Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-27T13:37:40.846Z Has data issue: false hasContentIssue false
  • English
  • Français

Tracking a heterosis effect in the field: tadpole resistance to parasites in the water frog hybridogenetic complex

Published online by Cambridge University Press:  24 June 2009

B. PLANADE ,
J.-P. LENA ,
H. LI ,
S. PLENET ,
J.-F. GUEGAN ,
F. THOMAS ,
S. HURTREZ-BOUSSES ,
F. RENAUD  and
P. JOLY
B. PLANADE
Affiliation:
UMR 5023 Ecology of Fluvial Hydrosystems, Université Lyon 1, F-69622 Villeurbanne, France
J.-P. LENA
Affiliation:
UMR 5023 Ecology of Fluvial Hydrosystems, Université Lyon 1, F-69622 Villeurbanne, France
H. LI
Affiliation:
UMR 5023 Ecology of Fluvial Hydrosystems, Université Lyon 1, F-69622 Villeurbanne, France VA Palo Alto Health Care System, 3801 Miranda Avenue, Palo Alto, CA 94304, US
S. PLENET
Affiliation:
UMR 5023 Ecology of Fluvial Hydrosystems, Université Lyon 1, F-69622 Villeurbanne, France
J.-F. GUEGAN
Affiliation:
UMR CNRS-IRD 2724 Génétique des Maladies Infectieuses, 911 Avenue Agropolis – BP 5045, F-34032 Montpellier Cedex 1, France
F. THOMAS
Affiliation:
UMR CNRS-IRD 2724 Génétique des Maladies Infectieuses, 911 Avenue Agropolis – BP 5045, F-34032 Montpellier Cedex 1, France
S. HURTREZ-BOUSSES
Affiliation:
UMR CNRS-IRD 2724 Génétique des Maladies Infectieuses, 911 Avenue Agropolis – BP 5045, F-34032 Montpellier Cedex 1, France
F. RENAUD
Affiliation:
UMR CNRS-IRD 2724 Génétique des Maladies Infectieuses, 911 Avenue Agropolis – BP 5045, F-34032 Montpellier Cedex 1, France
P. JOLY*
Affiliation:
UMR 5023 Ecology of Fluvial Hydrosystems, Université Lyon 1, F-69622 Villeurbanne, France
*
*Corresponding author: UMR 5023 Ecology of Fluvial Hydrosystems, Université Lyon 1; F-69622 Villeurbanne, France. Tel: +33 472 433 586. Fax: +33 472 431 141. E-mail: pjoly@univ-lyon1.fr
Get access Rights & Permissions [Opens in a new window]

Summary

Depending on the extent of evolutionary divergence among parent taxa, hybrids may suffer from a breakdown of co-adapted genes or may conversely exhibit vigour due to the heterosis effect, which confers advantages to increased genetic diversity. That last mechanism could explain the success of hybrids when hybridization zones are large and long lasting, such as in the water frog hybridization complex. In this hybridogenetic system, hybrid individuals exhibit full heterozygosity that makes it possible to investigate in situ the impact of hybridization. We have compared parasite intensity between hybrid Rana esculenta and parental R. lessonae individuals at the tadpole stage in two populations inhabiting contrasted habitats. We estimated intensity of Gyrinicola sp. (Nematoda) in the gut, Echinostome metacercariae in the kidneys and Haplometra cylindracea in the body cavity (both species belong to Trematoda). Despite high sampling effort, no variation in parasite intensity was detected between taxa, except a possible higher tolerance to H. cylindracea in hybrid tadpoles. The low effect of hybridization suggests efficient gene co-adaptation between the two genomes that could result from hemiclonal selection. Variation in infection intensity among ponds could support the Red Queen hypothesis.

