Lung Parasites in the Water Frog Hybridization Complex Pierre Joly, Vanessa Guesdon, Emmanuelle Gilot-Fromont, Sandrine Plénet, Odile Grolet, J.F
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Heterozygosity and parasite intensity : lung parasites in the water frog hybridization complex Pierre Joly, Vanessa Guesdon, Emmanuelle Gilot-Fromont, Sandrine Plénet, Odile Grolet, J.F. Guégan, S. Hurtrez-Boussès, F. Thomas, F. Renaud To cite this version: Pierre Joly, Vanessa Guesdon, Emmanuelle Gilot-Fromont, Sandrine Plénet, Odile Grolet, et al.. Heterozygosity and parasite intensity : lung parasites in the water frog hybridization complex. Para- sitology, Cambridge University Press (CUP), 2007, 135 (1), pp.95-104. 10.1017/S0031182007003599. halsde-00222991 HAL Id: halsde-00222991 https://hal.archives-ouvertes.fr/halsde-00222991 Submitted on 17 May 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Heterozygosity and parasite intensity: lung parasites in the water frog hybridization complex P. JOLY1*, V. GUESDON1,E.FROMONT2,S.PLENET1, O. GROLET1, J. F. GUEGAN3, S. HURTREZ-BOUSSES3,F.THOMAS3 and F. RENAUD3 1 UMR 5023 Ecology of Fluvial Hydrosystems, Universite´Claude Bernard Lyon1, F-69622 Villeurbanne, France 2 UMR 5558 Biometry and Evolutionary Biology, Universite´Claude Bernard Lyon1, F-69622 Villeurbanne, France 3 UMR CNRS-IRD 9926, Centre for the Study of Micro-organism Polymorphism, 911 Avenue Agropolis – BP 5045, F-34032 Montpellier Cedex 1, France 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. Key words: hybrid, hybridogenesis, water frogs, Rana species, lung parasites, Rhabdias bufonis, Haplometra cylindracea. INTRODUCTION divergence between susceptibility and resistance, taking advantage of the hybridogenetic system of the Because hybridization produces innovative genetic water frogs of the Rana lessonae-esculenta complex. combinations by joining two different genomes, In a hybridogenetic complex, the genome of one performance analysis of hybrid individuals may parental species carries distorter genes, which induce contribute to the study of host-parasite coevolution the elimination of the genome material of the other (Moulia et al. 1995; Arnold, 1997). The current parental species before meiosis in the germ line concepts about the evolution of hybrid-parasite sys- of hybrids (Schultz, 1969; Tunner 1974; Joly 2001). tems do not, however, allow the proposal of mono- The distorter genome is then duplicated and the lithic hypotheses, probably because of the great gametes of hybrid individuals carry only the genome diversity of genetic associations covered by the term of one of the parental species. These hybrids usually ‘hybridization’ (from subspecies to genus). While breed with the taxon whose genome is eliminated, hybridization between phylogenetically distant gen- thus restoring the hybridness of their descent (sexual omes is expected to promote high susceptibility to parasitism). In the hybrid lineages, the distorter the parasite, because of breakdown of genetic co- genome is transmitted clonally (hemiclones). Be- adaptation, hybridization between closely related cause of the lack of recombination between the taxa could enhance resistance through a heterosis parental genomes (cf Pagano and Schmeller, 1999), effect (Sage et al. 1986; Dupont and Crivelli, 1988; hybrids are genetically similar to F1 hybrids. In one Whitman, 1989; Moulia, 1999). The hypotheses of the water frog complexes (R. lessonae [LL genome] established by Fritz et al. (1999) for predicting the and its hybridogen R. esculenta [RL genome], which impact of herbivory in plants provide an initial carries a ridibunda [R hemigenome]), the success of theoretical framework for the study of parasite- hybrid lineages has been widely analysed; several hybrid systems. Our aim was to focus on the studies (Tunner and Nopp, 1979; Berger and Uzzell, 1980; Semlitsch, 1993, Hotz et al. 1999) support the hypothesis of heterotic advantage with respect * Corresponding