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

Parasitology

Volumn 136, Issue 9, 2009, Pages 1003-1013

  Planade, B ^a   Lena, J P ^a   Li, H ^a,c   Plenet, S ^a   Guegan, J F ^b   Thomas, F ^b   Hurtrez Bousses, S ^b   Renaud, F ^b   Joly, P ^a  

^a UNIVERSITÉ LYON 1   (France)

^b INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^c VA PALO ALTO HEALTH CARE SYSTEM   (United States)

Author keywords

Echinostome metacercariae; Gyrinicola sp.; Hemiclonal selection; Heterosis effect

Indexed keywords

ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ECHINOSTOMA; FROG; GYRINICOLA; HABITAT; HAPLOMETRA CYLINDRACEA; HETEROSIS; HOST RESISTANCE; HYBRID; KIDNEY; METACERCARIA; NEMATODE; NONHUMAN; ORGANISM HYBRIDIZATION; PRIORITY JOURNAL; SPECIES DIVERSITY; TADPOLE; TREMATODE; ANIMAL; ECOSYSTEM; FROGS AND TOADS; GENETIC PREDISPOSITION; GENETICS; HOST PARASITE INTERACTION; LARVA; PARASITOLOGY; PHYSIOLOGY;

ANURA; HAPLOMETRA CYLINDRACEA; NEMATODA; RANA ESCULENTA; TREMATODA;

ANIMALS; ANURA; ECOSYSTEM; GENETIC PREDISPOSITION TO DISEASE; HOST-PARASITE INTERACTIONS; HYBRID VIGOR; LARVA; NEMATODA; TREMATODA;

EID: 70349562253     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182009006489     Document Type: Article

References (64)

