Diversity, phylogeny and intraspecific variability of Paradiplozoon species (Monogenea: Diplozoidae) parasitizing endemic cyprinoids in the Middle East
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
37157105
PubMed Central
PMC10410381
DOI
10.1017/s0031182023000446
PII: S0031182023000446
Knihovny.cz E-zdroje
- Klíčová slova
- Cyprinoidei, evolutionary history, host specificity, parasite fauna, phylogeography,
- MeSH
- biologická evoluce MeSH
- Cyprinidae * MeSH
- fylogeneze MeSH
- Trematoda * genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Turecko epidemiologie MeSH
Diplozoidae are common monogenean ectoparasites of cyprinoid fish, with the genus Paradiplozoon being the most diversified. Despite recent studies on Diplozoidae from Europe, Africa and Asia, the diversity, distribution and phylogeny of this parasite group appears to be still underestimated in the Middle East. The objective of this study was to investigate the diversity, endemism and host specificity of diplozoids parasitizing cyprinoid fish from the Middle East, considering this region as an important historical interchange of fish fauna, and to elucidate the phylogenetic position of Middle Eastern Paradiplozoon species within Diplozoidae. Four Paradiplozoon species were collected from 48 out of 94 investigated cyprinoid species. Three known species, Paradiplozoon homoion, Paradiplozoon bliccae and Paradiplozoon bingolensis, were recorded on new cyprinoid host species, and a new species, Paradiplozoon koubkovae n. sp., was recorded on Luciobarbus capito and Capoeta capoeta from the Caspian Sea basin in Iran and Turkey. Paradiplozoon bliccae, exhibiting a wide host range in the Middle East, expressed both morphological and genetic intraspecific variabilities. The four Paradiplozoon species collected in the Middle East were placed in divergent clades, showing the rich evolutionary history of diplozoid parasites in the Middle East. Our study also revealed that two lineages of African diplozoids have a Middle Eastern origin. We stress the importance of applying an integrative approach combining morphological, ecological and molecular methods to reveal the real diversity of diplozoids.
Department of Ecology Faculty of Science Charles University Viničná 7 Prague 2 128 44 Czech Republic
Department of Zoology National Museum Václavské náměstí 68 Prague 1 110 00 Czech Republic
Faculty of Fisheries Recep Tayyip Erdogan University 53100 Rize Turkey
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Abdul-Ameer KN and Mhaisen FT (2013) Checklists of Gyrodactylus species (Monogenea) from fishes of Iraq. Basrah Journal of Agricultural Sciences 26(1 (special issue)), 8–25.
Al-Nasiri FS (2009) Diplozoid species (Monogenea) parasitizing gills of some cyprinid fishes from Tigris River passing through Tikreet city, Salah Al-Deen province. Iraq Journal of Agricultural Research 14(5), 182–186.
Al-Nasiri FS (2017) Paradiplozoon magnum (Monogenea: Diplozoidae) from some species of cyprinid fish in Tigris River, Iraq. Journal of Tikrit University for Agriculture Sciences 17, 129–133.
Al-Nasiri FS and Balbuena JA (2016) Paradiplozoon iraqensis n. sp. (Monogenea: Diplozoinae) from Cyprinion macrostomum (Cyprinidae) in the Tigris River, Iraq. Acta Parasitologica 61(2), 291–298. PubMed
Arken K, Hao CL, Guo AM, Zhang WR, Rong MJ, Kamal W, Tian SL, Kadir M and Yue C (2021) A new species of Paradiplozoon (Monogenea: Diplozoidae), a gill parasite of the Schizothorax fish (Cyprinidae: Schizothoracinae) from the Yarkand River, Xinjiang, China. Acta Parasitologica 67(1), 330–339. PubMed
Avenant-Oldewage A, Le Roux LE, Mashego SN and Van Vuuren BJ (2014) Paradiplozoon ichthyoxanthon n. sp. (Monogenea: Diplozoidae) from Labeobarbus aeneus (Cyprinidae) in the Vaal River, South Africa. Journal of Helminthology 88(2), 166–172. PubMed
Aydoğdu N, Avenant-Oldewage A, Dos Santos QM and Aydoğdu A (2020) Prevalence and intensity of Paradiplozoon homoion (Monogenea: Diplozoidae) from Manyas spirlin, Alburnoides manyasensis, an endemic fish of Turkey: new host and geographical record. Iranian Journal of Fisheries Sciences 19(6), 3301–3309.
