Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-26T18:42:45.011Z Has data issue: false hasContentIssue false

Heterozygosity and parasite intensity: lung parasites in the water frog hybridization complex

Published online by Cambridge University Press:  02 October 2007

P. JOLY*
Affiliation:
UMR 5023 Ecology of Fluvial Hydrosystems, Université Claude Bernard Lyon1, F-69622Villeurbanne, France
V. GUESDON
Affiliation:
UMR 5023 Ecology of Fluvial Hydrosystems, Université Claude Bernard Lyon1, F-69622Villeurbanne, France
E. FROMONT
Affiliation:
UMR 5558 Biometry and Evolutionary Biology, Université Claude Bernard Lyon1, F-69622Villeurbanne, France
S. PLENET
Affiliation:
UMR 5023 Ecology of Fluvial Hydrosystems, Université Claude Bernard Lyon1, F-69622Villeurbanne, France
O. GROLET
Affiliation:
UMR 5023 Ecology of Fluvial Hydrosystems, Université Claude Bernard Lyon1, F-69622Villeurbanne, France
J. F. GUEGAN
Affiliation:
UMR CNRS-IRD 9926, Centre for the Study of Micro-organism Polymorphism, 911 Avenue Agropolis – BP 5045, F-34032 Montpellier Cedex 1, France
S. HURTREZ-BOUSSES
Affiliation:
UMR CNRS-IRD 9926, Centre for the Study of Micro-organism Polymorphism, 911 Avenue Agropolis – BP 5045, F-34032 Montpellier Cedex 1, France
F. THOMAS
Affiliation:
UMR CNRS-IRD 9926, Centre for the Study of Micro-organism Polymorphism, 911 Avenue Agropolis – BP 5045, F-34032 Montpellier Cedex 1, France
F. RENAUD
Affiliation:
UMR CNRS-IRD 9926, Centre for the Study of Micro-organism Polymorphism, 911 Avenue Agropolis – BP 5045, F-34032 Montpellier Cedex 1, France
*
*Corresponding author: UMR 5023 Ecology of Fluvial Hydrosystems, Université Claude Bernard Lyon1, F-69622 Villeurbanne, France. Tel: +33 472 433 586. Fax: 33 472 431 141. E-mail: [email protected]

Summary

In hybridogenetic systems, hybrid individuals are fully heterozygous because one of the parental genomes is discarded from the germinal line before meiosis. Such systems offer the opportunity to investigate the influence of heterozygosity on susceptibility to parasites. We studied the intensity of lung parasites (the roundworm Rhabdias bufomis and the fluke Haplometra cylindracea) in 3 populations of water frogs of the Rana lessonae-esculenta complex in eastern France. In these mixed populations, hybrid frogs (R. esculenta) outnumbered parental ones (R. lessonae). Despite variation in parasite intensity and demographic variability among populations, the relationship between host age and intensity of parasitism suggests a higher susceptibility in parentals than in hybrids. Mortality is probably enhanced by lung parasites in parental frogs. On the other hand, while parental frogs harboured higher numbers of H. cylindracea than hybrid frogs, the latter had higher numbers of R. bufonis. Despite such discrepancies, these results support the hybrid resistance hypothesis, although other factors, such as differences in body size, age-related immunity, differential exposure risks and hemiclonal selection, could also contribute to the observed patterns of infection.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2007