author: UMR 5023 Ecology of Fluvial Hydrosystems, Universite´ Claude Bernard Lyon1, F- to fecundity, predation avoidance or hypoxic toler- 69622 Villeurbanne, France. Tel: +33 472 433 586. Fax: ance of froglets (heterosis effect). However, other 33 472 431 141. E-mail: [email protected] studies (Pagano et al. 2001; Ple´net et al. 2000a, b, 1 2005; Negovetic et al. 2001) support a simple addi- whereas females were frozen until performing tissue tive hypothesis with regard to habitat use, hypoxic sampling and measurements. Length from snout to tolerance of tadpoles and thermal tolerance (inter- urostyle was measured to the closest 0.1 mm using mediate performances of the hybrids). The water callipers. We measured body mass after removing frog hybridization complex thus makes it possible the ovaries, which were weighed separately. We to investigate in situ the relationship between hy- estimated body condition by the residuals of the bridization and parasite infection by comparing the regression of body mass on body length, both infection rates of 2 taxa (the hybrid Rana esculenta measurements being converted into natural logar- and the sexual host R. lessonae) that occur con- ithms. This index was used because it was shown to comitantly in the same habitats (Rana ridibunda be independent of the population under consider- usually does not occur in the same habitats as ation (Jakob et al. 1996). Body condition was defined R. lessonae). Water frogs host a great diversity of independently for each genotype, because the re- parasites (Walton, 1949; Saglam and Arikan, 2006) lationship between body mass and length was con- of which we studied the infection with lung parasites sidered to vary according to the genotype considered. Rhabdias bufonis (Nematoda) and Haplometra cylin- We identified parental species from hybrids by dracea (Trematoda). In the present study, our aim specific allozymic markers detected by protein was to compare the intensity of parasite infection electrophoresis of finger tissue using lactate de- between the two taxa of 3 populations occupying hydrogenase (LDH-B; EC 1.1.1.27) and mannose-6- fishponds in eastern France. We took advantage phosphate isomerase (MPI; EC 5.3.1.8) (Beerli, of the possibility of determining individual ages by 1994; Pagano et al. 1997). We estimated individual means of skeletochronology, in order to analyse the age by skeletochronology performed on finger bones relationships between age, mortality and parasite (Castanet et al. 1977; Augert and Joly, 1993). accumulation. Lung parasites MATERIALS AND METHODS We elected to specifically study lung parasites after Study sites performing a preliminary analysis of the parasite intensity of the whole body (40 frogs examined). The The frogs were sampled on the Dombes Plateau parasite fauna was mainly composed of roundworms (north-east of Lyon, France), where 1000 fishponds and flukes in the digestive tract and in the lungs. devoted to growing carp are distributed over a 2 Because lung parasites (Rhabdias bufonis and Haplo- 900 km area. Water frogs of the LE hybridogenetic metra cylindracea) were frequent and their damage complex occur in high densities at the banks of these to lung tissues was expected to be more severe than ponds. We sampled the frogs at 3 ponds: Boufflers that of gastrointestinal parasites, we focussed on pond (designated as POND A) which is within them. While we identified the roundworm as Rhab- the estate of the Pierre Ve´rots Foundation, Saint- dias bufonis, the recent discovery of new species x k x k Jean-de-Thurigneux (4 51 E-45 56 N), La Tille identified in North and Central America (Tkach pond (POND B) at Saint-Andre´-le-Bouchoux et al. 2006; Kuzmin et al. 2007) suggests that the x k x k (5 55 E-46 59 N) and a third pond (POND C) of taxonomy of the genus Rhabdias needs to be revised. the Regional Research Institute for Aquaculture However, we decided to use this taxon name until x k x k (IRRA) at Saint-Nizier-le-De´sert