Baehellerie JP and Qu LH (1993) Ribosomal RNA probes for detection and identification of species. In Hyde JE (ed.), Protocols in Molecular Parasitology. Methods in Molecular Biology™, Vol. 21. Totowa, USA: Humana Press, pp. 249–263. 10.1385/0-89603-239-6:249. PubMed DOI
Batra V (1984) Prevalence of helminth parasites in three species of cichlids from a man-made lake in Zambia. Zoological Journal of the Linnean Society 82(3), 319–333.
Benovics M, Koubková B, Civáňová K, Rahmouni I, Čermáková K and Šimková A (2021) Diversity and phylogeny of Paradiplozoon species (Monogenea: Diplozoidae) parasitising endemic cyprinoids in the peri-Mediterranean area, with a description of three new Paradiplozoon species. Parasitology Research 120(2), 481–496. PubMed
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis, et al. revisited. The Journal of Parasitology 83(4), 575–583. PubMed
Bychowsky BE and Nagibina LF (1959) On the systematics of the genus Diplozoon Nordmann (Monogenoidea). Zoologicheskii Zhurnal 38(3), 362–377 (in Russian, summary in English).
Cao S, Fu P, Zou H, Li M, Wu S, Wang G, Blazhekovikj-Dimovska D and Li W (2022) Sindiplozoon coreius n. sp. (Monogenea: Diplozoidae) from the gills of Coreius guichenoti (Cyprinidae) in China. Parasitology International 87, 102494. PubMed
Cinar ME (2014) Checklist of the phyla Platyhelminthes, Xenacoelomorpha, Nematoda, Acanthocephala, Myxozoa, Tardigrada, Cephalorhyncha, Nemertea, Echiura, Brachiopoda, Chaetognatha, and Chordata (Tunicata, Cephalochordata, and Hemichordata) from the coasts of Turkey. Turkish Journal of Zoology 38(6), 698–722.
Cinar ME, Mhaisen FT, Al-Rubaie AL, Selver M, Aydoğdu A, Cirak V, Borji H, Naghibi A, Nasiri MR and Ahmadi A (2016) Checklists of fish parasites of Al-Najaf Al-Ashraf province, Iraq. Turkish Journal of Zoology 38(6), 86–95.
Civáňová K, Koyun M and Koubková B (2013) The molecular and morphometrical description of a new diplozoid species from the gills of the Garra rufa (Heckel, 1843) (Cyprinidae) from Turkey – including a commentary on taxonomic division of Diplozoidae. Parasitology Research 112(8), 3053–3062. PubMed
Coad BW (1996) Zoogeography of the fishes of the Tigris-Euphrates Basin. Zoology in the Middle East 13(1), 51–70.
