A molecular phylogeny of Asian species of the genus Metagonimus (Digenea)—small intestinal flukes—based on representative Japanese populations

Abstract

Metagonimus Katsurada, 1912 is a genus of small intestinal parasites. The genus comprises eight species, primarily from far-eastern Asia, with two exceptions reported from Europe. Metagonimus yokogawai, the most widespread species, is the main agent responsible for the intestinal disease, metagonimiasis, in Japan and some other East Asian countries. On the basis of the ratio of the size of the ventral and oral suckers, Metagonimus has traditionally been morphologically divided into two groups; however, the genus has not been extensively studied using molecular data. To reveal phylogenetic relationships within Metagonimus based on molecular data, we analyzed six of the seven species present in Asia using samples collected in central Japan. Maximum likelihood and Bayesian analyses of a combined 28S ribosomal DNA (rDNA), internal transcribed spacer 2 (ITS2), and mitochondrial cox1 gene sequence dataset separated the six species into two well-supported clades. One clade comprised M. yokogawai, M. takahashii, M. miyatai, and M. hakubaensis, whereas the other consisted of M. otsurui and M. katsuradai. Genetic distances calculated from 28S rDNA and ITS2 nucleotide sequences and a comparison of the predicted amino acid sequences of cox1 gene suggested that M. otsurui and M. katsuradai may have diverged recently. None of the four main morphological characters used to delimit species of Metagonimus (i.e., sucker ratio, positions of the uterus and testes, and distribution of vitelline follicles) was consistent with the distribution of species in the molecular tree.

Life cycle, morphology of developmental stages ofMetorchis ussuriensissp. nov. (Trematoda: Opisthorchiidae), and phylogenetic relationships with other opisthorchiids

“…These values indicate that the representatives of Metorchis , Opisthorchis , and Clonorchis may belong to one genus, despite some differences in morphology (Bray, Gibson, & Jones, ). This assumption is consistent with data based on ITS2 sequences, because the values of genetic distances between different genera based on this marker are also equal to the distances within Metagonimus (Pornruseetairatn et al., ; Shumenko et al., ). It should be noted that the description of morphological features is not always sufficient to identify species of trematodes.…”

“…The genetic distances between M. ussuriensis sp. nov. and other representatives of the family Opisthorchiidae ( Opisthorchis , Clonorchis ) are similar to the distances between species of the genus Metagonimus (family Heterophyidae) (Pornruseetairatn et al., ; Shumenko et al., ), while the genetic distances between other genera of each family mentioned above are 3–11 times higher. These values indicate that the representatives of Metorchis , Opisthorchis , and Clonorchis may belong to one genus, despite some differences in morphology (Bray, Gibson, & Jones, ).…”

“…Low distances between a representative of another genus ( P. truncatum ) and M. xanthosomus and large differences in morphology demonstrate that this genetic marker is unsuitable for species identification and for phylogenetic reconstructions among the genus Metorchis and the family Opisthorchiidae in general. In addition, the ITS2 region does not separate representatives of other families of trematodes (Després, Kruger, Imbert‐Establet, & Adamson, ; Pornruseetairatn et al., ). Similar to ITS2 sequences, the distances between the ITS1 sequences of M. ussuriensi s, M. bilis, and M. xanthosomus are in the range of genetic distances within species of the family Opisthorchiidae, while distances between these species and M. orientalis were 3–7.5 times higher, but did not reach the values between the genera of the family (Kang et al., ; Tatonova et al., ).…”

“…The 28S gene is more suited to the genetics of trematodes including Opisthorchioidea (Olson, Cribb, Tkach, Bray, & Littlewood, 2003;Shumenko, Tatonova, & Besprozvannykh, 2017 (Pornruseetairatn et al, 2016;Shumenko et al, 2017), while the genetic distances between other genera of each family mentioned above are 3-11 times higher.…”

The ribosomal transcription units of Haplorchis pumilio and H. taichui and the use of 28S rDNA sequences for phylogenetic identification of common heterophyids in Vietnam

“…Sequences from various portions of the rTU (18S, ITS1, ITS2 and 28S) have been widely used for inference of phylogenetic relationships and taxonomic clarification within and between many trematode families (e.g. [15, 18, 22, 25–31]). Sequences of complete or near-complete rTUs are only available for a few species of trematode [12, 16, 20, 32, 33].…”