1. 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.
2. Adamson, M. L. (1981). Development and transmission of Gyrinicola batrachiensis (Walton, 1929) Adamson, 1981 (Pharyngodonidae: Oxyuridea). Canadian Journal of Zoology 59, 1351-1367.
3. Bakke, T. A., Soleng, A. and Harris, P. D. (1999). The susceptibility of Atlantic salmon (Salmo salar L.)rbrown trout (Salmo trutta L.) hybrids to Gyrodactylus salaris Malmberg and Gyrodactylus derjavini Mikailov. Parasitology 119, 467-481.
4. 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.
5. Buchmann, K. and Lindenström, T. (2002). Interactions between monogenean parasites and their fish hosts. International Journal for Parasitology 32, 309-319.
6. Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multimodel Inference: a Practical Information-Theoretic Approach, Springer-Verlag, New York, USA.
7. 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.
8. Combes, C. (2001). Ecology and Evolution of Intimate Interactions. Chicago U. P., Chicago, USA.
9. 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.
10. 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.
11. Dupont, F. and Crivelli, A. J. (1988). Do parasites confer a disadvantage to hybrids? A case study of Alburnus alburnusrRutilus rubilio, a natural hybrid of Lake Mikri Prespa, Northern Greece. Oecologia 75, 587-592.
12. 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.
13. 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.
14. Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183-190.
15. Grabda-Kazubska, B. (1970). Studies on the life-cycle of Haplometra cylindrica (Zeder 1800) (Trematoda:Plagiorchidae). Acta Parasitologica Polonica 18, 497-512.
16. 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.
17. Hellriegel, B. and Reyer, H. U. (2000). Factors in.uencing the composition of mixed populations of a hemiclonal hybrid and its sexual host. Journal of Evolutionary Biology 13, 906-918.
18. 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.
19. 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.
20. 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.
21. 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.
22. 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.
23. Joly, P. and Morand, A. (1994). Theoretical habitat templets, species traits, and species richness: amphibian in the Upper Rhône and its fioodplain. Freshwater Biology 31, 455-468.
24. 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.
25. Koprivnikar, J., Forbes, M. R. and Baker, R. L. (2006). On the effcacy of anti-parasite behaviour: a case study of tadpole susceptibility to cercariae of Echinostoma trivolvis. Canadian Journal of Zoology 84, 1623-1629.
26. 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.
27. Lengagne, T., Plé net, 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.
28. Lively, C. M. and Dybdahl, M. E. (2000). Parasite adaptation to locally common host genotypes. Nature, London 405, 679-681.
29. 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.
30. Moore, W. S. (1977). An evaluation of narrow hybrid zones in vertebrates. The Quarterly Review of Biology 52, 263-277.
31. Moulia, C. (1999). Parasitism of plant and animal hybrids: are facts and fate the same? Ecology 80, 392-406.
32. 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.
33. 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.
34. Mullahy, J. (1986). Specification and testing of some modified count data models. Journal of Econometrics 33, 341-365.
35. 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.
36. 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.
37. 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.
38. 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.
39. Plénet, S., Hervant, F. and Joly, P. (2000a). Ecology of the hybridogenetic Rana esculenta complex: differential oxygen requirements of tadpoles. Evolutionary Ecology 14, 13-23. (Pubitemid 32402527)
40. 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.
41. Plénet, S., Pagano, A., Joly, P. and Fouillet, P. (2000b). Variation of plastic responses to oxygen availability within the hybridogenetic Rana esculenta complex. Journal of Evolutionary Biology 13, 20-28.
42. Potts, J. M. and Elith, J. (2006). Comparing species abundance models. Ecological Modelling 199, 153-163.
43. Prudhoe, S. and Bray, R. A. (1982). Platyhelminth Parasites of the Amphibia, Oxford University Press, Oxford, UK.
44. 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.
45. 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.
46. 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.
47. Sage, R. D., Heyneman, D., Lim, K.-C. and Wilson, A. C. (1986). Wormy mice in a hybrid zone. Nature, London 324, 60-63.
48. 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.
49. SAS Institute Inc. (2000). Statistics, SAS Campus Drive, Cary, North Carolina, USA.
50. Schultz, R. J. (1969). Hybridization, unisexuality, and polyploidy in the teleost Poeciliopsis (Poecilidae) and other vertebrates. The American Naturalist 103, 605-619.
51. Semlitsch, R. D. 1993. Asymmetric competition in mixed populations of tadpoles of the hybridogenetic Rana esculenta complex. Evolution 47, 510-519.
52. 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.
53. Thiemann, G. W. and Wasserzug, R. J. (2000a). Biased distribution of trematode metacercariae in the nephric system of Rana tadpoles. Journal of Zoology 252, 534-538.
54. Thiemann, G. W. and Wasserzug, R. J. (2000b). Patterns and consequences of behavioural responses to predators and parasites in Rana tadpoles. Biological Journal of the Linnean Society 71, 513-528.
55. Tunner, H. G. (1974). Die klonale Struktur einer Wasserfroschpopulation. Zeitschrift für zoologishe Systematik und Evolutionforschung 12, 309-314.
56. Tunner, H. G. and Nopp, H. (1979). Heterosis in the common European waterfrog. Naturwissenschaften 66, 268-269.
57. 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.
58. Vrijenhoeck, R. C. (1994). Unisexual fish: model systems for studying ecology and evolution. Annual Reviews in Ecology and Systematics 25, 71-96.
59. Whitman, T. G. (1989). Plant hybrid zones as sinks for pests. Science 244, 1490-1493.
60. Wilson, K., Grenfeld, B. T. and Shaw, D. J. (1996). Analysis of aggregated parasite distributions : A comparison of methods. Functional Ecology 10, 592-601.
61. Wolinska, J., Keller, B., Bittner, K., Lass, S. and Spaak, P. (2004). Do parasites lower Daphnia hybrid fitness? Limnology and Oceanography 49, 1401-1407.
62. 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.
63. Wolinska, J., Lively, C. M. and Spaak, P. (2008). Parasites in hybridizing communities: the Red Queen again? Trends in Parasitology 24, 121-126.
64. Zorn, C. J. W. (1996). Evaluating zero-infiated and hurdle Poisson specifications. Midwest Political Science Association, April 18-20, pp. 1-16.