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Myxosporean hyperparasites of gill monogeneans are basal to the multivalvulida.

ABSTRACT: BACKGROUND: Myxosporeans are known from aquatic annelids but parasitism of platyhelminths by myxosporeans has not been widely reported. Hyperparasitism of gill monogeneans by Myxidium giardi has been reported from the European eel and Myxidium-like hyperparasites have also been observed during studies of gill monogeneans from Malaysia and Japan.The present study aimed to collect new hyperparasite material from Malaysia for morphological and molecular descriptions. In addition, PCR screening of host fish was undertaken to determine whether they are also hosts for the myxosporean. RESULTS: Heavy myxosporean infections were observed in monogeneans from two out of 14 fish and were detected from a further five fish using specific PCRs and pooled monogenean DNA. Positive DNA isolates were sequenced and were from a single species of myxosporean. Myxospore morphology was consistent with Myxidium with histozoic development in the parenchymal tissues of the monogenean. Simultaneous infections in the fish could not be confirmed microscopically; however, identical myxosporean DNA could be amplified from kidney, spleen and intestinal tract tissues using the specific PCR. Small subunit (SSU) rDNA for the myxosporean was amplified and was found to be most similar (92%) to that of another hyperparasitic myxosporean from a gill monogenean from Japan and to numerous multivalvulidan myxosporeans from the genus Kudoa (89-91%). Phylogenetic analyses placed the hyperparasite sequence basally to clades containing Kudoa, Unicapsula and Sphaerospora. CONCLUSIONS: The myxosporean infecting the gill monogenean, Diplectanocotyla gracilis, from the Indo-Pacific tarpon, Megalops cyprinoides, is described as a new species, Myxidium incomptavermi, based on a histozoic development in the monogenean host and its phylogenetic placement.We have demonstrated for the first time that a myxosporean hyperparasite of gill monogeneans is detectable in the fish host. However, myxospores could not be isolated from the fish and confirmation was by PCR alone. The relationship between the myxosporean infection in gill monogeneans and the presence of parasitic DNA in fish is not yet fully understood. Nonetheless, myxospores with a Myxidium-like morphology, two of which we have shown to be phylogenetically related, have now been reported to develop in three different gill monogeneans, indicating that myxosporeans are true parasites of monogeneans.

SUBMITTER: Freeman MA

PROVIDER: S-EPMC3235069 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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Myxosporean hyperparasites of gill monogeneans are basal to the multivalvulida.

Freeman Mark A MA Shinn Andrew P AP

Parasites & vectors 20111124

<h4>Background</h4>Myxosporeans are known from aquatic annelids but parasitism of platyhelminths by myxosporeans has not been widely reported. Hyperparasitism of gill monogeneans by Myxidium giardi has been reported from the European eel and Myxidium-like hyperparasites have also been observed during studies of gill monogeneans from Malaysia and Japan.The present study aimed to collect new hyperparasite material from Malaysia for morphological and molecular descriptions. In addition, PCR screeni ...[more]

PMID: 22115202

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Project description:During the examination of 913 fish specimens belonging to four families in the Campeche Bank (Gulf of Mexico), 23 gill ectoparasitic monogenean species were found, which belong to three families: Dactylogyridae, Microcotylidae and Diclidophoridae. The species Euryhaliotremaamydrum, E.carbuncularium, E.dunlapae, E.fajeravilae, E.fastigatum, E.longibaculum, E.paracanthi, E.tubocirrus, Haliotrematoidescornigerum, H.gracilihamus, H.heteracantha, H.longihamus, H.magnigastrohamus, H.striatohamus, Hamatopedunculariabagre, Neotetraonchusbravohollisae, and N.felis (all Dactylogyridae) were found on the hosts Lutjanussynagris, L.griseus, Ariopsisfelis, Bagremarinus, Archosargusrhomboidalis, and Haemulonplumieri. Additionally, Microcotylearchosargi, Microcotyle sp., and Microcotyloidesincisa (all Microcotylidae) were found on L.griseus and A.rhomboidalis; finally, Choricotyle sp. 1, Choricotyle sp. 2, and Choricotyle sp. 3 (all Diclidophoridae) were found on H.plumieri. The prevalence, abundance, mean intensity of infection, and supplementary taxonomic revisions for all monogeneans found are provided. Partial sequences of the 28S rRNA gene were also obtained for monogeneans of ariid, sparid, and haemulid host fishes to explore their systematic position within the Monogenea. New locality and host records for some previously described species of Euryhaliotrema, Hamatopeduncularia, Microcotyle, and Choricotyle from lutjanid, ariid, sparid, and haemulid hosts were reported. The present study adds evidence supporting the interoceanic occurrence of the same monogenean species (on lutjanids) on the west-east Atlantic and Pacific Oceans (= amphiamerican species). As previously suggested, there are at least, two possibilities to explain that parasite distribution: differentiation of morphological features in these monogeneans have resulted in only slight to insignificant morphological changes developing over the extended period of 3.2 mya (when the Isthmus of Panama was closing) and/or speciation is only evident at molecular level.

