Abstract
BackgroundThe systematics of echinostomes within the so-called 'revolutum' group of the genus Echinostoma, which encompasses the type-species E. revolutum and a number of morphologically similar species, has long been controversial. Recent molecular studies indicate the existence of more species than previously considered valid, thus stressing the need for wider taxon sampling from natural host populations. This is especially true for Europe where morphological evidence indicates higher species diversity than previously thought, but where molecular data are virtually lacking. This gap in our knowledge was addressed in the present study through an integration of morphological and molecular approaches in the investigation of a dataset with larger taxonomic and geographical coverage.MethodsMore than 20,000 freshwater snails belonging to 16 species were collected during 1998–2012 from various localities in eight countries in Europe. Snail screening provided representative larval isolates for five species of the 'revolutum' group, identified by their morphology. Adult isolates for four species recovered from natural and experimental infections were also identified. Partial fragments of the mitochondrial nad1 and 28S rRNA genes were amplified for 74 and 16 isolates, respectively; these were analysed together with the sequences of Echinostoma spp. available on GenBank.ResultsDelineation of the European Echinostoma spp. was carried out based on molecular, morphological and ecological data. The large-scale screening revealed infections with five Echinostoma spp., including one new species: E. revolutum (sensu stricto), E. miyagawai, E. paraulum, E. bolschewense and Echinostoma n. sp. The newly-generated nad1 sequences from Europe fall into six distinct, well-supported, reciprocally monophyletic lineages corresponding to the species identifications based on morphology; this was corroborated by the 28S rDNA sequences. The analyses of the total nad1 dataset provided evidence for 12 monophyletic groups and five singletons, which represent seven described/named species and ten cryptic species-level lineages of Echinostoma.ConclusionWe conclude that nad1 should be the first choice for large-scale barcode-based identification of the species of the 'revolutum' group. Our study provides a comprehensive reference library for precisely identified isolates of the European species and highlights the importance of an integrative approach for species identification linking molecular, morphological and biological data.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-014-0520-8) contains supplementary material, which is available to authorized users.
Highlights
The systematics of echinostomes within the so-called 'revolutum' group of the genus Echinostoma, which encompasses the type-species E. revolutum and a number of morphologically similar species, has long been controversial
IG), eight snail species are found to be infected with Echinostoma spp. in Europe, namely the lymnaeids Lymnaea stagnalis, Radix auricularia, R. peregra and Stagnicola palustris; the planorbids Planorbis planorbis, Anisus vortex and Planorbarius corneus; and the viviparid Viviparus acerosus
Five species acted as hosts of a single species of Echinostoma: A. vortex (E. miyagawai), S. palustris (E. revolutum), P. planorbis (E. miyagawai), P. corneus (Echinostoma n. sp.) and V. acerosus (E. bolschewense) and three lymnaeids hosted two Echinostoma spp. each: L. stagnalis (E. revolutum and E. paraulum), R. auricularia and R. peregra
Summary
The systematics of echinostomes within the so-called 'revolutum' group of the genus Echinostoma, which encompasses the type-species E. revolutum and a number of morphologically similar species, has long been controversial. Kanev and colleagues [5,6,7] enlarged the ‘revolutum’ group to five species, i.e. E_revolutum (syns E. audyi Lie & Umathevy, 1965, E. ivaniosi Mohandas, 1973, E. paraulum Dietz, 1909 and E. revolutum of Kosupko [8,9,10,11]), E. trivolvis (Cort, 1914) (syns E. revolutum of Beaver [4] and E. rodriguesi Hsu, Lie & Basch, 1968), E. caproni Richard, 1964 (syns E. liei Jeyarasasingam et al, 1972, E. togoensis Jourdan & Kulo, 1981 and E. paraensei Lie & Basch, 1967), E. jurini (Skvortsov, 1924) (syns E. sisjakowi Skvortzov, 1934, E. orlovi Romashov, 1966 and E. bolschewense (Kotova, 1939)) and E. echinatum (Zeder, 1803) (syns Cercaria spinifera La Valette, 1855, E. lindoense Sandground & Bonne, 1940, E. barbosai Lie & Basch, 1966, E. miyagawai of Kosupko [8,9,10,11] and E. revolutum of Našincová [12]) These authors distinguished the five species based mainly on a single morphological feature of their larval stages (the number of outlets of the paraoesophageal gland-cells in the cercaria), the specificity towards the snail first intermediate host (at the familial level), their ability to infect avian or mammalian hosts (or both) and their geographical range on a global scale (continents) (see Kostadinova et al [1] and Kostadinova & Gibson [3] for detailed comments). The re-examination of the voucher specimens from Kanev’s experimental studies used in his delimitation of E. revolutum and E. echinatum revealed a number of erroneous identifications including members of the genera Hypoderaeum Dietz, 1909 and Echinoparyphium Dietz, 1909, and a species of Echinostoma with 47 collar spines [1,13]
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