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

Agresti, A. (1990). Categorical Data Analysis. John Wiley and Sons, New York.Google Scholar
Anderson, R. M. and Gordon, D. M. (1982). Processes influencing the distribution of parasite numbers within host populations, with special emphasis on parasite-induced host mortalities. Parasitology 85, 373398.CrossRefGoogle ScholarPubMed
Arnold, M. L. (1997). Natural Hybridisation and Evolution. Oxford Series in Ecology and Evolution. Oxford University Press, Oxford.CrossRefGoogle Scholar
Augert, D. and Joly, P. (1993). Plasticity of age at maturation in neighbouring populations of the common frog, Rana temporaria. Canadian Journal of Zoology 71, 2633.CrossRefGoogle Scholar
Baker, M. R. (1979). The free-living and parasitic development of Rhabdias spp. (Nematoda: Rhabdiasidae) in amphibians. Canadian Journal of Zoology 57, 161178.CrossRefGoogle Scholar
Barta, J. R., Boulard, Y. and Desser, S. S. (1989). Blood parasites of Rana esculenta from Corsica: comparison of its parasites with those of eastern North American Ranids in the context of host phylogeny. Transactions of the American Microscopical Society 108, 620.CrossRefGoogle Scholar
Beerli, P. (1994). Genetic isolation and calibration of an average protein clock in western Paleartic water frogs of the Aegean region. Ph. D. Dissertation, University of Zürich, Switzerland.Google Scholar
Berger, L. and Uzzell, T. (1980). The eggs of European water frogs (Rana esculenta complex) and their hybrids. Folia Biologica (Krakow) 28, 325.Google ScholarPubMed
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Castanet, J., Meunier, F. and de Ricqlès, A. (1977). L'enregistrement de la croissance osseuse chez les vertébrés poïkilothermes: données comparatives et essais de synthèse. Bulletin de Biologie Franco-Belge 111, 183202.Google Scholar
Colon, L. (2004). Dispersion de Rana ridibunda dans la vallée du Rhône et relations génétiques avec le complexe d'hybridation esculenta. Ph. D. thesis, Lyon 1 University, France.Google Scholar
Cooper, E. L. and Hildemann, W. H. (1965). The immune response of larval bullfrogs (Rana catesbeiana) to diverse antigens. Annals of the New York Academy of Sciences 126, 647661.CrossRefGoogle ScholarPubMed
Dupont, F. and Crivelli, A. J. (1988). Do parasites confer a disadvantage to hybrids? Oecologia 75, 587592.CrossRefGoogle Scholar
Fritz, R. S., Moulia, C. and Newcombe, G. (1999). Resistance of hybrid plants and animals to herbivores, pathogens, and parasites. Annual Review of Ecology and Systematics 30, 565591.CrossRefGoogle Scholar
Goater, C. P. (1992). Experimental population dynamics of Rhabdias bufonis (Nematoda) in toads (Bufo bufo): density dependence in the primary infection. Parasitology 104, 179187.CrossRefGoogle ScholarPubMed
Goater, C. P. and Ward, P. I. (1992). Negative effects of Rhabdias bufonis (Nematoda) on the growth and survival of toads (Bufo bufo). Oecologia 89, 161165.CrossRefGoogle ScholarPubMed
Goumghar, M. D., Abrous, M., Ferdonnet, D., Dreyfuss, G. and Rondelaud, D. (2000). Prevalence of Haplometra cylindracea infection in three species of Lymnaea snails in central France. Parasitology Research 86, 337339.CrossRefGoogle ScholarPubMed
Grabda-Kazubska, B. and Moczo, T. (1981). Nervous system and chaetotaxy in the cercaria of Haplometra cylindracea (Zeder 1800) (Digenea, Plagiorchiidae). Parasitology Research 65, 5361.Google Scholar
Guisan, A. and Harrell, F. E. (2000). Ordinal response regression models in ecology. Journal of Vegetation Sciences 11, 617626.CrossRefGoogle Scholar
