Phylogenetic systematics of the genus Echinococcus (Cestoda: Taeniidae)

Echinococcosis is a serious helminthic zoonosis in humans, livestock and wildlife. The pathogenic organisms are members of the genus Echinococcus (Cestoda: Taeniidae). Life cycles of Echinococcus spp. are consistently dependent on predator–prey association between two obligate mammalian hosts. Carnivores (canids and felids) serve as definitive hosts for adult tapeworms and their herbivore prey (ungulates, rodents and lagomorphs) as intermediate hosts for metacestode larvae. Humans are involved as an accidental host for metacestode infections. The metacestodes develop in various internal organs, particularly in liver and lungs. Each metacestode of Echinococcus spp. has an organotropism and a characteristic form known as an unilocular (cystic), alveolar or polycystic hydatid. Recent molecular phylogenetic studies have demonstrated that the type species, Echinococcus granulosus, causing cystic echinococcosis is a cryptic species complex. Therefore, the orthodox taxonomy of Echinococcus established from morphological criteria has been revised from the standpoint of phylogenetic systematics. Nine valid species including newly resurrected taxa are recognised as a result of the revision. This review summarises the recent advances in the phylogenetic systematics of Echinococcus, together with the historical backgrounds and molecular epidemiological aspects of each species. A new phylogenetic tree inferred from the mitochondrial genomes of all valid Echinococcus spp. is also presented. The taxonomic nomenclature for Echinococcus oligarthrus is shown to be incorrect and this name should be replaced with Echinococcus oligarthra.     

Echinococcus granulosus (Cestoda: Taeniidae) infections in moose (Alces alces) from southwestern Quebec

Investigation of the distribution of larval Echinococcus granulosus in a moose population from southwestern Quebec revealed a distinct and stable pattern of infection with a prevalence of 44% (n = 580). Positive correlations between moose age and the intensity, mean cyst weight and biomass of the hydatid cysts suggested a process of continued parasite acquisition and cyst growth. The distribution of cyst sizes within individual moose provided circumstantial evidence of interaction between cysts, perhaps mediated through the host's immunological response.     

Phylogenetic relationships within Echinococcus and Taenia tapeworms (Cestoda: Taeniidae): an inference from nuclear protein-coding genes

The family Taeniidae of tapeworms is composed of two genera, Echinococcus and Taenia, which obligately parasitize mammals including humans. Inferring phylogeny via molecular markers is the only way to trace back their evolutionary histories. However, molecular dating approaches are lacking so far. Here we established new markers from nuclear protein-coding genes for RNA polymerase II second largest subunit (rpb2), phosphoenolpyruvate carboxykinase (pepck) and DNA polymerase delta (pold). Bayesian inference and maximum likelihood analyses of the concatenated gene sequences allowed us to reconstruct phylogenetic trees for taeniid parasites. The tree topologies clearly demonstrated that Taenia is paraphyletic and that the clade of Echinococcus oligarthrus and Echinococcusvogeli is sister to all other members of Echinococcus. Both species are endemic in Central and South America, and their definitive hosts originated from carnivores that immigrated from North America after the formation of the Panamanian land bridge about 3 million years ago (Ma). A time-calibrated phylogeny was estimated by a Bayesian relaxed-clock method based on the assumption that the most recent common ancestor of E. oligarthrus and E. vogeli existed during the late Pliocene (3.0 Ma). The results suggest that a clade of Taenia including human-pathogenic species diversified primarily in the late Miocene (11.2 Ma), whereas Echinococcus started to diversify later, in the end of the Miocene (5.8 Ma). Close genetic relationships among the members of Echinococcus imply that the genus is a young group in which speciation and global radiation occurred rapidly.     

Genetic characterization and phylogenetic position of Echinococcus felidis (Cestoda: Taeniidae) from the African lion

Echinococcus felidis had been described in 1937 from African lions, but was later included in Echinococcus granulosus as a subspecies or a strain. In the absence of any genetic characterization, most previous records of this taxon from a variety of large African mammals remained unconfirmed due to the lack of diagnostic criteria and the possible confusion with the sympatric E. granulosus sensu stricto, Echinococcus ortleppi and Echinococcus canadensis. In this study, we obtained taeniid eggs from lion feces in Uganda and amplified DNA from individual eggs. Mitochondrial and nuclear DNA sequences showed similarities with those of other Echinococcus spp., but high values of percentage divergence of mitochondrial genes indicated the presence of a distinct species. In a second step, we compared this material with the preserved specimens of adult E. granulosus felidis, which had been identified morphologically approximately 40 years ago in South Africa. All DNA fragments (<200 bp) that could be amplified from the adults showed 100% similarity with the Ugandan material. In the phylogenetic tree of Echinococcus which was constructed from the mitochondrial genes, E. felidis is positioned as a sister taxon of E. granulosus sensu stricto. The data obtained will facilitate the development of diagnostic tools necessary to study the epidemiology of this enigmatic parasite.     

