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Causal mechanisms underlying host specificity in bat ectoparasites

  • Behavioural Ecology
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Abstract

In parasites, host specificity may result either from restricted dispersal capacity or from fixed coevolutionary host-parasite adaptations. Knowledge of those proximal mechanisms leading to particular host specificity is fundamental to understand host-parasite interactions and potential coevolution of parasites and hosts. The relative importance of these two mechanisms was quantified through infection and cross-infection experiments using mites and bats as a model. Monospecific pools of parasitic mites (Spinturnix myoti and S. andegavinus) were subjected either to individual bats belonging to their traditional, native bat host species, or to another substitute host species within the same bat genus (Myotis). The two parasite species reacted differently to these treatments. S. myoti exhibited a clear preference for, and had a higher fitness on, its native host, Myotis myotis. In contrast, S. andegavinus showed no host choice, although its fitness was higher on its native host M. daubentoni. The causal mechanisms mediating host specificity can apparently differ within closely related host-parasite systems.

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References

  • Becnel JJ, Andreadis TG (1998) Amblyospora salinaria n. sp. (Microsporidia: Amblyosporidae), parasite of Culex salinarius (Diptera: Culicidae): its life cycle stage in an intermediate host. J Invertebr Pathol 71:258–262

    Article  CAS  PubMed  Google Scholar 

  • Christe P, Arlettaz R, Vogel P (2000) Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecol Lett 3:207–212

    Article  Google Scholar 

  • Christe P, Giorgi MS, Vogel P, Arlettaz R (2003) Differential species-specific ectoparasitic mite intensities in two intimately coexisting sibling bat species: resource-mediated host attractiveness or parasite specialization? J Anim Ecol 72:866–872

    Google Scholar 

  • Combes C (1991) Evolution of parasite life cycles. In: Toft CA, Aeschlimann A, Bolis L (eds) Parasite-host associations. Coexistence or conflict? Oxford University Press, London, pp 62–82

  • Combes C (1995) Interactions durables: ecologie et évolution du parasitisme. Masson, Paris

    Google Scholar 

  • Combes C (1997) Fitness of parasites—pathology and selection [Review]. Int J Parasitol 27:1–10

    Article  CAS  PubMed  Google Scholar 

  • Cox R, Stewart PD, Macdonald DW (1998) The ectoparasites of the European badger, Meles meles, and the behavior of the host-specific flea, Paraceras melis. J Insect Behav 12:245–265

    Article  Google Scholar 

  • Deunff J (1977) Observations on Spinturnicidae of Occidental Paleartic Region (Acarina, Mesostigmata)—specificity, distribution and repartition. Acarologia 18:602–616

    Google Scholar 

  • Deunff J, Beaucournu JC (1981) Phenology and variations of dermecos in some species of Spinturnicidae (Acarina, Mesostigmata). Ann Parasitol 56:203–224

    CAS  Google Scholar 

  • Deunff J, Keller A, Aellen V (1997) Redescription of Spinturnix punctata (Sundevall, 1833) (Acari, Mesostigmata, Spinturnicidae), a specific parasite of Barbastella barbastellus (Chiroptera, Vespertilionidae). Rev Suisse Zool 104:199–206

    Google Scholar 

  • Devine GJ, Ingvarsdottir A, Mordue W, Pike AW, Pickett J, Duce I, Murdue AJ (2000) Salmon lice, Lepeophtheirus salmonis, exhibit specific chemotactic responses to semiochemicals originating from the salmonid, Salmo salar. J Chem Ecol 26:1833–1847

    Article  CAS  Google Scholar 

  • Du Preez LH, Kok DJ (1997) Supporting experimental evidence of host specificity among Southern African polystomes (Polystomatidae, Monogenea). Parasitol Res 83:558–562

    Article  PubMed  Google Scholar 

  • Du Preez LH, Kok DJ, Seaman MT (1997) Host recognition behaviour of polystome oncomiracidia (Polystomatidae: Monogenea) in contact with natural and substitute hosts. J Afr Zool 111:47–55

