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Chapter Three - Wild rodents as a natural model to study within-host parasite interactions

from Part I - Understanding within-host processes

Published online by Cambridge University Press:  28 October 2019

By
Amy B. Pedersen  and
Andy Fenton
Edited by
Kenneth Wilson ,
Andy Fenton  and
Dan Tompkins
Kenneth Wilson
Affiliation:
Lancaster University
Andy Fenton
Affiliation:
University of Liverpool
Dan Tompkins
Affiliation:
Predator Free 2050 Ltd
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Summary

Individuals are typically coinfected with multiple parasite species. Laboratory studies have shown that coinfecting parasites can interact strongly within individual hosts with potentially serious consequences for disease progression and successful treatment. Understanding the occurrence of these interactions in natural systems and their effect on host health and parasite epidemiology in the wild are only beginning. Rodents are the ideal ‘wild’ model taxon to study these effects due to their ubiquity, high abundance, ease of capture, diagnostic assessment, and experimentation in their natural setting. Also, their close phylogenetic relatedness to the standard laboratory mouse (Mus musculus) model means that studies of wild rodents have great potential to advance our understanding of the dynamics and mechanisms of coinfection interactions. We review coinfection studies in wild rodents and compare the findings with predictions of general coinfection theory. We show that the relationship between coinfection interactions at the within-host scale and their pattern of association at the host population scale can be complex, as predicted by the general theory. Patterns of parasite association at the host population level can be poor predictors of the occurrence or direction of the underlying within-host interaction.

Keywords

Coinfectionwithin-host parasite interactionsmicroparasitemacroparasiteepidemiological modelshelminthsparasite community ecologyinterspecific interactionsmiceSIR models
Type
Chapter
Information
Wildlife Disease Ecology
Linking Theory to Data and Application
 , pp. 58 - 90
Publisher: Cambridge University Press
Print publication year: 2019

