BACKGROUND: The composition of parasite communities in two cyprinid species in southern France - native and threatened Parachondrostoma toxostoma and introduced Chondrostoma nasus - was investigated. In sympatry, these two species form two hybrid zones in the Durance and Ardeche Rivers. Due to their different feeding preference and habitat positions in allopatry, we supposed a difference in parasite communities between fish species. We expected more similar parasite communities in sympatric zones associated with habitat overlap (facilitating the transmission of ectoparasites) and similar feeding (more generalist behaviour when compared to allopatry, facilitating the transmission of endoparasites) in both fish species. Finally, we investigated whether P. toxostoma x C. nasus hybrids are less parasitized then parental species. METHODS: One allopatric population of each fish species plus two sympatric zones were sampled. Fish were identified using cytochrome b gene and 41 microsatellites loci and examined for all metazoan parasites. RESULTS: A high Monogenea abundance was found in both allopatric and sympatric populations of C. nasus. Trematoda was the dominant group in parasite communities of P. toxostoma from the allopatric population. In contrast, the populations of P. toxostoma in sympatric zones were parasitized by Dactylogyrus species found in C. nasus populations, but their abundance in endemic species was low. Consequently, the similarity based on parasite presence/absence between the sympatric populations of P. toxostoma and C. nasus was high. Sympatric populations of P. toxostoma were more similar than allopatric and sympatric populations of this species. No difference in ectoparasite infection was found between P. toxostoma and hybrids, whilst C. nasus was more parasitized by Monogenea. CONCLUSIONS: The differences in endoparasites between P. toxostoma and C. nasus in allopatry are probably linked to different feeding or habitat conditions, but host-parasite evolutionary associations also play an important role in determining the presence of Chondrostoma-specific monogeneans. Our findings suggest that Dactylogyrus expanded with the source host C. nasus into introduced areas and that P. toxostoma became infected after contact with C. nasus. Although the genotype of P. toxostoma and recombinant genotypes of hybrids are susceptible to Dactylogyrus transmitted from C. nasus, the intensity of infection is low in these genotypes.

Department of Botany and Zoology Masaryk University Brno Czech Republic

Zobrazit více v PubMed

Bohn T, Amundsen PA. The competitive edge of an invading specialist. Ecology. 2001;82:2150–2163.

Kelly DW, Patterson RA, Townsend CR, Poulin R, Tompkins DM. Parasite spillback: A neglected concept in invasion ecology? Ecology. 2009;90:2047–2056. doi: 10.1890/08-1085.1. PubMed DOI

Dunn AM. Parasites and biological invasions. Adv Parasit. 2009;68:161–184. PubMed

Poulin R, Paterson RA, Townsend CR, Tompkins DM, Kelly DW. Biological invasions and the dynamics of the endemic diseases in freshwater ecosystems. Freshwater Biol. 2011;56:676–688. doi: 10.1111/j.1365-2427.2010.02425.x. DOI

Keane RM, Crawley MJ. Exotic plants invasions and the enemy release hypothesis. Trends Ecol Evol. 2002;17:164–170. doi: 10.1016/S0169-5347(02)02499-0. DOI

Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM. Introduced species and their missing parasites. Nature. 2003;421:628–630. doi: 10.1038/nature01346. PubMed DOI

Colautti RI, Ricciardi A, Grigorovich IA, MadIsaac HJ. Is invasion success explained by the enemy release hypothesis? Ecol Lett. 2004;7:721–733. doi: 10.1111/j.1461-0248.2004.00616.x. DOI

Prenter J, MacNeil C, Dick JTA, Dunn AM. Roles of parasites in animal invasions. Trends Ecol Evol. 2004;19:385–390. doi: 10.1016/j.tree.2004.05.002. PubMed DOI

Taraschewski H. Host and parasites as aliens. J Helminthol. 2006;80:99–128. doi: 10.1079/JOH2006364. PubMed DOI

Elvira B, Almodovar A. Freshwater fish introductions in Spain: facts and figures at the beginning of the 21st century. J Fish Biol. 2001;59:232–331.

Moulia C, Le Brun N, Loubes C, Marin R, Renaud F. Hybrid vigor against parasites in interspecific crosses between 2 mice species. Heridity. 1995;74:48–52. doi: 10.1038/hdy.1995.6. PubMed DOI

Goldberg SR, Bursey CR, Malmos KB, Sullivan BK, Cheam H. Helminths of the southwestern toad, Bufo microscaphus, woodhouse´s toad, Bufo woodhousii (Bufonidae), and their hybrids from central Arizona. Great Basin Nat. 1996;56:369–374.

