A. P., Merino, S. and Clobert, J. (2001). Does clutch size evolve in response to parasites and immunocompetence? Proceedings of the National Academy of Sciences, USA 98, 2071–2076.CrossRefGoogle ScholarPubMed
Marzal, A., Bensch, S., Reviriego, M., Balbontin, J. and De Lope, J. F. (2008). Effects of malaria double infection in birds: one plus one is not two. Journal of Evolutionary Biology 21, 979–987.CrossRefGoogle Scholar
McCullagh, P. and Nelder, J. (1989). Generalized Linear Models, Second Edition. Boca Raton: Chapman and Hall.CrossRefGoogle Scholar
Møller, A. P., Christe, P. H., Erritzoe, J. and Mavarez, A. (1998). Condition, disease and immune defence. Oikos 83, 301–306.CrossRefGoogle Scholar
Morand, S. and Deter, J. (2008). Parasitism and regulation of the host population. In Ecology and Evolution of Parasitism (ed. Thomas, F., Guégan, J. F. and Renaud, F.), pp. 83–105. Oxford University Press.CrossRefGoogle Scholar
Morand, S. and Poulin, R. (2000). Nematode parasite species richness and the evolution of spleen size in birds. Canadian Journal of Zoology 78, 1356–1360.CrossRefGoogle Scholar
Navarro-Gonzalez, N., Verheyden, H., Hoste, H., Cargnelutti, B., Lourtet, B., Merlet, J., Daufresne, T., Lavín, S., Hewison, A. J. M., Morand, S. and Serrano, E. (2011). Diet quality and immunocompetence influence parasite load of roe deer in a fragmented landscape. European Journal of Wildlife Research (in press).CrossRefGoogle Scholar
Nelson, R. J. and Demas, G. E. (1996). Seasonal changes in immune function. Quarterly Review of Biology 71, 511–548.CrossRefGoogle ScholarPubMed
Nelson, R. J., Demas, G. E., Klein, S. L. and Kriegsfeld, L. J. (2002). Seasonal Patterns of Stress, Immune Function and Disease. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Owens, I. P. F. and Short, R. V. (1995). Hormonal basis of sexual dimorphism in birds – implications for new theories of sexual selection. Trends in Ecology and Evolution 10, 44–47.CrossRefGoogle ScholarPubMed
Pagès, M., Chaval, Y., Herbreteau, V., Waengsothorn, S., Cosson, J.-F., Hugot, J.-P., Morand, S. and Michaux, J. (2010). Revisiting the taxonomy of the Rattini tribe: a phylogeny-based delimitation of species boundaries. BMC Evolutionary Biology 10, e184.CrossRefGoogle Scholar
Paradis, E. (2006). Analysis of Phylogenetics and Evolution with R. Springer, New York.CrossRefGoogle Scholar
Parker, G. A. (1970). Sperm competition and its evolutionary consequences in insects. Biological Reviews of the Cambridge Philosophical Society 45, 525–567.CrossRefGoogle Scholar
Paz Nava, M., Veiga, J. P. and Puerta, M. (2001). White blood cell counts in house sparrows (Passer domesticus) before and after moult and after testosterone treatment. Canadian Journal of Zoology 79, 145–148.CrossRefGoogle Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites, Second Edition. Princeton and Oxford Princeton University Press.CrossRefGoogle Scholar
Poulin, R. and Mouillot, D. (2004). The evolution of taxonomic diversity in helminth assemblages of mammalian hosts. Evolutionary Ecology 18, 231–247.CrossRefGoogle Scholar
R Development Core Team (2010). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL: http://www.R-project.org.Google Scholar
Ricotta, C. (2002). Bridging the gap between ecological diversity indices and measures of biodiversity with Shannon's entropy: comment to Izsak and Papp. Ecological Modelling 152, 1–3.CrossRefGoogle Scholar
Ricotta, C. and Avena, G. C. (2003). An information-theoretical measure of taxonomic diversity. Acta Biotheoretica 51, 35–41.CrossRefGoogle ScholarPubMed
Salvador, A., Veiga, J. P., Martin, J., Lopez, P., Abelenda, M. and Puerta, M. (1996). The cost of producing a sexual signal: Testosterone increases the susceptibility of male lizards to ectoparasitic infestation. Behavioral Ecology 7, 145–150.CrossRefGoogle Scholar
Sanderson, M. J. (2002). Estimating absolute rates of molecular evolution and divergence times: A penalized likelihood approach. Molecular Biology and Evolution 19, 101–109.CrossRefGoogle ScholarPubMed
Schlinger, B. A., Soma, K. K. and Saldanha, C. (2001). Advances in avian behavioral endocrinology. Auk 118, 283–289.CrossRefGoogle Scholar
Shannon, C. (1948). A mathematical theory of communication. Bell Systems Technical Journal 27, 379–423.CrossRefGoogle Scholar
Sheldon, B. C. and Verhulst, S. (1996). Ecological immunology: Costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317–321.CrossRefGoogle ScholarPubMed
Smith, K. G. and Hunt, J. L. (2004). On the use of spleen mass as a measure of avian immune system strength. Oecologia 138, 28–31.CrossRefGoogle ScholarPubMed
Stoehr, A. M. and Kokko, H. (2006). Sex differences in immunocompetence: what does life history theory predict?. Behavioural Ecology 17, 751–756.CrossRefGoogle Scholar
Taylor, L. H., Mackinnon, M. J. and Read, A. F. (1998). Virulence of mixed-clone and single-clone infections of the rodent malaria Plasmodium chabaudi. Evolution 52, 583–591.CrossRefGoogle ScholarPubMed
Tew, T. E. and Macdonald, D. W. (1994). Dynamics of space use and male vigour amongst wood mice, Apodemus sylvaticus, in the cereal ecosystem. Behavioural Ecology and Sociobiology 34, 337–345.CrossRefGoogle Scholar
Vincent, A. L. and Ash, L. R. (1978). Further observations on spontaneous neoplasms in the Mongolian gerbil, Meriones unguiculatus. Laboratory Animal Science 28, 297–300.Google ScholarPubMed
Vicente, J., Perez-Rodriguez, L. and Gortazar, C. (2007). Sex, age, spleen size, and kidney fat of red deer relative to infection intensities of the lungworm Elaphostrongylus cervi. Naturwissenschaften 94, 581–587.CrossRefGoogle Scholar
Wakelin, K. (1996). Immunity to Parasites. Cambridge University Press, Cambridge.Google ScholarPubMed
Watkins, R. A., Moshier, S. E., Odell, W. D. and Pinter, A. J. (1991). Splenomegaly and reticulocytosis caused by Babesia microti infections in natural-populations of the montane vole, Microtus montanus. Journal of Protozoology 38, 573–576.CrossRefGoogle ScholarPubMed
Wilson, K., Bjornstad, A. P., Dobson, A. P., Merler, S., Poglayen, G., Randolph, S. E., Read, A. F. and Skorping, A. (2002). Heterogeneities in macroparasite infections: patterns and processes. In The Ecology of Wildlife Diseases (eds. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P.), pp 6–44. Oxford University Press, New York.CrossRefGoogle Scholar
Wingfield, J. C., Hegner, R. E., Dufty, A. M. Jr. and Ball, G. F. (1990). The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. American Naturalist 136, 829–846.CrossRefGoogle Scholar
Zuk, M. and Stoehr, A. M. (2002). Immune defense and host life history. American Naturalist 160, 9–22.CrossRefGoogle ScholarPubMed