Massive encapsulation of larval Anguillicoloides crassus in the intestinal wall of Japanese eels

<p>Abstract</p> <p>Background</p> <p>Within the last 25 years, after the introduction of the swimbladder nematode <it>Anguillicoloides </it>crassus from East-Asia to Europe, a body of work has aggregated on the host parasite interactions in the acquired host <it>Anguilla anguilla</it>. Despite the emerging evolutionary interest there is still a lack of knowledge about host parasite relations of <it>A. crassus </it>in its natural host <it>Anguilla japonica</it>. We examined the <it>Anguillicoloides </it>infections of wild-caught Japanese eels as well as from aquacultured specimens in Taiwan with respect to the fate of migratory L3 larvae and performed infection experiments with Japanese eels.</p> <p>Results</p> <p>Inside the intestinal wall of cultured eels, where the infective pressure was higher than among wild eels, we found large numbers of granuloma-like cysts. In a few eels these cysts contained nematodes still recognizable as L3 larvae of <it>A. crassus</it>, while in most cases the content of these capsules was degraded to amorphous matter. Occurrence of these objects was correlated with the number of encapsulated larvae in the swimbladder wall. We were able to show, that the cysts contained disintegrated L3 larvae by amplification and subsequent sequencing of large subunit ribosomal rRNA. Furthermore we identified repeated infections with high doses of larvae as prerequisites for the processes of encapsulation in infection experiments.</p> <p>Conclusion</p> <p>Under high infective pressure a large percentage of L3 larvae of <it>A. crassus </it>coming from the gut lumen are eliminated by the natural host within its intestinal tissue. It is possible to reproduce this condition in infection experiments. We provide a fast, easy and reliable PCR-based method for identification of encapsulated swimbladder parasites.</p

The phylogenetics of Anguillicolidae (Nematoda: Anguillicolidea), swimbladder parasites of eels

BACKGROUND: Anguillicolidae Yamaguti, 1935 is a family of parasitic nematode infecting fresh-water eels of the genus Anguilla, comprising five species in the genera Anguillicola and Anguillicoloides. Anguillicoloides crassus is of particular importance, as it has recently spread from its endemic range in the Eastern Pacific to Europe and North America, where it poses a significant threat to new, naïve hosts such as the economic important eel species Anguilla anguilla and Anguilla rostrata. The Anguillicolidae are therefore all potentially invasive taxa, but the relationships of the described species remain unclear. Anguillicolidae is part of Spirurina, a diverse clade made up of only animal parasites, but placement of the family within Spirurina is based on limited data. RESULTS: We generated an extensive DNA sequence dataset from three loci (the 5' one-third of the nuclear small subunit ribosomal RNA, the D2-D3 region of the nuclear large subunit ribosomal RNA and the 5' half of the mitochondrial cytochrome c oxidase I gene) for the five species of Anguillicolidae and used this to investigate specific and generic boundaries within the family, and the relationship of Anguillicolidae to other spirurine nematodes. Neither nuclear nor mitochondrial sequences supported monophyly of Anguillicoloides. Genetic diversity within the African species Anguillicoloides papernai was suggestive of cryptic taxa, as was the finding of distinct lineages of Anguillicoloides novaezelandiae in New Zealand and Tasmania. Phylogenetic analysis of the Spirurina grouped the Anguillicolidae together with members of the Gnathostomatidae and Seuratidae. CONCLUSIONS: The Anguillicolidae is part of a complex radiation of parasitic nematodes of vertebrates with wide host diversity (chondrichthyes, teleosts, squamates and mammals), most closely related to other marine vertebrate parasites that also have complex life cycles. Molecular analyses do not support the recent division of Anguillicolidae into two genera. The described species may hide cryptic taxa, identified here by DNA taxonomy, and this DNA barcoding approach may assist in tracking species invasions. The propensity for host switching, and thus the potential for invasive behaviour, is found in A. crassus, A. novaezelandiae and A. papernai, and thus may be common to the group

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

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

Data from: The phylogenetics of Anguillicolidae (Nematoda: Anguillicolidea), swimbladder parasites of eels

BACKGROUND: Anguillicolidae Yamaguti, 1935 is a family of nematode parasites infecting fresh-water eels of the genus Anguilla, with five species in the genera Anguillicola and Anguillicoloides. Anguillicolidae is part of Spirurina, a diverse clade made up of only animal parasites. Anguillicoloides crassus is of particular importance, as it has recently spread from its endemic range in the Eastern Pacific to Europe and North America, where it poses a significant threat to new, naïve hosts such as the economic important eel species Anguilla anguilla and Anguilla rostrata. The Anguillicolidae are therefore all potentially invasive taxa, but the relationships of the described species remain unclear. RESULTS: We generated an extensive DNA sequence dataset from three loci (the 5' one-third of the nuclear small subunit ribosomal RNA, the D2-D3 region of the nuclear large subunit ribosomal RNA and the 5' half of the mitochondrial cytochrome c oxidase I gene) for the five species of Anguillicolidae and used this to investigate species and generic boundaries within the family, and the relationship of Anguillicolidae to other spirurine nematodes. Neither nuclear nor mitochondrial sequences supported monophyly of the genera Anguillicola and Anguillicoloides. Genetic diversity within the African species Anguillicoloides papernai was suggestive of cryptic taxa, as was the finding of divergent lineages of Anguillicoloides novaezelandiae in New Zealand and Tasmania. Phylogenetic analysis of the Spirurina grouped the Anguillicolidae together with members of the Gnathostomatidae and Seuratidae. CONCLUSIONS: The Anguillicolidae is part of a complex radiation of vertebrate parasitic nematodes with wide host diversity (cartilaginous and bony fish, reptiles and mammals), most closely related to other parasites of marine vertebrates that also have complex lifecycles. Molecular analyses do not support the recent division of Anguillicolidae into two genera. The described species may hide cryptic taxa, identified here by DNA taxonomy, and this DNA barcoding approach may assist in tracking species invasions. The propensity for host switching, and thus the potential for invasive behaviour, is found in A. crassus, A. novaezelandiae and A. papernai, and thus may be common to the group

Phylogeny of the Anguillicolidae Supplementary Data

Sequence data files and keys thereto as a single compressed file, expandable to a folder containing: Cytochrome oxidase 1 data, COX1.haplotypes.nex, NEXUS format file of aligned COXI haplotype sequences, COX1.haplotypes.labels.txt, text file describing the assignment of individual COXI sequences to hapolotypes, COX1.haplotypes.crassus.nex, NEXUS format file of aligned A. crassus COXI haplotype sequences, COX1.haplotypes.crassus.labels.txt, text file describing the assignment of individual A. crassus COXI sequences to hapolotypes, COX1.nex, NEXUS format file of all aligned COXI haplotype sequences, Nuclear large subunit ribosomal RNA data, 28_S.haplotypes.nexNEXUS format file of aligned nLSU or 28S haplotype sequences, 28_S.nex, NEXUS format file of all aligned nLSU or 28S haplotype sequences, Nuclear small subunit ribosomal RNA data, 18_S.haplotypes.nex, NEXUS format file of aligned nSSU or 18S haplotype sequences, 18_S.spirurina_B.nex, NEXUS format file of aligned nSSU or 18S haplotype sequences, 18_S.nex, NEXUS format file of all aligned nSSU or 18S haplotype sequence