Dos Santos QM and Avenant-Oldewage A (2016) The description of a new diplozoid species, Paradiplozoon krugerense n. sp., from Labeo rosae Steindachner, 1894 and Labeo congoro Peters, 1852 in the Kruger National Park, South Africa with notes on the effect of water quality on its infection variables. Hydrobiologia 777(1), 225–241. 10.1007/s10750-016-2776-9 DOI
Dos Santos QM and Avenant-Oldewage A (2020) Review on the molecular study of the Diplozoidae: analyses of currently available genetic data, what it tells us, and where to go from here. Parasites & Vectors 13(1), 539. PubMed PMC
Dos Santos QM, Van Vuuren BJ and Avenant-Oldewage A (2015) Paradiplozoon vaalense n. sp. (Monogenea: Diplozoidae) from the gills of moggel, Labeo umbratus (Smith, 1841), in the Vaal River System, South Africa. Journal of Helminthology 89(1), 58–67. PubMed
Dos Santos QM, Dzika E and Avenant-Oldewage A (2019) Using scanning electron microscopy (SEM) to study morphology and morphometry of the isolated haptoral sclerites of three distinct diplozoid species. PLoS ONE 14(2), e0211794. PubMed PMC
Durand JD, Tsigenopoulos CS, Ünlü E and Berrebi P (2002) Phylogeny and biogeography of the family Cyprinidae in the Middle East inferred from cytochrome b DNA – evolutionary significance of this region. Molecular Phylogenetics and Evolution 22(1), 91–100. PubMed
Echi PC and Ezenwaji HMG (2010) The parasite fauna of characids’ (Osteichthyes: Characidae) Anambra River, Nigeria. African Journal of Ecology 48(1), 1–4.
Ergens R (1976) Variability of hard parts of opisthaptor of two species of Gyrodactylus Nordmann, 1832 (Monogenoidea) from Phoxinus phoxinus (L.). Folia Parasitologica 23(2), 111–126. PubMed
Ergens R and Gelnar M (1985) Experimental verification of the effect of temperature on the size of hard parts of opisthaptor of Gyrodactylus katharineri Malmberg, 1964 (Monogenea). Folia Parasitologica 32, 377–380.
Fan L, Meng F, Bai J, Xu W and Wang X (2018) Paradiplozoon yunnanensis n. sp. (Monogenea, Diplozoidae) from Sikukia gudgeri (Cyprinidae, Barbinae) in southwest China. Parasite 25, 46. PubMed PMC
Gelnar M, Koubková B, Pláňková H and Jurajda P (1994) Report on metazoan parasites of fishes of the river Morava with remarks on the effects of water pollution. Helminthologia 31(1/2), 47–56.
Georgiev B (1986) In toto staining method for cestodes with iron acetocarmine. Helminthologia 23, 279–281.
Gilbert BM and Avenant-Oldewage A (2016a) Effects of altered water quality and trace elements on the infection variables of Paradiplozoon ichthyoxanthon (Monogenea: Diplozoidae) from two sites in the Vaal River System, South Africa. Acta Parasitologica 61(1), 52–62. PubMed
Gilbert BM and Avenant-Oldewage A (2016b) Seasonal occurrence and microhabitat specificity of Paradiplozoon ichthyoxanthon Avenant-Oldewage in Avenant-Oldewage, et al., 2014 (Monogenea: Diplozoidae) infecting Labeobarbus aeneus (Burchell) (Teleostei: Cyprinidae) from the Vaal Dam, South Africa: water quality and host size as determining factors? Folia Parasitologica 63, 2016.004. PubMed
International Commission on Zoological Nomenclature (2012) Amendment of articles 8, 9, 10, 21 and 78 of the International Code of Zoological Nomenclature to expand and refine methods of publication. ZooKeys 219, 1–10. PubMed PMC
İnnal D, Ünal MC, Çaglan DC, Civáňová K and Özmen Ö (2020) Some parasitological features of Paradiplozoon bliccae (Monogenea: Diplozoidae) infestation in Pseudophoxinus burduricus an endemic fish species from Doğanbaba creek (Lake Salda, Turkey). Acta Aquatica Turcica 16(4), 498–505.
Jiang NC, Wu BH and Wang SX (1985) Four new species of Diplozoon from Zhejiang and Jiangxi provinces in China. Acta Zootaxonomica Sinica 10, 117–118.