Keywords

hemiclonal selectionGyrinicola sp.Echinostome metacercariaeheterosis effect
Type
Research Article
Information
Parasitology , Volume 136 , Issue 9 , August 2009 , pp. 1003 - 1013
Copyright
Copyright © Cambridge University Press 2009

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

Abt, G. and Reyer, H. U. (1993). Mate choice and fitness in a hybrid frog – Rana-esculenta females prefer Rana-lessonae males over their own. Behavioral Ecology and Sociobiology 32, 221–228.CrossRefGoogle Scholar
Adamson, M. L. (1981). Development and transmission of Gyrinicola batrachiensis (Walton, 1929) Adamson, 1981 (Pharyngodonidae: Oxyuridea). Canadian Journal of Zoology 59, 1351–1367.CrossRefGoogle Scholar
Bakke, T. A., Soleng, A. and Harris, P. D. (1999). The susceptibility of Atlantic salmon (Salmo salar L.)×brown trout (Salmo trutta L.) hybrids to Gyrodactylus salaris Malmberg and Gyrodactylus derjavini Mikailov. Parasitology 119, 467–481.CrossRefGoogle ScholarPubMed
Boag, B., Lello, J., Fenton, A., Tompkins, D. M. and Hudson, P. J. (2001). Patterns of parasite aggregation in the wild European rabbit (Oryctolagus cuniculus). International Journal for Parasitology 31, 1421–1428.CrossRefGoogle ScholarPubMed
Buchmann, K. and Lindenström, T. (2002). Interactions between monogenean parasites and their fish hosts. International Journal for Parasitology 32, 309–319.CrossRefGoogle ScholarPubMed
Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multimodel Inference: a Practical Information-Theoretic Approach, Springer-Verlag, New York, USA.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
Combes, C. (2001). Ecology and Evolution of Intimate Interactions. Chicago U. P., Chicago, USA.Google Scholar
Derothe, J. M., Loubes, C., Perriat-Sanguinet, M., Orth, A. and Moulia, C. (1999). Experimental trypanosomiasis of natural hybrids between house mouse subspecies. International Journal for Parasitology 29, 1011–1016.CrossRefGoogle ScholarPubMed
Derothe, J. M., Porcherie, A., Perriat-Sanguinet, M., Loubes, C. and Moulia, C. (2004). Recombination does not generate pinworm susceptibility during experimental crosses between two mouse subspecies. Parasitology Research 93, 356–363.CrossRefGoogle Scholar
Dupont, F. and Crivelli, A. J. (1988). Do parasites confer a disadvantage to hybrids? A case study of Alburnus alburnus×Rutilus rubilio, a natural hybrid of Lake Mikri Prespa, Northern Greece. Oecologia 75, 587–592.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, 565–591.CrossRefGoogle Scholar
Fritz, R. S., Nichols-Orians, C. M. and Brunsfeld, S. J. (1994). Interspecific hybridization of plants and resistance to herbivores: hypotheses, genetics, and variable responses in a diverse herbivore community. Oecologia 97, 106–117.CrossRefGoogle Scholar
Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183–190.Google Scholar
Grabda-Kazubska, B. (1970). Studies on the life-cycle of Haplometra cylindrica (Zeder 1800) (Trematoda:Plagiorchidae). Acta Parasitologica Polonica 18, 497–512.Google Scholar
Graf, J.-D. and Polls Pelaz, M. (1989). Evolutionary genetics of the Rana esculenta complex. In Evolution and Ecology of Unisexual Vertebrates (ed. Dawley, R. M. and Bogart, J. P.), Bulletin 466, pp. 289–302. New York State Museum, Albany, New York, USA.Google 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, 906–918.CrossRefGoogle Scholar
Holland, M. P., Skelly, D. K., Kashgarian, M., Bolden, S. R., Harrison, L. M. and Cappello, M. (2007). Echinostome infection in green frogs (Rana clamitans) is stage and age dependent. Journal of Zoology 271, 455–462.CrossRefGoogle 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, 255–270.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, 2171–2176.CrossRefGoogle ScholarPubMed
Johnson, P. T. J. and Hartson, R. B. (2009). All hosts are not equal: explaining differential patterns of malformations in an amphibian community. Journal of Animal Ecology 78, 191–201.CrossRefGoogle ScholarPubMed