Mitochondrial and nuclear sequence polymorphisms reveal geographic structuring in Amazonian populations of Echinococcus vogeli (Cestoda: Taeniidae)

To date, nothing is known about the genetic diversity of the Echinococcus neotropical species, Echinococcus vogeli and Echinococcus oligarthrus. Here we used mitochondrial and nuclear DNA sequence polymorphisms to uncover the genetic structure, transmission and history of E. vogeli in the Brazilian Amazon, based on a sample of 38 isolates obtained from human and wild animal hosts. We confirm that the parasite is partially synanthropic and show that its populations are diverse. Furthermore, significant geographical structuring is found, with western and eastern populations being genetically divergent.     

Cysticerci (Cestoda: Taeniidae) from white-tailed deer, Odocoileus virginianus, in southern Florida

Metacestodes (cysticerci) of Taenia omissa Lühe, 1910, and Taenia hydatigena Pallas, 1776, were found in 9 and 1 of 124 white-tailed deer, respectively, in southern Florida in 1984-1986. Intensities of T. omissa varied from 1 to 15 (mean = 4.6); only 1 cysticercus of T. hydatigena was collected. No significant difference in the prevalences of T. omissa according to sex, age, or locality was observed.     

Intestinal parasites of Agouti paca (Rodentia: Dasyproctidae) in Costa Rica

In a sample of 23 breeding places of pacas (Agouti paca) in Costa Rica, the following parasites were found: Eimeria agoutii, Balantidium coli, Capillaria sp., Trichuris sp., Taenia sp., Strongyloides sp., and members of the superfamilies Strongyloidea and Ascaroidea.     

Echinococcus vogeli Rausch and Bernstein, 1972, from the paca, Cuniculus paca L. (Rodentia: Dasyproctidae), in the Departamento de Santa Cruz, Bolivia

Among approximately 2,000 mammals examined for helminths in various regions of Bolivia during 1983-1987, cysts of Echinococcus vogeli Rausch and Bernstein, 1972, were found in a single paca, Cuniculus paca L., collected at La Laguna, Departamento de Santa Cruz (lat. 16 degrees 36'W; long. 62 degrees 42'S). This record, the first from Bolivia, represents a considerable extension of the known geographic range of this species in South America. Upon analysis of the morphologic characteristics of the protoscoleces derived from the cysts, the sizes of rostellar hooks from the material from the paca were found to be well within the ranges reported in previous studies. Statistical analysis of frequency distributions of hook characteristics revealed some deviations from normality. These results indicate that parametric statistics should be applied with caution in analyses of inter-and intraspecific variation of morphologic characteristics of hooks of metacestodes of the genus Echinococcus.     

The karyotype of Sphiggurus villosus (Rodentia: Erethizontidae) from Brazil

Karyotypic analysis was performed in two male specimens of Sphiggurus villosus collected in the Atlantic Forest of Rio de Janeiro State, Brazil. The observed 2n = 42 / FN = 76 karyotype was similar to those of other Erethizontidae such as Erethizon dorsatum and Sphiggurus vestitus and to hystricomorph rodents like Myocastor coypus. Current karyotypic data showed that two species of the genus Coendou share the same diploid and fundamental numbers (2n = 74 / FN = 82) but 3 Sphiggurus species differ in diploid number while sharing the same fundamental number.     

Subcutaneous cysticercosis due to Taenia crassiceps (Cestoda: Taeniidae) in an imported steppe lemming in Japan

This study describes a subcutaneous proliferative cysticercosis in a pet steppe lemming, Lagurus lagurus (Rodentia: Cricetidae), bred and imported from Czech Republic into Japan. Numerous metacestodes were collected from the subcutaneous cystic lesion of the left medial thigh. Four surgical removals were coupled with anthelmintic treatment but ended with recurrence. Based on morphological features and mitochondrial DNA sequences, the metacestodes were identified as the larval stage of Taenia crassiceps (Zeder, 1800). This is the first case of infection with larval T. crassiceps in rodents of the genus Lagurus, and becomes the third case of the parasite detected from imported animals in Japan. Related public health concerns are discussed.     