Jirsová D, Ding X, Civáňová K, Jirounková E, Ilgová J, Koubková B, Kašný M and Gelnar M (2018) Redescription of Paradiplozoon hemiculteri (Monogenea, Diplozoidae) from the type host Hemiculter leucisculus, with neotype designation. Parasite 25, 4. PubMed PMC
Jirsová D, Koubková B, Jirounková E, Vorel J, Zhou X, Ding X, Gelnar M and Kašný M (2021) Redescription of Paradiplozoon opsariichthydis (Jiang, Wu et Wang 1984) Jiang, Wu et Wang, 1989 (Monogenea, Diplozoidae). Parasitology International 84, 102409. PubMed
Kaci-Chaouch T, Verneau O and Desdevises Y (2008) Host specificity is linked to intraspecific variability in the genus Lamellodiscus (Monogenea). Parasitology 135(5), 607–616. PubMed
Katoh K, Misawa K, Kuma K and Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30(14), 3059–3066. PubMed PMC
Keane TM, Creevey CJ, Pentony MM, Naughton TJ and Mclnerney JO (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evolutionary Biology 6(1), 29. PubMed PMC
Khotenovsky I (1985a) Fauna of the USSR. Monogenea. Leningrad: Nauka; (in Russian).
Khotenovsky I (1985b) The Subclass Octomacrinea Khotenovsky. Leningrad: Nauka; (in Russian).
Kmentová N, Van Steenberge M, Raeymaekers JAM, Koblmüller S, Hablützel PI, Bukinga FM, N'sibula TM, Mulungula PM, Nzigidahera B and Ntakimazi G (2018) Monogenean parasites of sardines in Lake Tanganyika: diversity, origin and intraspecific variability. Contributions to Zoology 87(2), 105–132.
Littlewood DTJ, Rohde K and Clough KA (1997) Parasite speciation within or between host species? – Phylogenetic evidence from site-specific polystome monogeneans. International Journal for Parasitology 27(11), 1289–1297. PubMed
Machordom A and Doadrio I (2001) Evidence of a Cenozoic Betic-Kabilian connection based on freshwater fish phylogeography (Luciobarbus, Cyprinidae). Molecular Phylogenetics and Evolution 18, 252–263. PubMed
Malmberg G (1957) Om förekomsten av Gyrodactylus på svenska fiskar. Skrifter Utgivna av Södra Sveriges Fiskeriförening, Årsskrift, 19–76 (Swedish, with description of species and a summary in English).
Matějusová I, Gelnar M, McBeath AJA, Collins CM and Cunningham CO (2001a) Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). International Journal for Parasitology 31(7), 738–745. PubMed
Matějusová I, Koubková B, D'amelio S and Cunningham CO (2001b) Genetic characterization of six species of diplozoids (Monogenea; Diplozoidae). Parasitology 123(5), 465–474. PubMed
Matějusová I, Koubková B, Gelnar M and Cunningham CO (2002) Paradiplozoon homoion Bychowsky and Nagibina, 1959 versus P. gracile Reichenbach-Klinke, 1961 (Monogenea): two species or phenotypic plasticity? Systematic Parasitology 53(1), 39–47. PubMed
Matějusová I, Koubková B and Cunningham CO (2004) Identification of European diplozoids (Monogenea, Diplozoinae) by restriction digestion of the ribosomal RNA internal transcribed spacer. Journal of Parasitology 90(4), 817–822. PubMed
Mbokane EM, Theron J and Luus-Powell WJ (2019) Seasonal occurrence and ecological aspects of Afrodiplozoon polycotyleus (Monogenea: Diplozoidae) from the gills of three cyprinids from the Nwanedi-Luphephe dams, South Africa. African Journal of Aquatic Science 44(1), 53–60.
Mhaisen FT (2019) Checklists of parasites of fishes of Thi-Qar province, Iraq. Biological and Applied Environmental Research 3(2), 152–167.
Mhaisen FT and Abdul-Ameer KN (2014) Checklists of diplozoid species (Monogenea) from fishes of Iraq. Bulletin of the Iraq Natural History Museum 13(2), 95–110.
Mhaisen FT and Abdullah SMA (2017) Parasites of fishes of Kurdistan region, Iraq: checklists. Biological and Applied Environmental Research 1(2), 131–218.