Hellriegel, B. and Reyer, H. U. (2000). Factors influencing the composition of mixed populations of a hemiclonal hybrid and its sexual host. Journal of Evolutionary Biology 13, 906918.CrossRefGoogle Scholar
Holenweg Peter, A.-K. (2001). Dispersal rates and distances in adult water frogs, Rana lessonae, R. ridibunda and their hybridogenetic associate, R. esculenta. Herpetologica 57, 449460.Google Scholar
Hotz, H., Uzzell, T. and Berger, L. (1997). Linkage groups of protein-coding genes in western palearctic water frogs reveal extensive evolutionary conservation. Genetics 147, 255270.CrossRefGoogle ScholarPubMed
Hotz, H., Semlitsch, R. D., Gutmann, E., Guex, G.-D. and Beerli, P. (1999). Spontaneous heterosis in larval life-history traits of hemiclonal frog hybrids. Proceedings of the National Academy of Sciences, USA 96, 21712176.CrossRefGoogle ScholarPubMed
Hudson, P. J., Dobson, A. P., Cattadori, I. M., Newborn, D., Haydon, D. T., Shaw, D. J., Benton, T. G. and Grenfell, B. T. (2002). Trophic interactions and population growth rates: describing patterns and identifying mechanisms. Philosophical Transactions of the Royal Society of London, B 35, 12591271.CrossRefGoogle Scholar
Jakob, E. M., Marshall, S. D. and Uetz, G. W. (1996). Estimating fitness: a comparison of body condition indices. Oikos 77, 6167.CrossRefGoogle Scholar
Joly, P. (2001). The future of the selfish hemiclone: a neodarwinian approach of water frog evolution. Mitteilungen aus dem Museum für Naturkunde in Berlin 77, 3138.Google Scholar
Kuzmin, Y., Tkach, V. V. and Brooks, D. R. (2007). Two new species of Rhabdias (Nematoda, Rhabdiasidae) from the marine toad, Bufo marinus (L.) (Lissamphibia: Anura: Bufonidae), in Central America. Journal of Parasitology 93, 159165.CrossRefGoogle Scholar
Lawless, J. F. (1987). Negative binomial and mixed Poisson regression. Canadian Journal of Statistics 15, 209225.CrossRefGoogle Scholar
Lengagne, T., Grolet, O. and Joly, P. (2006). Male mating speed promotes hybridization in the Rana lessonae-Rana esculenta waterfrog system. Behavioural Ecology and Sociobiology 60, 123130.CrossRefGoogle Scholar
MacCullagh, P. and Nelder, J. A. (1989). Generalized Linear Models. Chapman and Hall, London.CrossRefGoogle Scholar
Moulia, C. (1999). Parasitism of plant and animal hybrids: are facts and fates the same? Ecology 80, 392406.CrossRefGoogle Scholar
Moulia, C., Le Brun, N., Loubès, C., Marin, R. and Renaud, F. (1995). Hybrid vigour against parasites in interspecific crosses between two mice species. Heredity 74, 4852.CrossRefGoogle ScholarPubMed
Negovetic, S., Anholt, B. R., Semlitsch, R. D. and Reyer, H. U. (2001). Specific responses of sexual and hybridogenetic European waterfrog tadpoles to temperature. Ecology 82, 766774.CrossRefGoogle Scholar
Pagano, A., Joly, P. and Hotz, H. (1997). Taxon composition and genetic variation of water frogs in the mid-Rhône floodplain. Comptes-Rendus de l'Académie des Sciences de Paris, 320, 759766.Google ScholarPubMed
Pagano, A. and Schmeller, D. (1999). Is recombination less negligible than previously described in hybridogenetic water frogs? In Current Studies in Herpetology (ed. Miaud, C. and Guyetant, R.), pp. 351356. Proceedings of the 9th Ordinary General Meeting of the Societas Europaea Herpetologica, Chambéry, France.Google Scholar
Pagano, A., Joly, P., Plénet, S., Lehman, A. and Grolet, O. (2001). Breeding habitat partitioning in the Rana esculenta complex: the intermediate niche hypothesis supported. Ecoscience 8, 294300.CrossRefGoogle Scholar