Joly, P. (2001). The future of the selfish hemiclone: a Neodarwinian approach to water frog evolution. Mitteilungen des Museums für Naturkunde, Berlin – Zoologische Reihe 77, 31–38.Google Scholar
Joly, P. and Morand, A. (1994). Theoretical habitat templets, species traits, and species richness: amphibian in the Upper Rhône and its floodplain. Freshwater Biology 31, 455–468.CrossRefGoogle Scholar
Joly, P., Guesdon, V., Fromont, E., Plenet, S., Grolet, O., Guegan, J. F., Hurtrez-Bousses, S., Thomas, F. and Renaud, F. (2007). Heterozygosity and parasite intensity: lung parasites in the water frog hybridization complex. Parasitology 135, 95–104.CrossRefGoogle ScholarPubMed
Koprivnikar, J., Forbes, M. R. and Baker, R. L. (2006). On the efficacy of anti-parasite behaviour: a case study of tadpole susceptibility to cercariae of Echinostoma trivolvis. Canadian Journal of Zoology 84, 1623–1629.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, 123–130.CrossRefGoogle Scholar
Lengagne, T., Plénet, S. and Joly, P. (2008). Breeding behaviour and hybridization: variation in male chorusing behaviour promotes mating among taxa in waterfrogs. Animal Behaviour 75, 443–450.CrossRefGoogle Scholar
Lively, C. M. and Dybdahl, M. E. (2000). Parasite adaptation to locally common host genotypes. Nature, London 405, 679–681.CrossRefGoogle ScholarPubMed
Lo, C.-T. (1995). Echinostoma macrorchis: life history, population dynamics of intramolluscan stages, and the first and second intermediate hosts. The Journal of Parasitology 81, 569–576.CrossRefGoogle ScholarPubMed
Moore, W. S. (1977). An evaluation of narrow hybrid zones in vertebrates. The Quarterly Review of Biology 52, 263–277.CrossRefGoogle Scholar
Moulia, C. (1999). Parasitism of plant and animal hybrids: are facts and fate the same? Ecology 80, 392–406.CrossRefGoogle Scholar
Moulia, C., Le Brun, N., Loubes, C., Marin, R. and Renaud, F. (1995). Hybrid vigour against parasites in interspecific crosses between two mice species. Heredity 74, 48–52.CrossRefGoogle ScholarPubMed
Moulia, C. and Joly, P. (2008). Parasitism and hybrid zones. In Ecology and Evolution of Parasitism (ed. Thomas, F., Guégan, J. F. and Renaud, F.), pp. 69–82. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Mullahy, J. (1986). Specification and testing of some modified count data models. Journal of Econometrics 33, 341–365.CrossRefGoogle Scholar
Negovetic, S., Anholt, B. R., Semlitsch, R. D. and Reyer, H.-U. (2001). Specific responses of sexual and hybridogenetic European water frog tadpoles to temperature. Ecology 82, 766–774.CrossRefGoogle Scholar
Pagano, A., Joly, P. and Hotz, H. (1997). Taxon composition and genetic variation of water frogs in the mid-Rhone floodplain. Comptes Rendus de l'Académie des Sciences Serie III-Life Sciences 320, 759–766.Google ScholarPubMed
Pagano, A., Joly, P., Plénet, S., Lehmann, A. and Grolet, O. (2001). Breeding habitat partitioning in the Rana esculenta complex: the intermediate niche hypothesis supported. Ecoscience 8, 294–300.CrossRefGoogle Scholar
Planade, B., Bain, O., Léna, J. P. and Joly, P. (2008). Gyrinicola chabadamsoni n. sp. and G. tba (Dinnik 1930) (Nematoda, Oxyuroidea) from tadpoles of the hybridogenetic complex Rana lessonae-esculenta (Amphibia, Ranoidea). Zootaxa 1764, 25–40.Google Scholar
Plénet, S., Hervant, F. and Joly, P. (2000 a). Ecology of the hybridogenetic Rana esculenta complex: differential oxygen requirements of tadpoles. Evolutionary Ecology 14, 13–23.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 hybridization complex. Journal of Evolutionary Biology 18, 1575–1586.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, 20–28.CrossRefGoogle Scholar
Potts, J. M. and Elith, J. (2006). Comparing species abundance models. Ecological Modelling 199, 153–163.CrossRefGoogle Scholar
Prudhoe, S. and Bray, R. A. (1982). Platyhelminth Parasites of the Amphibia, Oxford University Press, Oxford, UK.Google Scholar