Hedrick RP, Waltzek TB, McDowell TS. Susceptibility of koi carp, common carp, goldfish, and goldfish x common carp hybrids to cyprinid herpesvirus-2 and herpesvirus-3. J Aquat Anim Health. 2006;18:26–34. doi: 10.1577/H05-028.1. DOI

Sage RD, Heynemen D, Lim KC, Wilson AC. Wormy mice in hybrid zone. Nature. 1986;324:60–63. doi: 10.1038/324060a0. PubMed DOI

Moulia C, Aussel JP, Bonhomme F, Boursot P, Nielsen JT, Renaud F. Wormy mice in a hybrid zone: a genetic control of susceptibility to parasite infection. J Evol Biol. 1991;4:679–687. doi: 10.1046/j.1420-9101.1991.4040679.x. DOI

Moulia C, Le Brun N, Dallas J, Orth A, Renaud F. Experimental evidence of genetic determinism in high susceptibility to intestinal pinworms infection in mice: a hybrid zone model. Parasitology. 1993;106:387–393. doi: 10.1017/S0031182000067135. PubMed DOI

Derothe J-M, Loubes C, Perriat-Sanguinet M, Orth A, Moulia C. Experimental trypanosomiasis of natural hybrids between House Mouse subspecies. Int J Parasitol. 1999;29:1011–1016. doi: 10.1016/S0020-7519(99)00069-7. PubMed DOI

Derothe J-M, Le Brun N, Loubes C, Perriat-Sanguinet M, Moulia C. Susceptibility of natural hybrids between house mouse subspecies to Sarcocystis muris. Int J Parasitol. 2001;31:15–19. doi: 10.1016/S0020-7519(00)00155-7. PubMed DOI

Matondo BN, Ovidio M, Poncin P, Kakesa TA, Wamuini LS, Philippart JC. Hybridization success of three common European cyprinid species, Rutilus rutilus,Blicca bjoerkna and Abramis brama and larval resistance to stress tests. Fisheries Sci. 2007;73:1137–1146. doi: 10.1111/j.1444-2906.2007.01445.x. DOI

Vetešník L, Halačka K, Papoušek I, Mendel J, Šimková A. The first record of a natural hybrid of the roach Rutilus rutilus and nase Chondrostoma nasus in the Danube River Basin, Czech Republic: morphological, karyological and molecular characteristics. J Fish Biol. 2009;74:1669–1676. doi: 10.1111/j.1095-8649.2009.02220.x. PubMed DOI

Toscano BJ, Pulcini D, Hayden B, Russo T, Kelly-Quinn M, Mariani S. An ecomorphological framework for the coexistence of two cyprinid fish and their hybrids in a novel environment. Biol J Linn Soc. 2010;99:768–783. doi: 10.1111/j.1095-8312.2010.01383.x. DOI

Crespin L, Berrebi P, Lebreton J-D. Asymmetrical introgression in a freshwater fish hybrid zone as revealed by a morphological index of hybridization. Biol J Linn Soc. 1999;67:57–72. doi: 10.1111/j.1095-8312.1999.tb01929.x. DOI

Costedoat C, Pech N, Chappaz R, Salducci MD, Lim P, Gilles A. Étude de l´hybridation introgressive entre Chondrostoma t. toxostoma et Chondrostoma n. nasus (Téléostéen, Cyprinidae) en utilisant une approach multiple. Cybium. 2004;28:51–61.

Costedoat C, Pech N, Chappaz R, Gilles A. Novelties in hybrid zones: crossroads between population genomic and ecological approaches. PLoS One. 2007;2(4):e357. doi: 10.1371/journal.pone.0000357. PubMed DOI PMC

Corse E, Nève G, Sinama M, Pech N, Costedoat C, Chappaz R, Gilles A. Plasticity of ontogenetic trajectories in cyprinids: a source of evolutionary novelties. Biol J Lin Soc. 2012;106:342–355. doi: 10.1111/j.1095-8312.2012.01873.x. DOI

Chappaz R, Brun G, Olivari G. New data about biology and ecology of a little-studied fish: Parachondrostoma toxostoma (Vallot, 1836). Comparison with nase, Chondrostoma nasus (L.,1766) Comp Rend Acad Sci, Ser 3. 1989;309:181–186.

Corse E, Costedoat C, Chappaz R, Pech N, Martin JF, Gilles A. A PCR-based method for diet analysis in freshwater organisms using 18SrDNA barcoding on faeces. Mol Ecol Res. 2010;10:96–108. doi: 10.1111/j.1755-0998.2009.02795.x. PubMed DOI

Nelva A. Biogéographie, Démographie et Écologie de Chondrostoma nasus (L., 1758) (Hotu, Poisson, Teléosteen, Cyprinidé) PhD thesis, Université Claude Bernard - Lyon I, Lyon; 1985. in French.

Freyhoff J. Feeding traces as an indicator of habitat choice in nase, Chondrostoma nasus. Folia Zool. 1995;44:57–61.

