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Journal ArticleDOI

Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from northern Pacific marine mammals.

01 Dec 2005-Journal of Parasitology (American Society of Parasitologists)-Vol. 91, Iss: 6, pp 1413-1429
TL;DR: Phylogenetic analysis of LSU sequences revealed strong support for the monophyly of Anisakinae, Contracaecum plus Phocascaris, Pseudoterranova, and Anisakis, which is primarily consistent with previously published phenograms based on multilocus electrophoretic data.
Abstract: Individual specimens of Anisakis, Pseudoterranova, and Contracaecum collected from marine mammals inhabiting northern Pacific waters were used for comparative diagnostic and molecular phylogenetic analyses. Forty-eight new sequences were obtained for this study of 14 Anisakis taxa, 8 Pseudoterranova taxa, 4 Contracaecum taxa, and 4 outgroup species. Partial 28S (LSU) and complete internal transcribed spacer (ITS-1, 5.8S, ITS-2) ribosomal DNA was amplified by the polymerase chain reaction and sequenced. Sequences of ITS indicated that Pseudoterranova specimens from Zalophus californianus (California sea lion), Mirounga angustirostris (northern elephant seal), Phoca vitulina (harbor seal), Enhydra lutris (sea otter), and Eumetopias jubatus (Steller's sea lion) exactly matched P. decipiens s. str., extending the host and geographic range of this species. Anisakis from northern Pacific marine mammals were most closely related to members of the A. simplex species complex. Comparison of Anisakis ITS sequences diagnosed the presence of A. simplex C in 2 M. angustirostris hosts, which is a new host record. Anisakis specimens from Phocoena phocoena (harbor porpoise), Lissodelphis borealis (Pacific rightwhale porpoise), and E. jubatus included 3 ITS sequences that did not match any known species. Contracaecum adults obtained from Z. californianus were most closely related to C. ogmorhini s.l. and C. rudolphii, but ITS sequences of these Contracaecum specimens did not match C. ogmorhini s. str. or C. margolisi. These novel Anisakis and Contracaecum ITS sequences may represent previously uncharacterized species. Phylogenetic analysis of LSU sequences revealed strong support for the monophyly of Anisakinae, Contracaecum plus Phocascaris, Pseudoterranova, and Anisakis. Phylogenetic trees inferred from ITS sequences yielded robustly supported relationships for Pseudoterranova and Anisakis species that are primarily consistent with previously published phenograms based on multilocus electrophoretic data.

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Citations
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Book ChapterDOI
TL;DR: Examples in which anisakid nematodes recognized genetically at the species level in definitive and intermediate/paratenic hosts from various geographical areas of the Boreal and Austral regions and their infection levels have been used as biological indicators of fish stocks and food-web integrity in areas at high versus low levels of habitat disturbance are presented.
Abstract: The application of molecular systematics to the anisakid nematodes of the genera Anisakis, Pseudoterranova and Contracaecum, parasites of aquatic organisms, over the last two decades, has advanced the understanding of their systematics, taxonomy, ecology and phylogeny substantially Here the results of this effort on this group of species from the early genetic works to the current status of their revised taxonomy, ecology and evolutionary aspects are reviewed for each of three parasitic groups It has been shown that many anisakid morphospecies of Anisakis, Contracaecum and Pseudoterranova include a certain number of sibling species Molecular genetic markers provided a rapid, precise means to screen and identify several species that serve as definitive and intermediate and or/paratenic hosts of the so far genetically characterized species Patterns of differential distribution of anisakid nematodes in various definitive and intermediate hosts are presented Differences in the life history of related species can be due both to differential host-parasite co-adaptation and co-evolution, and/or to interspecific competition, that can reduce the range of potential hosts in sympatric conditions Phylogenetic hypotheses attempted for anisakid nematodes and the possible evolutionary scenarios that have been proposed inferred from molecular data, also with respect to the phylogeny of their hosts are presented for the parasite-host associations Anisakis-cetaceans and Contracaecum-pinnipeds, showing that codivergence and host-switching events could have accompanied the evolution of these groups of parasites Finally, examples in which anisakid nematodes recognized genetically at the species level in definitive and intermediate/paratenic hosts from various geographical areas of the Boreal and Austral regions and their infection levels have been used as biological indicators of fish stocks and food-web integrity in areas at high versus low levels of habitat disturbance (pollution, overfishing, by-catch) are presented

402 citations


Cites background or methods or result from "Molecular phylogenetics and diagnos..."