Moravec F (2001) Checklist of the Metazoan Parasites of Fishes of the Czech Republic and the Slovak Republic (1873–2000). Prague, Czech Republic: Academia.
Nguyen LT, Schmidt HA, Von Haeseler A and Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32(1), 268–274. PubMed PMC
Nicoll W (1924) A reference list of the trematode parasites of British freshwater fishes. Parasitology 16(2), 127–144.
Nishihira T and Urabe M (2020) Morphological and molecular studies of Eudiplozoon nipponicum (Goto, 1891) and Eudiplozoon kamegaii sp. n. (Monogenea; Diplozoidae). Folia Parasitologica 67, 2020.018. PubMed
Nitta M and Nagasawa K (2018) Gyrodactylus medaka n. sp. (Monogenea: Gyrodactylidae) parasitic on wild and laboratory-reared medaka Oryzias latipes (Beloniformes: Adrianichthyidae) in Japan. Parasitology International 67(5), 651–658. PubMed
Öktener A (2003) A checklist of metazoan parasites recorded in freshwater fish from Turkey. Zootaxa 394, 1–28.
Öktener A (2014) Revision of parasitic helminths reported in freshwater fish from Turkey with new records. Transylvanian Review of Systematical and Ecological Research 16(1), 1–56.
Owen IL (1963) The attachment of the monogenean Diplozoon paradoxum to the gills of Rutilus rutilus L. I. Micro-habitat and adhesive attitude. Parasitology 53(3–4), 455–461.
Paperna I (1969) Monogenetic trematodes of the fish of the Volta basin and south Ghana. Bulletin de l'Institut Francais d'Afrique Noire. Serie A. Sciences Naturelles 31(3), 840–880.
Paperna I (1979) Monogenea of inland water fish in Africa. In Annales Musee Royal de l'Afrique Centrale – Sciences Zoologiques, Seria In-8 deg No. 226. pp. viii + 131, Tervuren, Belgium: Royal Museum for Central Africa.
Pazooki J and Masoumian M (2012) Synopsis of the parasites in Iranian freshwater fishes. Iranian Journal of Fisheries Sciences 11(3), 570–589.
Přikrylová I, Mašová Š, Gelnar M, Matla MM, Tavakol S and Luus-Powell WJ (2018) Redescription of the genus Afrodiplozoon Khotenovsky, 1981 and its only known species Afrodiplozoon polycotyleus (Paperna, 1973) (Monogenea: Diplozoidae) using a combined multidisciplinary approach. Parasitology International 67(2), 245–252. PubMed
Pugachev ON, Gerasev PI, Gussev AV, Ergens R and Khotenowsky I (2009) Guide to Monogenoidea of Freshwater Fish of Palaearctic and Amur Regions. Milan, Italy: Ledizione-Ledi Publishing.
Rahmouni C, Van Steenberge M, Vanhove MPM and Šimková A (2021) Intraspecific morphological variation in Cichlidogyrus (Monogenea) parasitizing two cichlid hosts from Lake Tanganyika exhibiting different dispersal capacities. Hydrobiologia 848(16), 3833–3845.
Rahmouni C, Vanhove MPM, Šimková A and Van Steenberge M (2022) Morphological and genetic divergence in a gill monogenean parasitizing distant cichlid lineages of lake Tanganyika: Cichlidogyrus nshomboi (Monogenea: Dactylogyridae) from representatives of Boulengerochromini and Perissodini. Evolutionary Biology 49(2), 221–238.
Rambaut A, Drummond AJ, Xie D, Baele G and Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67(5), 901–904. PubMed PMC
Řehulková E, Seifertová E, Přikrylová I and Francová K (2018) Monogenea. In Scholz T, Vanhove PM, Smit N and Gelnar M (eds), A Guide to the Parasites of African Freshwater Fishes. Brussels, Belgium: Royal Belgian Institute of Natural Sciences, Abc Taxa1, pp. 185–243.