    Google Scholar 

  • Estrada-Pena A, Serra-Cobo J (1991) The acarinia and nycteribidia zones of Miniopterus scheibersi Kuhl (Mammalia: Chiroptera) in the northeast of Spain. Folia Parasitol 38:345–354

    CAS  PubMed  Google Scholar 

  • Evans GO (1968) The external morphology of the post-embryonic developmental stages of Spinturnix myoti Kol. Acarologia 4:589–608

    Google Scholar 

  • Gandon S, Capowiez Y, Dubois Y, Michalakis Y, Olivieri I (1996) Local adaptation and gene-for-gene coevolution in a metapopulation model. Proc R Soc Lond B Biol Sci 263:1003–1009

    Google Scholar 

  • Giorgi MS, Arlettaz R, Christe P, Vogel P (2001) The energetic grooming costs imposed by a parasitic mite (Spinturnix myoti) upon its bat host (Myotis myotis). Proc R Soc Lond B Biol Sci 268:2071–2075

    Article  CAS  PubMed  Google Scholar 

  • Glantz SA, Slinker BK (1991) Primer of applied regression and analysis of variance. McGraw-Hill, New York

  • Gurevitch J, Chester ST (1986) Analysis of repeated measures experiments. Ecology 67:251–255

    Google Scholar 

  • Jaenike J (1990) Host specialization in phytophagous insects. Annu Rev Ecol Syst 21:243–273

    Article  Google Scholar 

  • Jaenike J (1996) Population-level consequences of parasite aggregation. Oikos 76:155–160

    Google Scholar 

  • Johnson KP, Williams BL, Drown DM, Adams RJ, Clayton DH (2002) The population genetics of host specificity: genetic differentiation in dove lice (Insecta: Phthiraptera). Mol Ecol 11:25–38

    Article  CAS  PubMed  Google Scholar 

  • Kawecki TJ (1998) Red queen meets Santa Rosalia—arms races and the evolution of host specialization in organisms with parasitic lifestyles. Am Nat 152:635–651

    Article  Google Scholar 

  • Kethley JB (1971) Population regulation in quill mites (Acarina: Syringophilidae). Ecology 52:1113–1118

    Google Scholar 

  • Kosoy MY, Saito EK, Green D, Marston EL, Jones DC, Childs JE (2000) Experimental evidence of host specificity of Bartonella infection in rodents. Comp Immunol Microbiol Infect Dis 23:221–238

    Article  CAS  PubMed  Google Scholar 

  • Kristoffersen AB, Lingjaerde OC, Stenseth NC, Shimada M (2001) Non-parametric modelling of nonlinear density dependence: a three-species host-parasitoid system. J Anim Ecol 70:1098–1098

    Article  Google Scholar 

  • Le Brun N, Renaud F, Berrebi P, Lambert A (1992) Hybrid zones and host-parasite relationships—effect on the evolution of parasitic specificity. Evolution 46:56–61

    Google Scholar 

  • McCoy KD, Boulinier T, Tirard C, Michalakis Y (2001) Host specificity of a generalist parasite: genetic evidence of sympatric host races in the seabird tick Ixodes uriae. J Evol Biol 14:395–405

    Article  Google Scholar 

  • Meeûs T de, Renaud F, Gabrion C (1990) A model for studying isolation mechanisms in parasite populations—the genus Lepeophtheirus (Copepoda, Caligidae). J Exp Zool 254:207–214

    PubMed  Google Scholar 

  • Meeûs T de, Hochberg ME, Renaud F (1995) Maintenance of two genetic entities by habitat selection. Evol Ecol 9:131–138

    Google Scholar 

  • Meeûs T de, Michalakis Y, Renaud F (1998) Santa Rosalia revisited: Or why are there so many kinds of parasites in ‘the garden of earthly delights’? Parasitol Today 14:10–13

    Article  Google Scholar 

  • Norton DA, Carpenter MA (1998) Mistletoes as parasites: host specificity and speciation. Trends Ecol Evol 13:101–105

    Article  Google Scholar 

  • Norton DA, De Lange PJ (1999) Host specificity in parasitic mistletoes (Loranthaceae) in New Zealand. Funct Ecol 13:552–559

