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Triple barcoding for a hyperparasite, its parasitic host, and the host itself: a study of Cyclocotyla bellones (Monogenea) on Ceratothoa parallela (Isopoda) on Boops boops (Teleostei).

ABSTRACT: Cyclocotyla bellones Otto, 1823 (Diclidophoridae) is a monogenean characterised by an exceptional way of life. It is a hyperparasite that attaches itself to the dorsal face of isopods, themselves parasites in the buccal cavity of fishes. In this study, Cy. bellones was found on Ceratothoa parallela (Otto, 1828), a cymothoid isopod parasite of the sparid fish Boops boops off Algeria in the Mediterranean Sea. We provide, for the first time, molecular barcoding information of a hyperparasitic monogenean, the parasitic crustacean host, and the fish host, with COI sequences.

SUBMITTER: Bouguerche C

PROVIDER: S-EPMC8183466 | biostudies-literature | 2021

REPOSITORIES: biostudies-literature

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Triple barcoding for a hyperparasite, its parasitic host, and the host itself: a study of Cyclocotyla bellones (Monogenea) on Ceratothoa parallela (Isopoda) on Boops boops (Teleostei).

Bouguerche Chahinez C Tazerouti Fadila F Gey Delphine D Justine Jean-Lou JL

Parasite (Paris, France) 20210607

Cyclocotyla bellones Otto, 1823 (Diclidophoridae) is a monogenean characterised by an exceptional way of life. It is a hyperparasite that attaches itself to the dorsal face of isopods, themselves parasites in the buccal cavity of fishes. In this study, Cy. bellones was found on Ceratothoa parallela (Otto, 1828), a cymothoid isopod parasite of the sparid fish Boops boops off Algeria in the Mediterranean Sea. We provide, for the first time, molecular barcoding information of a hyperparasitic monog ...[more]

PMID: 34096866

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Project description:The relative importance of bottom-up versus top-down control of population dynamics has been the focus of much debate. In infectious disease biology, research is typically focused on the bottom-up process of host resistance, wherein the direction of control flows from the lower to the higher trophic level to impact on pathogen population size and epidemiology. However, the importance of top-down control by a pathogen's natural enemies has been mostly overlooked.Here, we explore the effects of, and interaction between, host genotype (i.e., genetic susceptibility to pathogen infection) and infection by a hyperparasitic fungus, Ampelomyces spp., on the establishment and early epidemic growth and transmission of a powdery mildew plant pathogen (Podosphaera plantaginis). We used a semi-natural field experiment to contrast the impacts of hyperparasite infection, host-plant resistance and spatial structure to reveal the key factors that determine pathogen spread. We then used a laboratory-based inoculation approach to test whether the field experiment results hold across multiple pathogen-host genetic combinations and to explore hyperparasite effects on the pathogen's later life-history stages.We found that hyperparasite infection had a negligible effect on within-host infection development and between-host spread of the pathogen during the onset of epidemics. In contrast, host-plant resistance was the major determinant of whether plants became infected, and host genotype and proximity to an infection source determined infection severity.Our laboratory study showed that, while the interaction between host and pathogen genotypes was the key determinant of infection outcome, hyperparasitism did, on average, reduce the severity of infection. Moreover, hyperparasite infection negatively influenced the production of the pathogen's overwintering structures. Synthesis and applications. Our results suggest that bottom-up host resistance affects pathogen spread, but top-down control of powdery mildew pathogens is likely more effective against later life-history stages. Further, while hyperparasitism in this system can reduce early pathogen growth under stable laboratory conditions, this effect is not detectable in a semi-natural environment. Considering the effects of hyperparasites at multiple points in pathogen's life history will be important when considering hyperparasite-derived biocontrol measures in other natural and agricultural systems.

Project description:BackgroundThe host specificity of fish parasites is considered a useful parasite characteristic with respect to understanding the biogeography of their fish hosts. Dactylogyrus Diesing, 1850 (Monogenea) includes common parasites of cyprinids exhibiting different degrees of host specificity, i.e. from strict specialism to generalism. The phylogenetic relationships and historical dispersions of several cyprinid lineages, including Aulopyge huegelii Heckel, 1843, are still unclear. Therefore, the aims of our study were to investigate (i) the Dactylogyrus spp. parasites of A. huegelii, and (ii) the phylogenetic relationships of Dactylogyrus spp. parasitizing A. huegelii as a possible tool for understanding the phylogenetic position of this fish species within the Cyprininae lineage.ResultsTwo species of Dactylogyrus, D. vastator Nybelin, 1924 and D. omenti n. sp., were collected from 14 specimens of A. huegelii from the Šujica River (Bosnia and Herzegovina). While D. vastator is a typical species parasitizing Carassius spp. and Cyprinus carpio L, D. omenti n. sp. is, according to phylogenetic reconstruction, closely related to Dactylogyrus species infecting European species of Barbus and Luciobarbus. The genetic distance revealed that the sequence for D. vastator from A. huegelii is identical with that for D. vastator from Barbus plebejus Bonaparte, 1839 (Italy) and Carassius gibelio (Bloch, 1782) (Croatia). Dactylogyrus omenti n. sp. was described as a species new to science.ConclusionsOur findings support the phylogenetic position of A. huegelii within the Cyprininae lineage and suggest that A. huegelii is phylogenetically closely related to Barbus and Luciobarbus species. The morphological similarity between D. omenti n. sp. and Dactylogyrus species of Middle Eastern Barbus suggests historical contact between cyprinid species recently living in allopatry and the possible diversification of A. huegelii from a common ancestor in this area. On other hand, the genetic similarity between D. vastator ex A. huegelii and D. vastator ex C. gibelio collected in Balkan Peninsula suggests that A. huegelii was secondarily parasitized by D. vastator, originating from C. gibelio after introduction of this fish species from Asia to Europe.

Dataset Information

Triple barcoding for a hyperparasite, its parasitic host, and the host itself: a study of Cyclocotyla bellones (Monogenea) on Ceratothoa parallela (Isopoda) on Boops boops (Teleostei).

Publications

Triple barcoding for a hyperparasite, its parasitic host, and the host itself: a study of Cyclocotyla bellones (Monogenea) on Ceratothoa parallela (Isopoda) on Boops boops (Teleostei).

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