Project description:Monogenea is one of the most species-rich groups of parasitic flatworms worldwide, with many species described only recently, which is particularly true for African monogeneans. For example, Cichlidogyrus, a genus mostly occurring on African cichlids, comprises more than 100 nominal species. Twenty-two of these have been described from Lake Tanganyika, a famous biodiversity hotspot in which many vertebrate and invertebrate taxa, including monogeneans, underwent unique and spectacular radiations. Given their often high degrees of host specificity, parasitic monogeneans were also used as a potential tool to uncover host species relationships. This study presents the first investigation of the monogenean fauna occurring on the gills of endemic 'Gnathochromis' species along the Burundese coastline of Lake Tanganyika. We test whether their monogenean fauna reflects the different phylogenetic position and ecological niche of 'Gnathochromis' pfefferi and Gnathochromis permaxillaris. Worms collected from specimens of Limnochromis auritus, a cichlid belonging to the same cichlid tribe as G. permaxillaris, were used for comparison. Morphological as well as genetic characterisation was used for parasite identification. In total, all 73 Cichlidogyrus individuals collected from 'G.' pfefferi were identified as C. irenae. This is the only representative of Cichlidogyrus previously described from 'G.' pfefferi, its type host. Gnathochromis permaxillaris is infected by a species of Cichlidogyrus morphologically very similar to C. gillardinae. The monogenean species collected from L. auritus is considered as new for science, but sample size was insufficient for a formal description. Our results confirm previous suggestions that 'G.' pfefferi as a good disperser is infected by a single monogenean species across the entire Lake Tanganyika. Although G. permaxillaris and L. auritus are placed in the same tribe, Cichlidogyrus sp. occurring on G. permaxillaris is morphologically more similar to C. irenae from 'G.' pfefferi, than to the Cichlidogyrus species found on L. auritus. Various evolutionary processes, such as host-switching or duplication events, might underlie the pattern observed in this particular parasite-host system. Additional samples for the Cichlidogyrus species occuring on G. permaxillaris and L. auritus are needed to unravel their evolutionary history by means of (co-)phylogenetic analyses.

Project description:The phylogenetic relationships of dactylogyrids (Monogenea: Dactylogyridae) parasitising catfishes (Siluriformes) from the Neotropical region were investigated for the first time.Partial sequences of the 28S rRNA gene of 40 specimens representing 25 dactylogyrid species were analysed together with sequences from GenBank using Bayesian inference, Maximum likelihood and Parsimony methods. Monophyly of dactylogyrids infecting catfishes and the Ancyrocephalinae was evaluated using the Approximately Unbiased test.The Ancyrocephalinae is a paraphyletic group of species clustering in three main clades as follows: (i) clade A comprising freshwater dactylogyrids from the Holarctic parasitising perciforms clustering together with species (Ameloblastella, Unibarra and Vancleaveus) parasitising Neotropical catfishes; (ii) clade B including species of Dactylogyrus (Dactylogyrinae) and Pseudodactylogyrus (Pseudodactylogyrinae) along with Ancyrocephalus mogurndae, and marine dactylogyrids with cosmopolitan distribution, parasites of scorpaeniforms and perciforms, along with the freshwater Cichlidogyrus and Scutogyrus (infecting African cichlids [Cichlidae]) and (iii) clade C containing exclusively dactylogyrids of siluriforms, freshwater and marine, with Palaearctic, Ethiopian, Oriental and Neotropical distributions; species of Aphanoblastella and Dactylogyridae gen. sp. 4 from the Neotropical region clustering together with species allocated in the Ancylodiscoidinae, along with species of Cosmetocleithrum, Demidospermus and Dactylogyridae gen. spp.The position of the Ancylodiscoidinae within a larger clade of dactylogyrids (ancyrocephalines) indicates that this subfamily does not represent a natural group. Instead, species allocated to this clade (dactylogyrids of siluriforms along with species of the Ancylodiscoidinae) should be considered as a separate subfamily within the Dactylogyridae. The erection of this taxon requires the search for morphological diagnostic characters in addition to phylogenetic information. A similar strategy should be considered for a new classification of the paraphyletic Ancyrocephalinae. Members of the three clades do not seem to share obvious morphological synapomorphies nor clear patterns in host-parasite associations, zoogeographical distribution or ecology. Clade A should be considered as the Ancyrocephalinae sensu stricto since it includes the type species Ancyrocephalus paradoxus Creplin, 1839. A new subfamily should be proposed to accommodate species currently allocated to Ancyrocephalinae clustering within clade B. Future attempts to propose a new classification of the subfamilies in the Dactylogyridae should include the phylogenetically diverse Neotropical dactylogyrids.