  • ...pegreffii is also well supported by a phylogenetic analysis inferred from ITS rDNA sequence data sets (Nadler et al., 2005)....

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  • ...Codes: AN: Antarctica; BE: Bering Sea; BS: Barents Sea; FI: Faeroe Islands; JA: Japan Sea; LS: Labrador Sea; NEA: North-East Atlantic; NEP: North-East Pacific; NWA: NorthWest Atlantic; NWP: North-West Pacific; SEP: South-East Pacific (Chilean coast) (data from George-Nascimento and Llanos, 1995; George-Nascimento and Urrutia, 2000; Mattiucci et al., 1998; Nadler et al., 2005; Paggi et al., 1991, 1998c; Zhu et al., 2002)....

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  • ...) is widespread between 35 N and the Arctic Circle; it is present in both the western and eastern Atlantic and Pacific Oceans (Abe et al., 2005, 2006; Abollo et al., 2001; Mattiucci et al., 1997, 1998; Nadler et al., 2005; Paggi et al., 1998a; Umehara et al., 2006, 2008) (Fig....

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  • ...Parsimony and ML analyses indicated that the Raphidascarididae, Contracaecum plus Phocascaris, and the Anisakinae (here considering only Pseudoterranova and Anisakis) are each monophyletic, the latter two groups with consistently strong bootstrap support at MP and ML analyses (Nadler et al., 2005)....

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  • ...A congruent result was inferred from the ITS rDNA sequence analysis (Nadler et al., 2005) (see Section 4....

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Journal ArticleDOI
TL;DR: The morphological and morphometric analyses revealed the presence of morphological features that differed among the 3 biological species, and the tree topologies support the finding that A. simplex (s.s.), A. pegreffii, and A. berlandi n.
Abstract: Numerous specimens of the 3 sibling species of the Anisakis simplex species complex (A. pegreffii, A. simplex (senso stricto)), and A. simplex sp. C) recovered from cetacean species stranded within the known geographical ranges of these nematodes were studied morphologically and genetically. The genetic characterization was performed on diagnostic allozymes and sequences analysis of nuclear (internal transcribed spacer [ITS] of ribosomal [r]DNA) and mitochondrial (mitochondrial [mt]DNA cox2 and rrnS) genes. These markers showed (1) the occurrence of sympatry of the 2 sibling species A. pegreffii and A. simplex sp. C in the same individual host, the pilot whale, Globicephala melas Traill, from New Zealand waters; (2) the identification of specimens of A. pegreffii in the striped dolphin, Stenella coeruleoalba (Meyen), from the Mediterranean Sea; and (3) the presence of A. simplex (s.s.) in the pilot whale and the minke whale, Balaenoptera acutorostrata Lacepede, from the northeastern Atlantic wa...

166 citations


Cites background from "Molecular phylogenetics and diagnos..."

  • ...…have confirmed the existence of these 3 cryptic species by using phylogenetic analyses of DNA sequences of mitochondrial (mitochondrial [mt]DNA cox2) and nuclear (internal transcribed spacer [ITS] of ribosomal [r]DNA) genes (Nadler et al., 2005; Mattiucci et al., 2009; Cavallero et al., 2011)....

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Book ChapterDOI
TL;DR: This review addresses the biodiversity, biology, distribution, ecology, epidemiology, and consumer health significance of the so far known species of Anisakis, both in their natural hosts and in human accidental host populations, worldwide.
Abstract: This review addresses the biodiversity, biology, distribution, ecology, epidemiology, and consumer health significance of the so far known species of Anisakis, both in their natural hosts and in human accidental host populations, worldwide. These key aspects of the Anisakis species' biology are highlighted, since we consider them as main driving forces behind which most of the research in this field has been carried out over the past decade. From a public health perspective, the human disease caused by Anisakis species (anisakiasis) appears to be considerably underreported and underestimated in many countries or regions around the globe. Indeed, when considering the importance of marine fish species as part of the everyday diet in many coastal communities around the globe, there still exist significant knowledge gaps as to local epidemiological and ecological drivers of the transmission of Anisakis spp. to humans. We further identify some key knowledge gaps related to Anisakis species epidemiology in both natural and accidental hosts, to be filled in light of new 'omic' technologies yet to be fully developed. Moreover, we suggest that future Anisakis research takes a 'holistic' approach by integrating genetic, ecological, immunobiological, and environmental factors, thus allowing proper assessment of the epidemiology of Anisakis spp. in their natural hosts, in human populations, and in the marine ecosystem, in both space and time.

