Evolutionary divergence of the swim bladder nematode Anguillicola crassus after colonization of a novel host, Anguilla anguilla

BMC Evolutionary Biology

Horst Taraschewski¹  Yu San Han²  Trevor Petney¹  Bernhard Klar³  Tobias Baust³  Emanuel G Heitlinger¹  Urszula Weclawski¹ 

[1] Department of Ecology and Parasitology, Zoological Institute, Karlsruhe Institute of Technology, Kornblumenstrasse 13, Karlsruhe, Germany;Institute of Fisheries Science, College of Life Science, National Taiwan University, Taipei, Taiwan;Department of Stochastics, Karlsruhe Institute of Technology, Kaiserstrasse 89, Karlsruhe, Germany

关键词: Phenotypic plasticity;    Genetic divergence;    Rapid evolution;    Host switch;    Invasive;    Anguillicoloides crassus;    Anguillicola crassus;   

Others  :  1129303
DOI  :  10.1186/1471-2148-13-78

 received in 2012-12-12, accepted in 2013-03-20,  发布年份 2013

【 摘 要 】

Background

Anguillicola crassus, a swim bladder nematode naturally parasitizing the Japanese eel, was introduced about 30 years ago from East Asia into Europe where it colonized almost all populations of the European eel. We conducted a common garden experiment under a reciprocal transfer design infecting both European and Japanese eels with populations of A. crassus from Germany, Poland and Taiwan. We tested, whether differences in infectivity, developmental dynamics and reproductive output between the European and Asian parasite populations occur while harboured in the specimens of native and colonized eel host, and if these differences are genetically based or are plastic responses to the new environment.

Results

Under common garden conditions an evolutionary change in the both European parasite populations of A. crassus compared with their Taiwanese conspecifics was observed for infectivity and developmental dynamics, but not for reproductive output. When infecting the European eel, current European populations of the parasite were less infective and developed faster than their Taiwanese conspecifics. In the reciprocally infected Japanese eel the genetically induced differences between the parasite strains were less apparent than in the European eel but higher infectivity, faster development and higher larval mortality of the European parasite populations could be inferred.

Conclusions

The differences in infectivity and developmental dynamics between European and Taiwanese populations of A. crassus found in our study suggest rapid genetic divergence of this parasite after a successful host switch in Europe.