Project description:BackgroundThe patterns and processes linked to the host specificity of parasites represent one of the central themes in the study of host-parasite interactions. We investigated the evolution and determinants of host specificity in gill monogeneans of Cichlidogyrus and Scutogyrus species parasitizing African freshwater fish of Cichlidae.MethodsWe analyzed (1) the link between host specificity and parasite phylogeny, (2) potential morphometric correlates of host specificity (i.e. parasite body size and the morphometrics of the attachment apparatus), and (3) potential determinants of host specificity following the hypothesis of ecological specialization and the hypothesis of specialization on predictable resources (i.e. host body size and longevity were considered as measures of host predictability), and (4) the role of brooding behavior of cichlids in Cichlidogyrus and Scutogyrus diversification.ResultsNo significant relationships were found between host specificity and phylogeny of Cichlidogyrus and Scutogyrus species. The mapping of host specificity onto the parasite phylogenetic tree revealed that an intermediate specialist parasitizing congeneric cichlid hosts represents the ancestral state for the Cichlidogyrus/Scutogyrus group. Only a weak relationship was found between the morphometry of the parasites' attachment apparatus and host specificity. Our study did not support the specialization on predictable resources or ecological specialization hypotheses. Nevertheless, host specificity was significantly related to fish phylogeny and form of parental care.ConclusionsOur results confirm that host specificity is not a derived condition for Cichlidogyrus/Scutogyrus parasites and may reflect other than historical constraints. Attachment apparatus morphometry reflects only partially (if at all) parasite adaptation to the host species, probably because of the morphological similarity of rapidly evolved cichlids (analyzed in our study). However, we showed that parental care behavior of cichlids may play an important role linked to host specificity of Cichlidogyrus/Scutogyrus parasites.

Project description:Background Monogeneans, in general, show a range of unique adaptations to a parasitic lifestyle, making this group enormously diverse. Due to their unique biological properties, diplozoid monogeneans represent an attractive model group for various investigations on diverse biological interactions. However, despite numerous studies, there are still gaps in our knowledge of diplozoid biology and morphofunctional adaptations. Results In this study, we provide a comprehensive microscopic analysis of systems/structures involved in niche searching, sensing and self-protection against the host environment, and excretory/secretory processes in Eudiplozoon nipponicum. Freeze-etching enabled us to detect syncytium organisational features not visible by TEM alone, such as the presence of a membrane subjacent to the apical plasma membrane (separated by a dense protein layer) and a lack of basal plasma membrane. We located several types of secretory/excretory vesicles and bodies, including those attached to the superficial membranes of the tegument. Giant unicellular glands were seen accumulating predominantly in the apical forebody and hindbody haptor region. Muscle layer organisation differed from that generally described, with the outer circular and inner longitudinal muscles being basket-like interwoven by diagonal muscles with additional perpendicular muscles anchored to the tegument. Abundant muscles within the tegumentary ridges were detected, which presumably assist in fixing the parasite between the gill lamellae. Freeze-etching, alongside transmission electron and confocal microscopy with tubulin labelling, enabled visualisation of the protonephridia and nervous system, including the peripheral network and receptor innervation. Three types of receptor were identified: 1) uniciliated sensory endings with a subtle (or missing) tegumentary rim, 2) obviously raised uniciliated receptors with a prominent tegumentary rim (packed with massive innervation and muscles) and 3) non-ciliated papillae (restricted to the hindbody lateral region). Conclusions This study points to specific morphofunctional adaptations that have evolved in diplozoid monogeneans to confront their fish host. We clearly demonstrate that the combination of different microscopic techniques is beneficial and can reveal hidden differences, even in much-studied model organisms such as E. nipponicum. Supplementary Information The online version contains supplementary material available at 10.1186/s40850-021-00087-5.

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Myxosporean hyperparasites of gill monogeneans are basal to the multivalvulida.

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Myxosporean hyperparasites of gill monogeneans are basal to the multivalvulida.

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