158 citations

Journal ArticleDOI
TL;DR: It is suggested that anisakiasis in Japan is mainly caused by A. simplex sensu stricto because it penetrates the muscle of the fish at a higher rate than A. pegreffii.

142 citations

Journal ArticleDOI
TL;DR: This is the first instance of human intestinal anisakiasis diagnosed using PCR of DNA purified from a fixed eosinophilic granuloma embedded in paraffin, reinforcing the pathological significance of the species A. pegreffii to humans.
Abstract: Anisakiasis is an important fish-borne zoonosis provoked by larval stages of nematodes belonging to the genus Anisakis. The detection and identification of human infections is difficult. This is due to: a) the low specificity of the clinical features and symptomatology related to human infections; b) the paucity of diagnostic features of larvae found in granulomatous lesions characteristic of "invasive anisakiasis"; and c) the lack morphological characters diagnostic at the specific level when larvae of Anisakis are detected. Thus, molecular-based diagnostic approaches are warranted. We have developed a PCR method that amplifies the DNA of Anisakis spp. in fixed paraffin-embedded tissues. This method was applied to a granuloma removed from a human case of intestinal anisakiasis in Italy. Specific primers of the mtDNA cox2 gene were used and sequence analysis was performed according to the procedures already established for species of Anisakis. The sequence obtained (629 bp) was compared with those of the other species of Anisakis which have so far been genetically characterized and with sequences obtained from larval stages of Anisakis collected from the Mediterranean fish Engraulis encrasicolus. This enabled the genetic identification of the larva in the human tissue as A. pegreffii. This is the first instance of human intestinal anisakiasis diagnosed using PCR of DNA purified from a fixed eosinophilic granuloma embedded in paraffin. The case of human anisakiasis presented reinforces the pathological significance of the species A. pegreffii to humans. The molecular/genetic methodological approach based on mtDNA cox2 sequence analysis, described here, can allow easy and rapid identification of Anisakis spp. in formalin-fixed and paraffin embedded tissues removed from cases of either gastric or intestinal human anisakiasis.

128 citations


Cites background from "Molecular phylogenetics and diagnos..."

  • ...The systematics of the species of Anisakis has been clarified in recent decades by the application of such molecular methodologies [1,18-34]....

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References
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Journal ArticleDOI
TL;DR: A simplex contains a potent allergen in the excretory gland, named Ani s 1, which could have important clinical relevance, as shown by the high number of positive sera in the specific IgE immunoblotting.
Abstract: Background: Ingestion of raw or undercooked fish can lead to infection of human subjects by the fish parasite Anisakis simplex , a disease known as anisakiasis or anisakidosis. Patients sensitized to this fish parasite show high levels of total and specific IgE. Cross-reactions seem to explain the fact that specific IgE antibodies are also found in a high number of normal subjects, as reported in other parasitoses. Objective: We sought to purify and characterize a major IgE-binding protein from the parasite. Methods: A protein was purified from the crude parasite extract by means of ethanol precipitation and reversed-phase HPLC. Its clinical relevance was tested on 20 parasite-positive sera by using IgE and IgG4 immunoblotting. A monospecific human serum was used to study its localization in the parasite body. Results: A 24-kd protein was purified, to which only 45% of the sera had specific IgG4, but 85% of sera had specific IgE. The protein was present only in the excretory gland, as shown by immunohistochemistry. N-terminal amino acid sequence (17 residues) showed no homology to previously described proteins. Conclusion: A simplex contains a potent allergen in the excretory gland. This major parasite allergen, named Ani s 1, could have important clinical relevance, as shown by the high number of positive sera in the specific IgE immunoblotting. (J Allergy Clin Immunol 2000;106:177-82.)