Pryor, G. S. and Bjorndall, K. A. (2005). Effects of the nematode Gyrinicola batrachiensis on development, gut morphology, and fermentation in bullfrog tadpoles (Rana catesbeiana): a novel mutualism. Journal of Experimental Zoology, Part A Comparative Experimental Biology 303A, 704–712.CrossRefGoogle Scholar
Raffel, T. R., LeGros, R. P., Love, B. C., Rohr, J. R. and Hudson, P. J. (2009). Parasite age-intensity relationships in red-spotted newts: does immune memory influence salamander disease dynamics? International Journal for Parasitology 39, 231–241.CrossRefGoogle ScholarPubMed
Rousset, F., Thomas, F., De Meeüs, T. and Renaud, F. (1996). Inference of parasite induced host mortality from distributions of parasite loads. Ecology 77, 2203–2211.CrossRefGoogle Scholar
Sage, R. D., Heyneman, D., Lim, K.-C. and Wilson, A. C. (1986). Wormy mice in a hybrid zone. Nature, London 324, 60–63.CrossRefGoogle Scholar
Sandland, G. J., Foster, A. V., Zavodna, M. and Minchella, D. J. (2007). Interplay between host genetic variation and parasite transmission in the Biomphalaria glabrata-Schistosoma mansoni system. Parasitology Research 101, 1083–1089.CrossRefGoogle ScholarPubMed
SAS Institute Inc. (2000). Statistics, SAS Campus Drive, Cary, North Carolina, USA.Google Scholar
Schultz, R. J. (1969). Hybridization, unisexuality, and polyploidy in the teleost Poeciliopsis (Poecilidae) and other vertebrates. The American Naturalist 103, 605–619.CrossRefGoogle Scholar
Semlitsch, R. D. 1993. Asymmetric competition in mixed populations of tadpoles of the hybridogenetic Rana esculenta complex. Evolution 47, 510–519.CrossRefGoogle ScholarPubMed
Schotthoefer, A. M., Cole, R. A. and Beasley, V. R. (2003). Relationship of tadpole stage to location of echinostome cercariae encystment and the consequences for tadpole survival. Journal of Parasitology 89, 475–482.CrossRefGoogle ScholarPubMed
Thiemann, G. W. and Wasserzug, R. J. (2000 a). Biased distribution of trematode metacercariae in the nephric system of Rana tadpoles. Journal of Zoology 252, 534–538.CrossRefGoogle Scholar
Thiemann, G. W. and Wasserzug, R. J. (2000 b). Patterns and consequences of behavioural responses to predators and parasites in Rana tadpoles. Biological Journal of the Linnean Society 71, 513–528.CrossRefGoogle Scholar
Tunner, H. G. (1974). Die klonale Struktur einer Wasserfroschpopulation. Zeitschrift für zoologishe Systematik und Evolutionforschung 12, 309–314.CrossRefGoogle Scholar
Tunner, H. G. and Nopp, H. (1979). Heterosis in the common European waterfrog. Naturwissenschaften 66, 268–269.CrossRefGoogle Scholar
Volgar, L. G. (1959). Adaptation of the nematode Thelandros tba (Dinnik, 1930) to the peculiarities in the life cycle of its host. Doklady Akademii Nauk SSSR 124, 1375–1376.Google Scholar
Vrijenhoeck, R. C. (1994). Unisexual fish: model systems for studying ecology and evolution. Annual Reviews in Ecology and Systematics 25, 71–96.CrossRefGoogle Scholar
Whitman, T. G. (1989). Plant hybrid zones as sinks for pests. Science 244, 1490–1493.Google Scholar
Wilson, K., Grenfeld, B. T. and Shaw, D. J. (1996). Analysis of aggregated parasite distributions: A comparison of methods. Functional Ecology 10, 592–601.CrossRefGoogle Scholar
Wolinska, J., Keller, B., Bittner, K., Lass, S. and Spaak, P. (2004). Do parasites lower Daphnia hybrid fitness? Limnology and Oceanography 49, 1401–1407.CrossRefGoogle Scholar
Wolinska, J., Keller, B., Manca, M. and Spaak, P. (2007). Parasite survey of a Daphnia hybrid complex: host-specificity and environment determine infection. Journal of Animal Ecology 76, 191–200.CrossRefGoogle ScholarPubMed
Wolinska, J., Lively, C. M. and Spaak, P. (2008). Parasites in hybridizing communities: the Red Queen again? Trends in Parasitology 24, 121–126.CrossRefGoogle Scholar
Zorn, C. J. W. (1996). Evaluating zero-inflated and hurdle Poisson specifications. Midwest Political Science Association, April 18–20, pp. 1–16.Google Scholar