【 授权许可】

   
2013 Weclawski et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Lonsdale W: Global patterns of plant invasions and the concept of invasibility. Ecology 1999, 80:1522-1536.
• [2]Mack RN, Simberloff D, Mark Lonsdale W, Evans H, Clout M, Bazzaz FA: Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 2000, 10:689-710.
• [3]Reznick DN, Ghalambor CK: The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 2001, 112:183-198.
• [4]Lee CE: Evolutionary genetics of invasive species. Trends Ecol Evolut 2002, 17:386-391.
• [5]Facon B, Genton BJ, Shykoff J, Jarne P, Estoup A, David P: A general eco-evolutionary framework for understanding bioinvasions. Trends Ecol Evolut 2006, 21:130-135.
• [6]Poulin R: Interactions between species and the structure of helminth communities. Parasitology 2001, 122:3-11.
• [7]Taraschewski H: Hosts and parasites as aliens. J Helminthol 2006, 80:99-128.
• [8]Kirk RS: The impact of Anguillicola crassus on European eels. Fish Manag Ecol 2003, 10:385-394.
• [9]Poulin R, Krasnov BR, Mouillot D: Host specificity in phylogenetic and geographic space. Trends Parasitol 2011, 27:355-361.
• [10]Knopf K: The swimbladder nematode Anguillicola crassus in the European eel Anguilla anguilla and the Japanese eel Anguilla japonica: differences in susceptibility and immunity between a recently colonized host and the original host. J Helminthol 2006, 80:129-136.
• [11]Schabuss M, Kennedy CR, Konecny R, Grillitsch B, Reckendorfer W, Schiemer F, Herzig A: Dynamics and predicted decline of Anguillicola crassus infection in European eels, Anguilla anguilla. Neusiedler See, Austria. J Helminthol 2005, 79:159-167.
• [12]Neumann W: Schwimmblasenparasit Anguillicola bei Aalen. Fisch Teichwirt 1985, 11:322.
• [13]Wielgoss S, Taraschewski H, Meyer A, Wirth T: Population structure of the parasitic nematode Anguillicola crassus, an invader of declining North Atlantic eel stocks. Mol Ecol 2008, 17:3478-3495.
• [14]Moravec F: Dracunculoid and Anguillicoloid Nematodes Parasitic in Vertebrates. Praha: Academia; 2006.
• [15]Laetsch DR, Heitlinger EG, Taraschewski H, Nadler SA, Blaxter ML: The phylogenetics of Anguillicolidae (Naematoda: Anguillicolidea), swimbladder parasites of eels. BMC Evol Biol 2012, 12:60. BioMed Central Full Text
• [16]De Charleroy D, Grisez L, Thomas K, Belpaire C, Ollevier F: The life cycle of Anguillicola crassus. Dis Aquat Org 1990, 8:77-84.
• [17]Sures B, Knopf K, Taraschewski H: Development of Anguillicola crassus (dracunculoidea, anguillicolidae) in experimentally infected Balearic congers ariosoma balearicum (Anguilloidea, Congridae). Dis Aquat Org 1999, 39:75-78.
• [18]Szekely C: Paratenic hosts for the parasitic nematode Anguillicola crassus in Lake Balaton, Hungary. Dis Aquat Org 1994, 18:11-20.
• [19]Moravec F: Aquatic invertebrates (snails) as new paratenic hosts of Anguillicola crassus (Nematoda: Dracunculoidea) and the role of paratenic hosts in the life cycle of this parasite. Dis Aquat Org 1996, 27:237-239.
• [20]Knopf K, Mahnke M: Differences in susceptibility of the European eel (Anguilla Anguilla) and the Japanese eel (Anguilla japonica) to the swim-bladder nematode anguillicola crassus. Parasitology 2004, 129:491-496.
• [21]Nuismer SL, Gandon S: Moving beyond common-garden and transplant designs: insight into the causes of local adaptation in species interactions. Am Nat 2008, 171:658-668.
• [22]Kerner von Marilaun A, Oliver FW: The Natural History of Plants: Their Forms, Growth, Reproduction, and Distribution. London: Blackie & Son, Ltd; 1895.
• [23]Sures B, Knopf K, Würtz J, Hirt J: Richness and diversity of parasite communities in European eels Anguilla anguilla of the River Rhine, Germany, with special reference to helminth parasites. Parasitology 1999, 119:323-330.
• [24]Fazio G, Sasal P, Da Silva C, Fumet B, Boissier J, Lecomte-Finiger R, Mone H: Regulation of Anguillicola crassus (Nematoda) infrapopulations in their definitive host, the European eel, Anguilla anguilla. Parasitology 2008, 135:1707-1716.
• [25]Würtz J, Taraschewski H: Histopathological changes in the swimbladder wall of the European eel Anguilla anguilla due to infections with Anguillicola crassus. Dis Aquat Org 2000, 39:121-134.
• [26]Fazio G, Moné H, Lecomte-Finiger R, Sasal P: Differential gene expression analysis in European eels (Anguilla anguilla, L. 1758) naturally infected by macroparasites. J Parasitol 2008, 94:571-577.
• [27]Molnár K, Székely C, Baska F: Mass mortality of eel in Lake Balaton due to Anguillicola crassus infection. Bull Eur Assn Fish P 1991, 11:211-212.