Corse E, Costedoat C, Pech N, Chappaz R, Grey J, Gilles A. Trade-off between morphological convergence and opportunistic diet behaviour in fish hybrid zone. Front Zool. 2009;6:26. doi: 10.1186/1742-9994-6-26. PubMed DOI PMC

Ergens R, Lom J. Causative agents of fish diseases. Prague: Academia; 1970. (in Czech)

Rohlenová K, Morand S, Hyršl P, Tolárová S, Flajšhans M, Šimková A. Are fish immune systems really affected by parasites? An immunoecological study of common carp (Cyprinus carpio) Parasites and Vectors. 2011;4:120. doi: 10.1186/1756-3305-4-120. PubMed DOI PMC

Costedoat C, Pech N, Salducci MD, Chappaz R, Gilles A. Evolution of mosaic hybrid zone between invasive and endemic species of Cyprinidae through space and time. Biol J Linn Soc. 2005;85:135–155. doi: 10.1111/j.1095-8312.2005.00478.x. DOI

Dubut V, Sinama M, Martin JF, Meglecz E, Fernandez J, Chappaz R, Gilles A, Costedoat C. Cross-species amplification of 41 microsatellites in European cyprinids: A tool for evolutionary, population genetics and hybridization studies. BMC Res Notes. 2010;3:135. doi: 10.1186/1756-0500-3-135. PubMed DOI PMC

Chatterji S, Pachter L. Reference based annotation with GeneMapper. Genome Biol. 2006;7:R29. doi: 10.1186/gb-2006-7-4-r29. PubMed DOI PMC

Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes. 2004;4:535–538. doi: 10.1111/j.1471-8286.2004.00684.x. DOI

Anderson EC, Thompson EA. A model-based method for identifying species hybrids using multilocus genetic data. Genetics. 2002;160:1217. PubMed PMC

Szpiech ZA, Jakobsson M, Rosenberg NA. ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics. 2008;24:2498. doi: 10.1093/bioinformatics/btn478. PubMed DOI PMC

Excoffier L, Laval G, Schneider S. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform. 2005;1:47. PubMed PMC

Coulon A. GENHET: an easy-to-use R function to estimate individual heterozygosity. Mol Ecol Res. 2010;10:167–169. doi: 10.1111/j.1755-0998.2009.02731.x. PubMed DOI

Magurran A. Ecological diversity and its measurement. London: Croom. Helm; 1988.

Loot G, Reyjol Y, Poulet N, Šimková A, Blanchet S, Lek S. Effects on small weirs on fish parasite communities. Parasitol Res. 2007;101:775–489. doi: 10.1007/s00436-007-0546-3. PubMed DOI

Šimková A, Morand S, Jobet E, Gelnar M, Verneau O. Molecular phylogeny of congeneric monogenean parasites (Dactylogyrus): a case of intra-host speciation. Evolution. 2004;58:1001–1018. PubMed

Bakke TA, Soleng A, Hartus PD. The susceptibility of Atlantic salmon (Salmo salar L.) x brown trout (Salmo trutta L.) hybrids to Gyrodactylus salaris Malmberg and Gyrodactylus derjavini Mikailov. Parasitology. 1999;119:467–481. doi: 10.1017/S0031182099004990. PubMed DOI

Dupont F, Crivelli AJ. Do parasite confer a disadvantage to hybrids? A case study of Alburnus alburnus x Rutilus rubilio, a natural hybrid of Lake Mikcri Prespa, Northern Greece. Oecologia. 1988;75:587–592. doi: 10.1007/BF00776424. PubMed DOI

Corse E. Le „barcoding alimentaire“: développement d’un nouvel outil d’écologie moléculaire pour les milieux d’eau douce. Exemple au travers de l’étude de la zone hybride Durance entre les deux Chondrostomes français. PhD thesis. Université de Provence, Marseille; 2010. in French.

Le Brun N, Renaud F, Berrebi P, Lambert A. Hybrid zones and host-parasite relationships: effect on the evolution of parasitic specificity. Evolution. 1992;46:56–61. doi: 10.2307/2409804. PubMed DOI

The parasites of a successful invader: monogeneans of the Asian topmouth gudgeon Pseudorasbora parva, with description of a new species of Gyrodactylus

Diversity of MHC IIB genes and parasitism in hybrids of evolutionarily divergent cyprinoid species indicate heterosis advantage

Distribution of host-specific parasites in hybrids of phylogenetically related fish: the effects of genotype frequency and maternal ancestry?

Metazoan parasite communities: support for the biological invasion of Barbus barbus and its hybridization with the endemic Barbus meridionalis

Genomic Porosity between Invasive Chondrostoma nasus and Endangered Endemic Parachondrostoma toxostoma (Cyprinidae): The Evolution of MHC IIB Genes

Does interspecies hybridization affect the host specificity of parasites in cyprinid fish?