156 citations

Journal ArticleDOI
TL;DR: Empirical data from noctuoid moths supports the view that in obtaining additional sequence data to solve a refractory systematic problem, it is prudent to take them from an independent gene.
Abstract: A central question concerning data collection strategy for molecular phylogenies has been, is it better to increase the number of characters or the number of taxa sampled to improve the robustness of a phylogeny estimate? A recent simulation study concluded that increasing the number of taxa sampled is preferable to increasing the number of nucleotide characters, if taxa are chosen specifically to break up long branches. We explore this hypothesis by using empirical data from noctuoid moths, one of the largest superfamilies of insects. Separate studies of two nuclear genes, elongation factor-1 alpha (EF-1 alpha) and dopa decarboxylase (DDC), have yielded similar gene trees and high concordance with morphological groupings for 49 exemplar species. However, support levels were quite low for nodes deeper than the subfamily level. We tested the effects on phylogenetic signal of (1) increasing the taxon sampling by nearly 60%, to 77 species, and (2) combining data from the two genes in a single analysis. Surprisingly, the increased taxon sampling, although designed to break up long branches, generated greater disagreement between the two gene data sets and decreased support levels for deeper nodes. We appear to have inadvertently introduced new long branches, and breaking these up may require a yet larger taxon sample. Sampling additional characters (combining data) greatly increased the phylogenetic signal. To contrast the potential effect of combining data from independent genes with collection of the same total number of characters from a single gene, we simulated the latter by bootstrap augmentation of the single-gene data sets. Support levels for combined data were at least as high as those for the bootstrap-augmented data set for DDC and were much higher than those for the augmented EF-1 alpha data set. This supports the view that in obtaining additional sequence data to solve a refractory systematic problem, it is prudent to take them from an independent gene.

152 citations


"Molecular phylogenetics and diagnos..." refers background in this paper

  • ...Such problems may be addressed by adding taxa, or characters, or both (Graybeal, 1998; Mitchell et al., 2000); however, in the most comprehensive phylogenetic analysis of Ascaridoidea, which included data from 3 genes plus morphological characters, support for the anisakid clade remained weak…...

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Journal ArticleDOI
TL;DR: Genetic variation of 1017 specimens of codworm, Pseudoterranova decipiens, collected from fish and seals at 23 sampling locations in the North Atlantic and Norwegian and Barents Seas, was analysed on the basis of 16 enzyme loci, indicating high levels of gene flow within each of the three species.

150 citations


"Molecular phylogenetics and diagnos..." refers background in this paper

  • ...Genetic evidence has revealed 1 instance of hybridization between P. decipiens s. str. and P. krabbei (Paggi et al., 1991), and hybridization of other anisakids has been suggested based on ITS sequences (Abollo et al., 2003)....

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  • ...The third common genus of marine mammal ascaridoid, Pseudoterranova, is also a complex of at least 5 species (Paggi et al., 1991; Mattiucci et al., 1998; George-Nascimento and Urrutia, 2000; Paggi et al., 2000; Zhu et al., 2002) that can be diagnosed by allozyme markers (Paggi et al., 2000),…...

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  • ...…differentiated sibling species with different geographic and host distributions (Mattiucci et al., 1986; Nascetti et al., 1986; Orecchia et al., 1986; Paggi et al., 1991; Nascetti et al., 1993; Mattiucci et al., 1997, 1998; Paggi, Mattiucci et al., 1998; Paggi et al., 2000; Mattiucci et al., 2003)....

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  • ...Previous systematic analyses of Pseudoterranova species have included comparisons based on allozyme genetic distances (Paggi et al., 1991; Bullini et al., 1997; Paggi et al., 2000) and a phenogram of uncorrected ITS rDNA distances (Zhu et al., 2002)....

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Journal ArticleDOI
TL;DR: The results identify some consistent putative shared-derived morphological features, but also strongly suggest that some key features emphasized by previous workers represent ancestral states or highly homoplastic characters.

150 citations


"Molecular phylogenetics and diagnos..." refers background or methods or result in this paper

  • ...The sister-group relationship of Anisakis and Pseudoterranova recovered in analysis of ribosomal DNA and mitochondrial sequences (Nadler and Hudspeth, 1998, 2000) and for regions of LSU sequence (this study) was the basis for using Anisakis to root the Pseudoterranova ITS tree, and in a separate…...