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References

Abu-Madi, M.A., Behnke, J.M., Lewis, J.W. & Gilbert, F.S. (1998) Descriptive epidemiology of Heligmosomoides polygyrus in Apodemus sylvaticus from three contrasting habitats in southeast England. Journal of Helminthology, 72, 93–100.Google Scholar
Abu-Madi, M.A., Behnke, J.M., Lewis, J.W. & Gilbert, F.S. (2000) Seasonal and site specific variation in the component community structure of intestinal helminths in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology, 74, 7–15.Google Scholar
Anderson, R.M. & May, R.M. (1978) Regulation and stability of host–parasite population interactions. I. Regulatory processes. Journal of Animal Ecology, 47, 219–247.Google Scholar
Anderson, R.M. & May, R.M. (1981) The population dynamics of microparasites and their invertebrate hosts. Philosophical Transactions of the Royal Society of London B, 291, 451–524.Google Scholar
Anderson, R.M. & May, R.M. (1992) Infectious Diseases of Humans: Dynamics and Control. Oxford: Oxford University Press.Google Scholar
Basáñez, M.-G., French, M.D., Walker, M. & Churcher, T.S. (2012) Paradigm lost: how parasite control may alter pattern and process in human helminthiases. Trends in Parasitology, 28, 161–171.Google Scholar
Behnke, J. & Harris, P.D. (2010) Heligmosomoides bakeri: a new name for an old worm? Trends in Parasitology, 26, 524–529.Google Scholar
Behnke, J.M., Bajer, A., Sinski, E. & Wakelin, D. (2001) Interactions involving intestinal nematodes of rodents: experimental and field studies. Parasitology, 122, S39–S49.CrossRefGoogle ScholarPubMed
Behnke, J.M., Gilbert, F.S., Abu-Madi, M.A. & Lewis, J.W. (2005) Do the helminth parasites of wood mice interact? Journal of Animal Ecology, 74, 982–993.Google Scholar
Bentwich, Z., Kalinkovich, A., Weisman, Z., et al. (1999) Can eradication of helminthic infections change the face of AIDS and tuberculosis? Immunology Today, 20, 485–487.Google Scholar
Blackwell, A.D., Martin, M., Kaplan, H. & Gurven, M. (2013) Antagonism between two intestinal parasites in humans: the importance of co-infection for infection risk and recovery dynamics. Proceedings of The Royal Society of London B, 280, 20131671.Google Scholar
Bordes, F., Guegan, J.F. & Morand, S. (2011) Microparasite species richness in rodents is higher at lower latitudes and is associated with reduced litter size. Oikos, 120, 1889–1896.Google Scholar
Bordes, F. & Morand, S. (2009) Coevolution between multiple helminth infestations and basal immune investment in mammals: cumulative effects of polyparasitism? Parasitology Research, 106, 33–37.Google Scholar
Bottomley, C., Isham, V. & Basanez, M.G. (2005) Population biology of multispecies helminth infection: interspecific interactions and parasite distribution. Parasitology, 131, 417–433.Google Scholar
Bottomley, C., Isham, V. & Basanez, M.G. (2007) Population biology of multispecies helminth infection: competition and coexistence. Journal of Theoretical Biology, 244, 81–95.Google Scholar
Bush, A.O. & Holmes, J.C. (1986) Intestinal helminths of lesser scaup ducks: an interactive community. Canadian Journal of Zoology – Revue Canadienne de Zoologie, 64, 142–152.CrossRefGoogle Scholar
Costa, F., Porter, F.H., Rodrigues, G., et al. (2014) Infections by Leptospira interrogans, Seoul Virus, and Bartonella spp. among Norway rats (Rattus norvegicus) from the urban slum environment in Brazil. Vector-borne and Zoonotic Diseases, 14(1), 33–40. DOI:10.1089/vbz.2013.1378.Google Scholar
Cox, F.E.G. (2001) Concomitant infections, parasites and immune responses. Parasitology, 122, S23–S38.Google Scholar
de Bellocq, J.G., Sara, M., Casanova, J.C., Feliu, C. & Morand, S. (2003) A comparison of the structure of helminth communities in the woodmouse, Apodemus sylvaticus, on islands of the western Mediterranean and continental Europe. Parasitology Research, 90, 64–70.Google Scholar
Dobson, A.P. (1985) The population dynamics of competition between parasites. Parasitology, 91, 317–347.Google Scholar
Dobson, A.P. (1988) The population biology of parasite-induced changes in host behavior. Quarterly Review of Biology, 63, 139–165.Google Scholar
Druilhe, P., Tall, A. & Sokhna, C. (2005) Worms can worsen malaria: towards a new means to roll back malaria? Trends in Parasitology, 21, 359–362.Google Scholar
Elton, C., Ford, E.B. & Baker, J.R. (1931) The health and parasites of a wild mouse population. Proceedings of the Royal Society of London B, 101, 657–721.Google Scholar