• [28]Baruš V, Halacka K, Prokes M: Presence and distribution of the nematode Anguillicola crassus in the European eel in the Morava river drainage basin, Czech Republic. Zivocisna Vyroba 1996, 41:219-224.
• [29]Ebert D: Virulence and local adaptation of a horizontally transmitted parasite. Science 1994, 265:1084-1486.
• [30]Blossey B, Notzold R: Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 1995, 83:887-889.
• [31]Wescott RB, Todd AC: Adaptation of Nippostrongylus brasiliensis to the mouse. J Parasitol 1966, 52:233-236.
• [32]Dobson C, Owen ME: Influence of serial passage on the infectivity and immunogenicity of Nematospiroides dubius in mice. Int J Parasitol 1977, 7:463-466.
• [33]Mackinnon M, Gaffney D, Read A: Virulence in rodent malaria: host genotype by parasite genotype interactions. Infect Genet Evol 2002, 1:287-296.
• [34]Mahnke M: Vergleichende Untersuchungen zur Wirkung des Schwimmblasennematoden Anguillicola crassus beim Europäischen Aal (Anguilla anguilla) und Japanischen Aal (Anguilla japonica). University of Karlsruhe: Zoological Institut I, Department of Ecology and Parasitology; 2002. [Master thesis]
• [35]Trouvé S, Sasal P, Jourdane J, Renaud F, Morand S: The evolution of life-history traits in parasitic and free-living platyhelminthes: a new perspective. Oecologia 1998, 115:370-378.
• [36]Münderle M: Ökologische, morphologische und genetische Untersuchungen an Populationen des invasiven Schwimmblasen-Nematoden Anguillicola crassus aus Europa und Taiwan. University of Karlsruhe: Zoological Institut I, Department of Ecology and Parasitology; 2005. [PhD thesis]
• [37]Paterson S, Barber R: Experimental evolution of parasite life-history traits in Strongyloides ratti (Nematoda). Proc R Soc Lond Biol 2007, 274:1467-1474.
• [38]Ewald PW: The evolution of virulence: a unifying link between parasitology and ecology. J Parasitol 1995, 81:659-669.
• [39]Rohde K: Intra-and interspecific interactions in low density populations in resource-rich habitats. Oikos 1991, 60:91-104.
• [40]Gordeeva NV, Salmenkova EA: Experimental microevolution: transplantation of pink salmon into the European North. Evol Ecol 2011, 25:1-23.
• [41]Paterson S, Viney M: Host immune responses are necessary for density dependence in nematode infections. Parasitology 2002, 125:283-292.
• [42]Fox CW, Czesak ME: Evolutionary ecology of progeny size in arthropods. Ann Rev Entomol 2000, 45:341-369.
• [43]Campbell RG, Wagner MM, Teegarden GJ, Boudreau CA, Durbin EG: Growth and development rates of the copepod Calanus finmarchicus reared in the laboratory. Mar Ecol Prog Ser 2001, 221:161-183.
• [44]David J, Gibert P, Moreteau B, Gilchrist G, Huey R: The fly that came in from the cold: geographic variation of recovery time from low-temperature exposure in Drosophila subobscura. Funct Ecol 2003, 17:425-430.
• [45]Addo-Bediako A, Chown SL, Gaston KJ: Metabolic cold adaptation in insects: a large-scale perspective. Funct Ecol 2002, 16:332-338.
• [46]Grapputo A, Boman S, Lindstroem L, Lyytinen A, Mappes J: The voyage of an invasive species across continents: genetic diversity of North American and European Colorado potato beetle populations. Mol Ecol 2005, 14:4207-4219.
• [47]James AC, Partridge L: Thermal evolution of rate of larval development in Drosophila melanogaster in laboratory and field populations. J Evol Biol 1995, 8:315-330.
• [48]James AC, Partridge L: Geographic variation in competitive ability in Drosophila melanogaster. Am Nat 1998, 151:530-537.
• [49]Mo TA, Steien SH: First observation of the eel swimbladder nematode Anguillicola crassus in Norway. Bull Eur Assoc Fish Pathol 1994, 14:163-164.
• [50]Die Landesanstalt für Umwelt, Messungen und Naturschutz Baden-Württemberg (LUBW). http://www.lubw.baden–wuerttemberg.de/servlet/is/72252/ webcite
• [51]Dlugosch KM, Parker IM: Invading populations of an ornamental shrub show rapid life history evolution despite genetic bottlenecks. Ecol Lett 2008, 11:701-709.
• [52]Kolbe JJ, Larson A, Losos JB, De Queiroz K: Admixture determines genetic diversity and population differentiation in the biological invasion of a lizard species. Biol Lett 2008, 4:434-437.
• [53]Thulin CG, Simberloff D, Barun A, Mccracken G, Pascal M, Islam MA: Genetic divergence in the small Indian mongoose (Herpestes auropunctatus), a widely distributed invasive species. Mol Ecol 2006, 15:3947-3956.
• [54]Moravec F, Di Cave D, Orecchia P, Paggi L: Present occurrence of Anguillicola novaezelandiae (Nematoda: Dracunculoidea) in Europe and its development in the intermediate host. Folia Parasit 1994, 41:203-208.
• [55]Knopf K, Würtz J, Sures B, Taraschewski H: Impact of low water temperature on the development of Anguillicola crassus in the final host Anguilla anguilla. Dis Aquat Org 1998, 33:143-149.