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  • ...Maximum parsimony and ML trees were rooted using Heterocheilus tunicatus (Ascaridoidea, Heterocheilidae), a choice supported by previous analyses of molecular datasets (Nadler and Hudspeth, 1998, 2000)....

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  • ...These sequences also matched the LSU sequence of P. decipiens s. str. (Nadler and Hudspeth, 1998)....

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  • ...Molecular phylogenetic studies of anisakids and other ‘‘aquatic’’ ascaridoids have been relatively limited with respect to species representation (Nadler and Hudspeth, 1998; Nadler et al., 2000; Nadler and Hudspeth, 2000)....

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  • ...Phylogenetic support for Anisakidae and Raphidascarididae has varied according to both the genes analyzed and the types of analytical methods used (Nadler and Hudspeth, 1998; Zhu, Gasser, and Chilton, 1998; Nadler and Hudspeth, 2000; Shih, 2004)....

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Journal ArticleDOI
TL;DR: By clarifying which taxonomic characters are of specific significance and by defining the intra specific limits of individual morphological variations, seventeen species of the genus Anisakis were shown to represent only three distinguishable forms, which were found to be satisfactory when discussed in geographical and ecological terms.
Abstract: By clarifying which taxonomic characters are of specific significance and by defining the intra specific limits of individual morphological variations, seventeen species of the genus Anisakis were shown to represent only three distinguishable forms, these being Anisakis simplex (Rudoiphi, 1809 det. Krabbe, 1878), A. typica (Diesing, 1860) and A. physeteris Baylis, 1923. The morphological characters in order of importance for identifying these species are the spicules, the postanal papillae, the form of the ventriculus, the position of the vulva and the form of the lips. These three species were also found to be satisfactory when discussed in geographical and ecological terms.The four remaining species in the genus, Anisakis dussumierii (van Beneden, 1870), A. alexandri Hsu and Hoeppli, 1933, A. insignis (Diesing, 1851) and A. schupakovi Mozgovoi, 1915 are retained as species inquirendae for lack of sufficient information concerning them.

149 citations


"Molecular phylogenetics and diagnos..." refers background or result in this paper

  • ...Nadler, Steven A.; D'Amelio, Stefano; Dailey, Murray D.; Paggi, Lia; Siu, Sandra; and Sakanari, Jusy A., "Molecular Phylogenetics and Diagnosis of Anisakis, Pseudoterranova, and Contracaecum from Northern Pacific Marine Mammals" (2005)....

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  • ...University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications from the Harold W. Manter Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of 2005 Molecular Phylogenetics and Diagnosis of Anisakis, Pseudoterranova, andContracaecum from Northern Pacific Marine Mammals Steven A. Nadler University of California - Davis, sanadler@ucdavis.edu Stefano D'Amelio University of Rome "La Sapienza" Murray D. Dailey Marine Mammal Center Lia Paggi University of Rome "La Sapienza" Sandra Siu University of California - Davis See next page for additional authors Follow this and additional works at: http://digitalcommons.unl.edu/parasitologyfacpubs Part of the Parasitology Commons This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln....

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  • ...Allozyme and morphological identification of Anisakis, Contracaecum and Pseudoterranova from Japanese waters (Nematoda, Ascaridoidea)....

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  • ...…1986; Orecchia et al., 1986; Paggi and Bullini, 1994; Bullini et al., 1997), have independently supported the validity of A. simplex s. str., A. typica, A. physeteris, and A. schupakovi, plus other species not recognized as valid by Davey (1971), such as A. brevispiculata (Mattiucci et al., 2001)....

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  • ...These investigations have characterized ascaridoids in Halichoerus grypus (gray seal, GS), Phoca vitulina (harbor seal, HS), Phoca hispida (ringed seal, RS), Cystophora cristata (hooded seal, HDS), Phoca groenlandica (harp seal, HRS), and Erignathus barbatus (bearded seal, BS), and have used molecular methods to identify species of Anisakis, Pseudoterranova, Contracaecum, Phocascaris, when assessing parasite abundance and host distribution....

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