Řehulková E, Rahmouni I, Pariselle A and Šimková A (2021) Integrating morphological and molecular approaches for characterizing four species of Dactylogyrus (Monogenea: Dactylogyridae) from Moroccan cyprinids, with comments on their host specificity and phylogenetic relationships. PeerJ 9, e10867. PubMed PMC
Reiczigel J, Marozzi M, Fábián I and Rózsa L (2019) Biostatistics for parasitologists – a primer to quantitative parasitology. Trends in Parasitology 35(4), 277–281. PubMed
Rohlenová K, Morand S, Hyršl P, Tolarová S, Flajšhans M and Šimková A (2011) Are fish immune systems really affected by parasites? An immunoecological study of common carp (Cyprinus carpio). Parasites & Vectors 4(1), 120. PubMed PMC
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA and Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3), 539–542. PubMed PMC
Rózsa L, Reiczigel J and Majoros G (2000) Quantifying parasites in samples of hosts. Journal of Parasitology 86(2), 228–232. PubMed
Šanda R, Vukić J, Choleva L, Křížek J, Šedivá A, Shumka S and Wilson IF (2008) Distribution of loach fishes (Cobitidae, Nemacheilidae) in Albania, with genetic analysis of populations of Cobitis ohridana. Folia Zoologica 57, 42–50.
Shah HB, Yousuf AR, Chishti MZ and Ahmad F (2013) Seasonal changes in infrapopulations of Diplozoon kashmirensis Kaw, 1950 (Monogenea: Diplozoidae) along a eutrophic gradient. Parasitology Research 112(9), 3347–3356. PubMed
Sicard M, Desmarais E and Lambert A (2001) Caractérisation moléculaire des populations de Diplozoidae sur cinq espèces de Cyprinidae: nouvelles données sur la spécificité parasitaire. Comptes Rendus de l'Académie Des Sciences-Series III-Sciences de La Vie 324(8), 709–717 (in French, with summary in English). PubMed
Sicard M, Desmarais E and Lambert C (2002) Is the Octomacridae the sister family of the Diplozoidae? Parasite 9(1), 85–87. PubMed
Šimková A, Morand S, Jobet E, Gelnar M and Verneau O (2004) Molecular phylogeny of congeneric monogenean parasites (Dactylogyrus): a case of intrahost speciation. Evolution 58, 1001–1018. PubMed
Šimková A, Pečínková M, Řehulková E, Vyskočilová M and Ondračková M (2007) Dactylogyrus species parasitizing European Barbus species: morphometric and molecular variability. Parasitology 134(12), 1751–1765. PubMed
Smyth JD and Halton DW (1983) The Physiology of Trematodes, 2nd Edn. Cambridge, UK: Cambridge University Press.
Sterba VG (1957) Zur morphologie und biologie der gattung Diplozoon. Zoologischer Anzeiger 158, 181–196.
Tamura K, Stecher G and Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution 38(7), 3022–3027. PubMed PMC
Thomas JD (1957) A new monogenetic trematode, Diplozoon ghanense sp. nov. (Polyopistho-cotylea: Discocotylea) from a West African freshwater fish Alestes macrolepidotus (C. and V., 1849), in West Africa. Journal of the West African Science Association 3(2), 178–182.
Unal MC, Innal D, Civáňová K, Stavrescu-Bedivan MM, Koubková B, Ozmen O and Gelnar M (2017) Identification of two gill parasites Lamproglena compacta (Copepoda: Lernaeidae) and Paradiplozoon bliccae (Monogenea: Diplozoidae) from endemic Aegean chub (Squalius fellowesii). Bulletin of the European Association of Fish Pathologists 37(4), 135–147.
Yildirim YB, Zeren A, Genc E, Erol C and Konas E (2010) Parasitological investigation on commercially important fish and crustacean species collected from the TIGEM (Dortyol Turkey) ponds. Journal of Animal and Veterinary Advances 9(11), 1597–1602.