Peters, A. (1977). Quantitative und Qualitative Aspekte des Helminthenfauna heimischer Grünfrosch- und Unkenpopulationen. Dissertation, Humboldt-Universität, Berlin, Germany.Google Scholar
Pickel, K., Müller, M. A. and ter Meulen, V. (1981). Analysis of age-dependent resistance to murine coronavirus JHM infection in mice. Infection and Immunity 34, 648654.CrossRefGoogle ScholarPubMed
Plénet, S., Hervant, F. and Joly, P. (2000 a). Ecology of the hybridogenetic Rana esculenta complex: differential oxygen requirements of tadpoles. Evolutionary Ecology 14, 1323.CrossRefGoogle Scholar
Plénet, S., Pagano, A., Joly, P. and Fouillet, P. (2000 b). Variation of plastic responses to oxygen availability within the hybridogenetic Rana esculenta complex. Journal of Evolutionary Biology 13, 2029.CrossRefGoogle Scholar
Plénet, S., Joly, P., Hervant, F., Fromont, E. and Grolet, O. (2005). Are hybridogenetic zones structured by environmental gradients? In situ experiments in the waterfrog hybridisation complex. Journal of Evolutionary Biology 18, 15751586.CrossRefGoogle Scholar
Sage, R. D., Heyneman, D., Lim, K. C. and Wilson, A. C. (1986). Wormy mice in a hybrid zone. Nature, London 324, 6063.CrossRefGoogle Scholar
Saglam, N. and Arikan, H. (2006). Endohelminth fauna of the marsh frog Rana ridibunda from Lake Hozar, Turkey. Diseases of Aquatic Organisms 72, 253260.CrossRefGoogle ScholarPubMed
Schultz, R. J. (1969). Hybridization, unisexuality, and polyploidy in the teleost Poeciliopis (Poeciliidae) and other vertebrates. The American Naturalist 103, 605619.CrossRefGoogle Scholar
Semlitsch, R. D. (1993). Effects of different predators on the survival and development of tadpoles from the hybridogenetic Rana esculenta complex. Oikos 67, 4046.CrossRefGoogle Scholar
Tietje, G. A. and Reyer, H. U. (2004). Larval development and recruitment of juveniles in a natural population of Rana lessonae and R. esculenta. Copeia, 638646.CrossRefGoogle Scholar
Tkach, V., Kuzmin, Y. and Pulis, E. E. (2006). A new species of Rhabdias from the lungs of the wood frog, Rana sylvatica, in North America: the last sibling of Rhabdias ranae? Journal of Parasitology 92, 631636.CrossRefGoogle ScholarPubMed
Tscherner, W. (1966). Helminthofaunistische Untersuchungen an Rana esculenta L und R. ridibunda Pall., mit besonderer Berücksichtigung der Europäischen Prosotocus-Arten (Trematoda: Lecithodendriidae). Mitteilungen aus dem Museum für Naturkunde in Berlin 42, 259279.Google Scholar
Tunner, H. G. (1974). Die klonale Struktur einer Wasserfroschpopulation. Zeitschrift für zoologische Systematik und Evolutionsforschung 12, 309314.CrossRefGoogle Scholar
Tunner, H. G. and Nopp, H. (1979). Heterosis in the common European waterfrog. Naturwissenschaften 66, 268269.CrossRefGoogle Scholar
Ujvari, B. and Madsen, T. (2006). Age, parasites, and condition affect humoral immune response in tropical pythons. Behavioral Ecology 17, 2024.CrossRefGoogle Scholar
Venables, W. N. and Ripley, B. D. (2002). Modern Statistics with S. Springer Verlag, Luxemburg.CrossRefGoogle Scholar
Walton, A. C. (1949). Parasites of the Ranidae (Amphibia). Transactions of the American Microscopical Society 68, 4954.CrossRefGoogle Scholar
Whitman, G. T. (1989). Plant hybrid zones as sinks for pests. Science 244, 14901493.Google Scholar
Wilson, K., Grenfell, B. T. and Shaw, D. J. (1996). Analysis of aggregated parasite distributions: a comparison of methods. Functional Ecology 10, 592601.CrossRefGoogle Scholar