Skip to main content
Log in

Coevolution between multiple helminth infestations and basal immune investment in mammals: cumulative effects of polyparasitism?

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Animals often suffer from multiple parasite attacks in natural conditions (i.e., polyparasitism). The community of these parasites, which simultaneously or sequentially infest given host species, has rarely been investigated as a parasitic pressure per se. From this perspective, and despite the impressive number of immunoecological or comparative studies, the impacts of polyparasitism on immune responses are far from being appreciated. Focusing on helminths across a wide range of mammalian species and using a phylogenetic comparative method, we show, for the first time, that an increase in the number of helminth parasite species is positively correlated with an increase in basal immune investment (estimated by the counts of white blood cells) across mammal species. After discussing inherent limits of this comparative approach, we put this result in the evolutionary perspective of multiple parasitic infestations.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Arrierero E, Møller A (2008) Host ecology and life history traits associated with blood parasite species richness in birds. J Evol Biol 21:1504–1513

    Article  Google Scholar 

  • Binida-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD et al (2007) The delayed rise of present-day mammals. Nature 446:507–512

    Article  Google Scholar 

  • Bordes F, Morand S (2008) Helminth species diversity of mammals: parasite species richness is a host species attribute. Parasitology 135:1–5

    Article  Google Scholar 

  • Bordes F, Morand S (2009) Parasite diversity: an overlooked measure of parasitic pressures? Oikos 118:801–806

    Article  Google Scholar 

  • Bradley JE, Jackson JA (2008) Measuring immune system variation to help understand host-pathogen community dynamics. Parasitology 135:807–823

    Article  CAS  PubMed  Google Scholar 

  • Carey JR, Judge DS (2000) Longevity records: life spans of mammals, birds, amphibians, reptiles, and fish. Monographs on population aging, vol. 8. Odense University Press, Odense

    Google Scholar 

  • Cox FEG (2000) Concomitant infections, parasites and immune responses. Parasitology 122:23–38

    Article  Google Scholar 

  • Davidar P, Morton ES (2006) Are multiple infections more severe for purple martins than single infections? The Auk 123:141–147

    Article  Google Scholar 

  • Ezeamama AE, Friedman JF, Olveda RM, Acosta LP, Kurtis et al (2005) Functional significance of low-intensity polyparasite helminth infections in anemias. J Infect Dis 192:2160–2170

    Article  PubMed  Google Scholar 

  • Ezenwa VO, Price SA, Altizer S, Vitone D, Cook KC (2006) Host traits and parasite species richness in even and odd-toed hoofed mammals, Artiodactyla and Perissodactyla. Oikos 115:526–536

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Goüy de Bellocq J, Charbonnel N, Morand S (2008) Coevolutionary relationship between helminth diversity and MHC class II polymorphism in rodents. J Evol Biol 21:1144–1150

    Article  PubMed  Google Scholar 

  • Graham AL (2008) Ecological rules governing helminth-microparasite coinfection. Proc Natl Acad Sci USA 105:566–570

    Article  CAS  PubMed  Google Scholar 

  • Graham AL, Lamb TJ, Read AF, Allen JE (2005) Malaria-Filarial co infection in mice makes malarial disease more severe unless Filarial infection achieves patency. J Inf Dis 191:410–421

    Article  Google Scholar 

  • Guernier V, Hochberg ME, Guégan JF (2004) Ecology drives the worldwide distribution of human diseases. PLOS One 2:740–746

    CAS  Google Scholar 

  • Hasselquist D (2007) Comparative immunoecology in birds: hypotheses and tests. J Ornith 148:571–582

    Article  Google Scholar 

  • Holmstad PR, Jensen KH, Skorping A (2008) Ectoparasite intensities are correlated with endoparasite infection loads in willow ptarmigan. Oikos 117:515–520

    Article  Google Scholar 

  • Jolles AE, Ezenwa V, Etienne RS, Turner WC, Olff H (2008) Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo. Ecology 89:2239–2250

    Article  PubMed  Google Scholar 

  • Krasnov BR, Shenbrot GI, Mouillot D, Khokhlova IS, Poulin R (2005) Spatial variation in species diversity and composition of flea assemblages in small mammalian hosts: geographical distance or faunal similarity. J Biog 32:633–644