    Article  Google Scholar 

  • Osterkamp J, Wahl U, Schmalfuss G, Haas W (1999) Host-odour recognition in two tick species is coded in a blend of vertebrate volatiles. J Comp Physiol 185:59–67

    Article  CAS  Google Scholar 

  • Poulin R (1992) Evolutionary ecology of parasites. From individual to communities. Chapman & Hall, London

  • Rudnick A (1960) A revision of the family Spinturnicidae. Univ Calif Publ Entomol 17:157–284

    Google Scholar 

  • Ruedi M, Mayer F (2001) Molecular systematics of bats of the genus Myotis (Vespertilionidae) suggests deterministic ecomorphological convergences. Mol Phylogenet Evol 21:436–448

    Article  CAS  PubMed  Google Scholar 

  • Soler JJ, Møller AP, Soler M (1999) A comparative study of host selection in the European cuckoo Cuculus canorus. Oecologia 118:265–276

    Article  Google Scholar 

  • Sonenshine DE (1993) Biology of ticks. Oxford University Press, New York

  • Talan MI, Kirov SA, Clow LA, Kosheleva NA (1996) Cold acclimation-associated changes in brown adipose tissue do not necessarily indicate an increase of nonshivering thermogenesis in C57BL/6 J mice. Physiol Behav 60:1285–1289

    Article  CAS  PubMed  Google Scholar 

  • Thompson JN (1994) The coevolutionary process. University of Chicago Press, Chicago

  • Thresher RE, Werner M, Hoeg JT, Svane I, Glenner H, Murphy NE, Wittwer C (2000) Developing the options for managing marine pests: specificity trials on the parasitic castrator, Sacculina carcini, against the European crab, Carcinus maenas, and related species. J Exp Mar Biol Ecol 254:37–51

    Article  PubMed  Google Scholar 

  • Timms R, Read AF (1999) What makes a specialist special? Trends Ecol Evol 14:333–334

    Article  PubMed  Google Scholar 

  • Tompkins DM, Clayton DH (1999) Host resources govern the specificity of swiftlet lice: size matters. J Anim Ecol 68:489–500

    Article  Google Scholar 

  • Tripet F, Richner H (1997) The coevolutionary potential of a ‘generalist’ parasite, the hen flea Ceratophyllus gallinae. Parasitology 115:419–427

    Article  PubMed  Google Scholar 

  • Tripet F, Jacot A, Richner H (2002a) Larval competition affects the life histories and dispersal behavior of an avian ectoparasite. Ecology 83:935–945

    Google Scholar 

  • Tripet F, Christe P, Møller AP (2002b) The importance of host spatial distribution for parasite specialization and speciation: a comparative study of bird fleas (Siphonaptera: Ceratophyllidae). J Anim Ecol 71:735–748

    Article  Google Scholar 

  • Tyler KM, Higgs PG, Matthews KR, Gull K (2001) Limitation of Trypanosoma brucei parasitaemia results from density-dependent parasite differentiation and parasite killing by the host immune response. Proc R Soc Lond B Biol Sci 268:2235–2243

    Article  CAS  PubMed  Google Scholar 

  • Ward SA, Leather SR, Pickup J, Harrington R (1998) Mortality during dispersal and the cost of host-specificity in parasites—how many aphids find hosts. J Anim Ecol 67:763–773

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Saddle River, USA

Download references

Acknowledgements

We are grateful to Névéna Basic, Brigitte Reutter and Sylvain Ursenbacher for help with fieldwork. We warmly thank Sara Helms Cahan for helpful comments and improving the English. This study was supported by a grant from the Swiss National Science Foundation to P.V., R.A. and P.C. (3100-052584.97 and 3100-061450.00/1). The experiments comply with the current laws of the country in which the experiments were performed.

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Correspondence to Maud S. Giorgi.

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Giorgi, M.S., Arlettaz, R., Guillaume, F. et al. Causal mechanisms underlying host specificity in bat ectoparasites. Oecologia 138, 648–654 (2004). https://doi.org/10.1007/s00442-003-1475-1

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