Ezenwa, V.O., Etienne, R.S., Luikart, G., Beja-Pereira, A. & Jolles, A.E. (2010) Hidden consequences of living in a wormy world: nematode-induced immune suppression facilitates tuberculosis invasion in African buffalo. American Naturalist, 176, 613–624.Google Scholar
Ezenwa, V.O. & Jolles, A.E. (2015) Opposite effects of anthelmintic treatment on microbial infection at individual versus population scales. Science, 347, 175–177.Google Scholar
Fenton, A. (2008) Worms and germs: the population dynamic consequences of microparasite–macroparasite co-infection. Parasitology, 135, 1545–1560.CrossRefGoogle ScholarPubMed
Fenton, A. (2013) Dances with worms: the ecological and evolutionary impacts of deworming on coinfecting pathogens. Parasitology, 140, 1119–1132.Google Scholar
Fenton, A., Knowles, S.C.L., Petchey, O.L. & Pedersen, A.B. (2014) The reliability of observational approaches for detecting interspecific parasite interactions: comparison with experimental results. International Journal for Parasitology, 44, 437–445.CrossRefGoogle ScholarPubMed
Fenton, A. & Perkins, S.E. (2010) Applying predator–prey theory to modelling immune-mediated, within-host interspecific parasite interactions. Parasitology, 137, 1027–1038.CrossRefGoogle ScholarPubMed
Fenton, A., Viney, M.E. & Lello, J. (2010) Detecting interspecific macroparasite interactions from ecological data: patterns and process. Ecology Letters, 13, 606–615.Google Scholar
Ferrari, N., Cattadori, I.M., Rizzoli, A. & Hudson, P.J. (2009) Heligmosomoides polygyrus reduces infestation of Ixodes ricinus in free-living yellow-necked mice, Apodemus flavicollis. Parasitology, 136, 305–316.Google Scholar
Forbes, K.M., Henttonen, H., Hirvela-Koski, V., et al. (2015) Food provisioning alters infection dynamics in populations of a wild rodent. Proceedings of the Royal Society of London B, 282, 20151939.Google Scholar
Gatto, M. & De Leo, G.A. (1998) Interspecific competition among macroparasites in a density-dependent host population. Journal of Mathematical Biology, 37, 467–490.Google Scholar
Gause, G.E. (1934) The Struggle for Existence. Baltimore, MD: Williams & Wilkins.Google Scholar
Graham, A.L. (2008) Ecological rules governing helminth–microparasite coinfection. Proceedings of the National Academy of Sciences of the United States of America, 105, 566–570.Google Scholar
Griffiths, E.C., Pedersen, A.B., Fenton, A. & Petchey, O.L. (2011) The nature and consequences of coinfection in humans. Journal of Infection, 63, 200–206.Google Scholar
Griffiths, E.C., Pedersen, A.B., Fenton, A. & Petchey, O.L. (2014) Analysis of a summary network of co-infection in humans reveals that parasites interact most via shared resources. Proceedings of the Royal Society of London B, 281, 20132286.Google Scholar
Gupta, S., Maiden, M.C.J., Feavers, I.M., et al. (1996) The maintenance of strain structure in populations of recombining infectious agents. Nature Medicine, 2, 437–442.Google Scholar
Gupta, S., Swinton, J. & Anderson, R.M. (1994) Theoretical studies of the effects of heterogeneity in the parasite population on the transmission dynamics of malaria. Proceedings of the Royal Society of London B, 256, 231–238.Google Scholar
Gutiérrez, R., Morick, D., Cohen, C., Hawlena, H. & Harrus, S. (2014) The effect of ecological and temporal factors on the composition of Bartonella infection in rodents and their fleas. ISME Journal, 8, 1598–1608.Google Scholar
Harms, G. & Feldmeier, H. (2002) HIV infection and tropical parasitic diseases – deleterious interactions in both directions? Tropical Medicine and International Health, 7, 479–488.Google Scholar
Harris, J.B., Podolsky, M.J., Bhuiyan, T.R., et al. (2009) Immunologic responses to Vibrio cholerae in patients co-infected with intestinal parasites in Bangladesh. PLoS Neglected Tropical Diseases, 3, e403.Google Scholar
Hastings, A. (1987) Can competition be detected using species co-occurrrence data? Ecology, 68, 117–123.Google Scholar
Haukisalmi, V. & Henttonen, H. (1993a) Coexistence in helminths of the bank vole Clethrionomys glareolus. 1. Patterns of co-occurrence. Journal of Animal Ecology, 62, 221–229.CrossRefGoogle Scholar
Haukisalmi, V. & Henttonen, H. (1993b) Coexistence in helminths of the bank vole Clethrionomys glareolus. 2. Intestinal distribution and interspecific interactions. Journal of Animal Ecology, 62, 230–238.Google Scholar