The complete mitochondrial DNA sequence of the cestode Echinococcus multilocularis (Cyclophyllidea: Taeniidae)

The 13,738 bp mitochondrial DNA from the cestode Echinococcus multilocularis has been sequenced. It contains two major noncoding regions and 36 genes (12 for proteins involved in oxidative phosphorylation, two for rRNAs and 22 for tRNAs) but a gene for ATPase subunit 8 is missing. All genes are transcribed in the same direction. Putative secondary structures of tRNAs indicate that most of them are conventional clover leaves but the dihydrouridine arm is unpaired in tRNA(Ser(AGN)), tRNA(Ser(UCN)), tRNA(Arg) and tRNA(Cys). The base composition at the wobble positions of fourfold degenerate codon families is highly biased toward U and against C.     

Genetic studies in representatives of genusRhipidomys (Rodentia, Sigmodontinae) from Brazil

Karyotypic polymorphism of five taxa of the rodent genusRhipidomys from the Brazilian Amazon and Cerrado biomes was analysed.Rhipidomys nitela Thomas, 1901 from Amazon has 2n=48, FN=68. The other species, all have 2n=44, but can be separated into two groups, one with high FNs (76, 80) and the other with low FNs (48, 52). Two cytotypes ofR. mastacalis (Lund, 1840) with high FNs were trapped in four localities of the Cerrado, showing 19 and 17 biarmed autosomes, respectively. A low FN (48) was observed inR. leucodactylus (Tschudi, 1844) in two localities of the Cerrado and FN=52 in one locality in the Cerrado and the Amazon. All taxa with 2n=44 have a medium-sized acrocentric X chromosome and a small Y.Rhipidomys nitela is different from the species with 2n=44 by presenting a heterochromatic short arm of the X chromosome. In all karyotypes analysed, the nucleolus organizer regions were located in the short arms of two to six pairs and the (T₂AG₃)_n telomeric probes hybridizedin situ in both the short and long arms of all pairs of the karyotypes.     

First report of Taenia arctos (Cestoda: Taeniidae) from grizzly (Ursus arctos horribilis) and black bears (Ursus americanus) in North America

The cestode Taenia arctos was found at necropsy in the small intestine of a grizzly (Ursus arctos horribilis) and a black bear (Ursus americanus) from Kananaskis Country in southwestern Alberta, Canada. The autolysis of the tapeworm specimens precluded detailed morphological characterization of the parasites but molecular analysis based on mitochondrial DNA cytochrome c oxidase subunit 1 gene confirmed their identity as T. arctos. This is the first report of T. arctos from definitive hosts in North America. Its detection in Canadian grizzly and black bears further supports the Holarctic distribution of this tapeworm species and its specificity for ursids as final hosts. Previously, T. arctos was unambiguously described at its adult stage in brown bears (Ursus arctos arctos) from Finland, and as larval stages in Eurasian elk (Alces alces) from Finland and moose (Alces americanus) from Alaska, USA. Given the morphological similarity between T. arctos and other Taenia species, the present study underlines the potential for misidentification of tapeworm taxa in previous parasitological reports from bears and moose across North America. The biogeographical history of both definitive and intermediate hosts in the Holarctic suggests an ancient interaction between U. arctos, Alces spp., and T. arctos, and a relatively recent host-switching event in U. americanus.     

A new karyotype of Oligoryzomys (Sigmodontinae, Rodentia) from central Brazil

A new karyotype of the genus Oligoryzomys was described for specimens collected in Brazilian Cerrado in Tocantins and Goiás States. Conventional staining, G-, C-banding, and Ag-NOR staining techniques were used for describe this karyotype with 2n=70, AN=74 or 76. The chromosome complement, with the highest diploid number known among Oligoryzomys species, differs from all others previously reported. This small sized Oligoryzomys species can be differentiated from other Brazilian Oligoryzomys not only by chromosomal complement, but also in some morphological attributes. The new species is apparently restricted in distribution and endemic of Brazilian Cerrado, occurring only in Rio Tocantins basin.