    Article  Google Scholar 

  • Krasnov B, Stanko M, Khokhlova IS, Miklisova D, Morand S, Shenbrot GI, Poulin R (2006) Relationships between local and regional species richness in flea communities of small mammalian hosts: saturation and spatial scale. Parasitol Res 98:403–413

    Article  PubMed  Google Scholar 

  • Krasnov BR, Korallo-Vinarskaya NP, Vinarsky MV, Shenbrot GI, Mouillot D, Poulin R (2008) Searching for general patterns in parasite ecology: host identity versus environmental influence on gamasid mite assemblages in small mammals. Parasitology 135:229–242

    CAS  PubMed  Google Scholar 

  • Lello J, Boag B, Hudson PJ (2005) The effects of single and concomitant infections on condition and fecundity of the wild rabbits (Oryctolagus cuniculus). Int J Parasitol 35:1509–1515

    Article  CAS  PubMed  Google Scholar 

  • Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, Allen JE (2004) Helminth parasites—masters of regulation. Imm Rev 201:89–116

    Article  CAS  Google Scholar 

  • Martin LB, Weil ZM, Nelson R (2008) Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Phil Trans R Soc Lond B 363:321–339

    Article  Google Scholar 

  • Meussen ENT, Balic A (2000) Do eosinophils have a role in the killing of helminths? Parasitol Today 16:95–101

    Article  Google Scholar 

  • Møller AP (1998) Evidence of larger impact of parasites in the tropics: investment in immune function within and outside the tropics. Oikos 82:265–270

    Article  Google Scholar 

  • Møller AP, Merino S, Brown CR, Robertson RJ (2001) Immune defence and host sociality: a comparative study of swallows and martins. Am Nat 152:136–145

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Munson L, Terio K, Kock R, Mlengeya T, Roelke ME et al (2008) Climate extremes promote fatal co-infections during canine distemper epidemics in African lions. PLOS One 3:1–6

    Article  Google Scholar 

  • Nunn CL (2002) A comparative study of leukocyte counts and disease risk in primates. Evolution 56:177–190

    PubMed  Google Scholar 

  • Nunn CL, Gittleman JL, Antonovics J (2000) Promiscuity and the primate immune system. Science 290:1168–1169

    Article  CAS  PubMed  Google Scholar 

  • Nunn CL, Gittleman JL, Antonovics J (2003) A comparative study of white blood cell counts and disease risk in carnivores. Proc R Soc Lond B 270:347–356

    Article  Google Scholar 

  • Owen JP, Clayton DH (2007) Where are the parasites in the PHA response? Trends Ecol Evol 22:228–229

    Article  PubMed  Google Scholar 

  • Petney TN, Andrews RH (1998) Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. Int J Parasitol 28:377–393

    Article  CAS  PubMed  Google Scholar 

  • Poulin R (2007) Evolutionary ecology of parasites, 2nd edn. Princeton University Press, Princeton

    Google Scholar 

  • Preston BT, Capellini I, McNamara P, Barton RA, Nunn CL (2009) Parasite resistance and the adaptive significance of sleep. BMC Evol Biol 9:1–9

    Article  Google Scholar 

  • Pullan R, Brooker S (2008) The health impact of polyparasitism in humans: are we under-estimated the burden of parasitic diseases? Parasitology 135:783–794

    Article  CAS  PubMed  Google Scholar 

  • Purvis A, Rambaut A (1995) Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Comp Appl Biosci 11:247–251

    CAS  PubMed  Google Scholar 

  • Read AF, Allen JE (2000) The economics of immunity. Science 10:1104–1105

    Article  Google Scholar 

  • Semple S, Cowlishaw G, Bennett P (2002) Immune system evolution among anthropoid primates: parasites, injuries and predators. Proc R Soc Lond B 269:1031–1037

    Article  Google Scholar 

  • Wegner KM, Reusch TBH, Kalbe M (2003) Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J Evol Biol 16:224–232

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study is supported by the French ANR Biodiversity (project CERoPath, “Community Ecology of Rodents and their Pathogens in a changing environment”, ANR 07 BDIV 012).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Serge Morand.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bordes, F., Morand, S. Coevolution between multiple helminth infestations and basal immune investment in mammals: cumulative effects of polyparasitism?. Parasitol Res 106, 33–37 (2009). https://doi.org/10.1007/s00436-009-1623-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-009-1623-6

Keywords

Navigation