Haukisalmi, V. & Henttonen, H. (1998) Analysing interspecific associations in parasites: alternative methods and effects of sampling heterogeneity. Oecologia, 116, 565–574.Google Scholar
Hayes, K.S., Bancroft, A.J., Goldrick, M., et al. (2010) Exploitation of the intestinal microflora by the parasitic nematode Trichuris muris. Science, 328, 1391–1394.Google Scholar
Holmes, J.C. (1961) Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). 1. General effects and comparison with crowding. Journal of Parasitology, 47, 209–216.Google Scholar
Holmes, J.C. (1962) Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). Effects on growth. Journal of Parasitology, 48, 87–96.CrossRefGoogle ScholarPubMed
Holmes, J.C. & Price, P.W. (1986) Communities of parasites. In: Kikkawa, J. & Anderson, D.J. (eds.), Community Ecology: Patterns and Processes (pp. 187–213).Oxford: Blackwell Scientific Publishers.Google Scholar
Johnson, P.T.J., De Roode, J.C. & Fenton, A. (2015) Why infectious disease research needs community ecology. Science, 349.Google Scholar
Kennedy, C.R. (2006) Ecology of the Acathocephala. Cambridge: Cambridge University Press.Google Scholar
Knowles, S.C.L., Fenton, A., Petchey, O.L., et al. (2013) Stability of within-host parasite communities in a wild mammal system. Proceedings of the Royal Society of London B, 280, 20130598.Google Scholar
Krasnov, B.R., Matthee, S., Lareschi, M., Korallo-Vinarskaya, N.P. & Vinarski, M.V. (2010) Co-occurrence of ectoparasites on rodent hosts: null model analyses of data from three continents. Oikos, 119, 120–128.Google Scholar
Kreisinger, J., Bastien, G., Hauffe, H.C., Marchesi, J. & Perkins, S.E. (2015) Interactions between multiple helminths and the gut microbiota in wild rodents. Philosophical Transactions of the Royal Society of London B – Biological Sciences, 370, 20150295.Google Scholar
Lello, J., Boag, B., Fenton, A., Stevenson, I.R. & Hudson, P.J. (2004) Competition and mutualism among the gut helminths of a mammalian host. Nature, 428, 840–844.Google Scholar
Lewis, J.W. (1968a) Studies on the helminth parasites of the long-tailed field mouse, Apodemus sylvaticus sylvaticus from Wales. Journal of Zoology, 154, 287–312.Google Scholar
Lewis, J.W. (1968b) Studies on the helminth parasites of voles and shrews from Wales. Journal of Zoology, 154, 313–331.CrossRefGoogle Scholar
Lotka, A.J. (1932) The growth of mixed populations: two species competing for a common food supply. Journal of the Washington Academy of Science, 22, 461–469.Google Scholar
Luong, L.T., Perkins, S.E., Grear, D.A., Rizzoli, A. & Hudson, P.J. (2010) The relative importance of host characteristics and co-infection in generating variation in Heligmosomoides polygyrus fecundity. Parasitology, 137, 1003–1012.Google Scholar
Maizels, R.M., Balic, A., Gomez-Escobar, N., et al. (2004) Helminth parasites – masters of regulation. Immunological Reviews, 201, 89–116.Google Scholar
Maurice, C.F., Knowles, S.C.L., Ladau, J., et al. (2015) Marked seasonal variation in the wild mouse gut microbiota. ISME Journal, 9, 2423–2434.CrossRefGoogle ScholarPubMed
May, R.M. & Nowak, M.A. (1995) Coinfection and the evolution of parasite virulence. Proceedings of the Royal Society of London B, 261, 209–215.Google ScholarPubMed
Montgomery, S.S.J. & Montgomery, W.I. (1988) Cyclic and non-cyclic dynamics in populations of the helminth parasites of wood mice, Apodemus sylvaticus. Journal of Helminthology, 62, 78–90.Google Scholar
Montgomery, S.S.J. & Montgomery, W.I. (1990) Structure, stability and species interactions in helminth communities of wood mice, Apodemus sylvaticus. International Journal for Parasitology, 20, 225–242.Google Scholar
Montoya, J.M. & Sole, R.V. (2002) Small world patterns in food webs. Journal of Theoretical Biology, 214, 405–412.CrossRefGoogle ScholarPubMed
Muller-Graf, C.D.M., Durand, P., Feliu, C., et al. (1999) Epidemiology and genetic variability of two species of nematodes (Heligmosomoides polygyrus and Syphacia stroma) of Apodemus spp. Parasitology, 118, 425–432.Google Scholar
Nieto, N.C., Leonhard, S., Foley, J.E. & Lane, R.S. (2010) Coinfection of western gray squirrel (Sciurus griseus) and other sciurid rodents with Borrelia burgdorferi sensu stricto and Anaplasma phagocytophilum in California. Journal of Wildlife Diseases, 46(1), 291&296. http://dx.doi.org/10.7589/0090-3558-46.1.291.Google Scholar
Nowell, F. & Higgs, S. (1989) Eimeria species infecting wood mice (genus Apodemus) and the transfer of two species to Mus musculus. Parasitology, 98, 329–336.Google Scholar
