Hidden diversity of the most basal tapeworms (Cestoda, Gyrocotylidea), the enigmatic parasites of holocephalans (Chimaeriformes)

Abstract Gyrocotylideans are evolutionary ancient parasitic flatworms, and like their hosts—a relict group of holocephalan fishes (Chimaeriformes)—they are considered to be “living fossils” of a vanished past. However, the species diversity, host associations and biogeography of these most basal tap...

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Main Authors: Daniel Barčák, Chia-Kwung Fan, Pasaikou Sonko, Roman Kuchta, Tomáš Scholz, Martina Orosová, Hsuan-Wien Chen, Mikuláš Oros
Format: Article
Language:English
Published: Nature Portfolio 2021-03-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-84613-y
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author Daniel Barčák
Chia-Kwung Fan
Pasaikou Sonko
Roman Kuchta
Tomáš Scholz
Martina Orosová
Hsuan-Wien Chen
Mikuláš Oros
author_facet Daniel Barčák
Chia-Kwung Fan
Pasaikou Sonko
Roman Kuchta
Tomáš Scholz
Martina Orosová
Hsuan-Wien Chen
Mikuláš Oros
author_sort Daniel Barčák
collection DOAJ
description Abstract Gyrocotylideans are evolutionary ancient parasitic flatworms, and like their hosts—a relict group of holocephalan fishes (Chimaeriformes)—they are considered to be “living fossils” of a vanished past. However, the species diversity, host associations and biogeography of these most basal tapeworms are poorly known. Herein, we provide evidence of a conspicuous contrast between the genetic and morphological data based on an examination of newly collected and properly processed Gyrocotyle specimens (hologenophores) isolated from holocephalans off Taiwan and Argentina. Our molecular data, inferred from three genes (COI, 28S rRNA, 18S rRNA), showed unexpected genetic interrelationships among isolates of the genus Gyrocotyle, because each of the four genotypes from Taiwan clustered with isolates of distinct gyrocotylideans from the North Atlantic. Three genotypes of Gyrocotyle from Taiwan were morphologically almost indistinguishable from each other but represented distinct genetic lineages; a single specimen of Gyrocotyle sp. genotype 4 exhibited a clear genetic and morphological distinctness, though its formal description as a new species would be premature. Additionally, specimens of Gyrocotyle rugosa Diesing, 1850, from the type host Callorhinchus callorynchus from Argentina, provided the first genetic data on the type species of the genus and enabled us to characterise it, which is necessary for future taxonomic studies. The finding of some specimens of Gyrocotyle sp. genotype 3 in Chimaera phantasma, and another one in C. cf. argiloba, together with the putative conspecificity of an unidentified gyrocotylidean from Callorhinchus milii off Australia and G. rugosa from C. callorynchus off Argentina, represent evidence that one gyrocotylidean species may parasitise more than one holocephalan host species. Existing taxonomic problems and conflicts between morphological and molecular data on species of Gyrocotyle can only be resolved if hologenophores from type hosts and localities of nominal taxa are properly characterised genetically and morphologically.
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spelling doaj.art-e0309b8b3d7c4ffe898685edce02976c2022-12-21T23:37:47ZengNature PortfolioScientific Reports2045-23222021-03-0111111110.1038/s41598-021-84613-yHidden diversity of the most basal tapeworms (Cestoda, Gyrocotylidea), the enigmatic parasites of holocephalans (Chimaeriformes)Daniel Barčák0Chia-Kwung Fan1Pasaikou Sonko2Roman Kuchta3Tomáš Scholz4Martina Orosová5Hsuan-Wien Chen6Mikuláš Oros7Institute of Parasitology, Slovak Academy of SciencesDepartment of Molecular Parasitology and Tropical Diseases, School of Medicine, College of Medicine, Taipei Medical UniversityDepartment of Molecular Parasitology and Tropical Diseases, School of Medicine, College of Medicine, Taipei Medical UniversityInstitute of Parasitology, Biology Centre of the Czech Academy of SciencesInstitute of Parasitology, Biology Centre of the Czech Academy of SciencesInstitute of Parasitology, Slovak Academy of SciencesDepartment of Biological Resources, National Chiayi UniversityInstitute of Parasitology, Slovak Academy of SciencesAbstract Gyrocotylideans are evolutionary ancient parasitic flatworms, and like their hosts—a relict group of holocephalan fishes (Chimaeriformes)—they are considered to be “living fossils” of a vanished past. However, the species diversity, host associations and biogeography of these most basal tapeworms are poorly known. Herein, we provide evidence of a conspicuous contrast between the genetic and morphological data based on an examination of newly collected and properly processed Gyrocotyle specimens (hologenophores) isolated from holocephalans off Taiwan and Argentina. Our molecular data, inferred from three genes (COI, 28S rRNA, 18S rRNA), showed unexpected genetic interrelationships among isolates of the genus Gyrocotyle, because each of the four genotypes from Taiwan clustered with isolates of distinct gyrocotylideans from the North Atlantic. Three genotypes of Gyrocotyle from Taiwan were morphologically almost indistinguishable from each other but represented distinct genetic lineages; a single specimen of Gyrocotyle sp. genotype 4 exhibited a clear genetic and morphological distinctness, though its formal description as a new species would be premature. Additionally, specimens of Gyrocotyle rugosa Diesing, 1850, from the type host Callorhinchus callorynchus from Argentina, provided the first genetic data on the type species of the genus and enabled us to characterise it, which is necessary for future taxonomic studies. The finding of some specimens of Gyrocotyle sp. genotype 3 in Chimaera phantasma, and another one in C. cf. argiloba, together with the putative conspecificity of an unidentified gyrocotylidean from Callorhinchus milii off Australia and G. rugosa from C. callorynchus off Argentina, represent evidence that one gyrocotylidean species may parasitise more than one holocephalan host species. Existing taxonomic problems and conflicts between morphological and molecular data on species of Gyrocotyle can only be resolved if hologenophores from type hosts and localities of nominal taxa are properly characterised genetically and morphologically.https://doi.org/10.1038/s41598-021-84613-y
spellingShingle Daniel Barčák
Chia-Kwung Fan
Pasaikou Sonko
Roman Kuchta
Tomáš Scholz
Martina Orosová
Hsuan-Wien Chen
Mikuláš Oros
Hidden diversity of the most basal tapeworms (Cestoda, Gyrocotylidea), the enigmatic parasites of holocephalans (Chimaeriformes)
Scientific Reports
title Hidden diversity of the most basal tapeworms (Cestoda, Gyrocotylidea), the enigmatic parasites of holocephalans (Chimaeriformes)
title_full Hidden diversity of the most basal tapeworms (Cestoda, Gyrocotylidea), the enigmatic parasites of holocephalans (Chimaeriformes)
title_fullStr Hidden diversity of the most basal tapeworms (Cestoda, Gyrocotylidea), the enigmatic parasites of holocephalans (Chimaeriformes)
title_full_unstemmed Hidden diversity of the most basal tapeworms (Cestoda, Gyrocotylidea), the enigmatic parasites of holocephalans (Chimaeriformes)
title_short Hidden diversity of the most basal tapeworms (Cestoda, Gyrocotylidea), the enigmatic parasites of holocephalans (Chimaeriformes)
title_sort hidden diversity of the most basal tapeworms cestoda gyrocotylidea the enigmatic parasites of holocephalans chimaeriformes
url https://doi.org/10.1038/s41598-021-84613-y
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