Pedersen, A.B. & Antonovics, J. (2013) Anthelmintic treatment alters the parasite community in a wild mouse host. Biology Letters, 9, 20130205.Google Scholar
Pedersen, A.B. & Babayan, S.A. (2011) Wild immunology. Molecular Ecology, 20, 872–880.Google Scholar
Pedersen, A.B. & Fenton, A. (2007) Emphasising the ecology in parasite community ecology. Trends in Ecology & Evolution, 22, 133–139.CrossRefGoogle Scholar
Pedersen, A.B. & Fenton, A. (2015) The role of antiparasite treatment experiments in assessing the impact of parasites on wildlife. Trends in Parasitology, 31, 200–211.Google Scholar
Petney, T.N. & Andrews, R.H. (1998) Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. International Journal for Parasitology, 28, 377–393.Google Scholar
Poulin, R. (1996) Richness, nestedness, and randomness in parasite infracommunity structure. Oecologia, 105, 545–551.Google Scholar
Poulin, R. (1997) Species richness of parasite assemblages: evolution and patterns. Annual Review of Ecology and Systematics, 28, 341–358.Google Scholar
Poulin, R. (2007) Evolutionary Ecology of Parasites, 2nd edition. Princeton, NJ: Princeton University Press.Google Scholar
Price, P.W. (1980) Evolutionary Biology of Parasites. Princeton, NJ: Princeton University Press.Google Scholar
Quinnell, R.J. (1992) The population dynamics of Heligmosomoides polygyrus in an enclosure population of wood mice. Journal of Animal Ecology, 61, 669–679.CrossRefGoogle Scholar
Rausch, R. (1952) Studies on the helminth fauna of Alaska. 11. Helminth parasites of microtine rodents – taxonomic considerations. Journal of Parasitology, 38, 415–444.Google Scholar
Rausch, R. & Kuns, M.L. (1950) Studies on some North American shrew cestodes. Journal of Parasitology, 36, 433–438.Google Scholar
Roberts, M.G. & Dobson, A.P. (1995) The population dynamics of communities of parasitic helminths. Mathematical Biosciences, 126, 191–214.Google Scholar
Rynkiewicz, E.C., Pedersen, A.B. & Fenton, A. (2015) An ecosystem approach to understanding and managing within-host parasite community dynamics. Trends in Parasitology, 31, 212–221.Google Scholar
Salvador, A.R., Guivier, E., Xuereb, A., et al. (2011) Concomitant influence of helminth infection and landscape on the distribution of Puumala hantavirus in its reservoir, Myodes glareolus. BMC Microbiology, 11, 30.Google Scholar
Schluter, D. (1984) A variance test for detecting species associations, with some example applications. Ecology, 65, 998–1005.Google Scholar
Sharpe, G.I. (1964) The helminth parasites of some small mammal communities. I. The parasites and their hosts. Parasitology, 54, 145–154.CrossRefGoogle ScholarPubMed
Shaw, D.J. & Dobson, A.P. (1995) Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology, 111, S111–133.CrossRefGoogle ScholarPubMed
Shaw, D.J., Grenfell, B.T. & Dobson, A.P. (1998) Patterns of macroparasite aggregation in wildlife host populations. Parasitology, 117, 597–610.Google Scholar
Sole, R.V. & Montoya, J.M. (2001) Complexity and fragility in ecological networks. Proceedings of the Royal Society of London B, 268, 2039–2045.Google Scholar
Stanko, M., Miklisova, D., de Bellocq, J.G. & Morand, S. (2002) Mammal density and patterns of ectoparasite species richness and abundance. Oecologia, 131, 289–295.Google Scholar
Stock, T.M. & Holmes, J.C. (1988) Functional relationships and microhabitat distributions of enteric helminths of grebes (Podicipedidae): the evidence for interactive communities. Journal of Parasitology, 74, 214–227.Google Scholar
Strogatz, S.H. (2001) Exploring complex networks. Nature, 410, 268–276.CrossRefGoogle ScholarPubMed
Telfer, S., Lambin, X., Birtles, R., et al. (2010) Species interactions in a parasite community drive infection risk in a wildlife population. Science, 330, 243–246.Google Scholar
Thomas, R.J. (1953) On the nematode and trematode parasites of some small mammals from the Inner Hebrides. Journal of Helminthology, 27, 143–168.CrossRefGoogle Scholar
van Baalen, M. & Sabelis, M.W. (1995) The dynamics of multiple infection and the evolution of virulence. American Naturalist, 146, 881–910.Google Scholar
Watts, D.J. & Strogatz, S.H. (1998) Collective dynamics of ‘small-world’ networks. Nature, 393, 440–442.Google Scholar
Yakob, L., Williams, G.M., Gray, D.J., et al. (2013) Slaving and release in co-infection control. Parasites & Vectors, 6, 157.CrossRefGoogle ScholarPubMed

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