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Morphological and genetic variability of the cryptic Gyrodactylus sphinx and Gyrodactylus gerasevi n. sp. (Platyhelminthes: Monogenea) from the Mediterranean Sea and Black Sea: two new members of the cross-ocean distributed Gyrodactylus orecchiae species group

Published online by Cambridge University Press:  04 February 2022

E. Dmitrieva Open the ORCID record for E. Dmitrieva [Opens in a new window] ,
D. Sanna ,
E. Vodiasova ,
D. Prokhorova ,
M. Casu ,
C. Burreddu ,
M.C. Piras ,
G. Garippa  and
P. Merella
E. Dmitrieva*
Affiliation:
Department of Ecological Parasitology, A.O. Kovalevsky Institute of Biology of the Southern Seas, Moscow, Russia
D. Sanna
Affiliation:
Dipartimento di Scienze Biomediche, Università di Sassari, Sassari, Italy
E. Vodiasova
Affiliation:
Laboratory of Biodiversity and Functional Genomics of the World Ocean, A.O. Kovalevsky Institute of Biology of the Southern Seas, Moscow, Russia
D. Prokhorova
Affiliation:
Department of Ecological Parasitology, A.O. Kovalevsky Institute of Biology of the Southern Seas, Moscow, Russia
M. Casu
Affiliation:
Dipartimento di Medicina Veterinaria, Università di Sassari, Sassari, Italy
C. Burreddu
Affiliation:
Dipartimento di Medicina Veterinaria, Università di Sassari, Sassari, Italy
M.C. Piras
Affiliation:
Dipartimento di Medicina Veterinaria, Università di Sassari, Sassari, Italy
G. Garippa
Affiliation:
Dipartimento di Medicina Veterinaria, Università di Sassari, Sassari, Italy
P. Merella
Affiliation:
Dipartimento di Medicina Veterinaria, Università di Sassari, Sassari, Italy
*
Author for correspondence: E. Dmitrieva, E-mail: [email protected]
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Abstract

Gyrodactylus sphinx Dmitrieva & Gerasev, 2000 is the only species of Gyrodactylus originally described from Aidablennius sphynx (Valenciennes) in the Black Sea. In the present study, monogeneans similar to G. sphinx are reported from the same host and from two other species of Blenniidae from the Black Sea, as well as from the Mediterranean Sea. This study aims to verify the taxonomic status of the specimens found in different hosts and localities, other than the type ones of G. sphinx. Twenty-two measurements of the haptoral structures of 169 gyrodactylids were used for the morphological study. Morphometric variability between different samples was analysed using analysis of variance, multivariate analysis of variance (MANOVA) and principal component analysis (PCA). Molecular studies were carried out using the nuclear internal transcribed spacer 2 and 5.8S ribosomal DNA regions. Network, Bayesian phylogenetic and species delimitation analyses were performed to infer the number of taxonomic units and the phylogeographic relationships occurring within and among them. MANOVA revealed a significant dependence of the morphometry of hamuli and marginal hooks on host species and regions, but a clear differentiation between samples was not confirmed by PCA. Moreover, the ranges of all dimensions overlapped between samples. However, molecular analyses suggested the occurrence of at least two taxonomic entities. The most common entity was present in individuals of the Black and Mediterranean seas, and is described here as Gyrodactylus gerasevi n. sp., whereas a second entity recognized as a G. sphinx was found only in individuals from two localities off Crimea. The monophyletic cluster grouping of these two species was placed within a large clade that also included a separate sister cluster with seven other species of the Gyrodactylus orecchiae cross-ocean species group.

Keywords

GyrodactylusMonogeneaPlatyhelminthesmorphological variabilitygenetic diversityphylogenetic relationshipsMediterranean SeaBlack Sea
Type
Research Paper
Information
Journal of Helminthology , Volume 96 , 2022 , e9
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Bakke, TA, Harris, PD and Cable, J (2002) Host specificity dynamics: observations on gyrodactylid monogeneans. International Journal for Parasitology 32, 281–308.CrossRefGoogle ScholarPubMed
Bandelt, HJ, Forster, P and Rohl, A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.CrossRefGoogle ScholarPubMed
Bueno-Silva, M, Boeger, WA and Pie, MR (2011) Choice matters: incipient speciation in Gyrodactylus corydori (Monogenoidea: Gyrodactylidae). International Journal for Parasitology 41, 657–667.CrossRefGoogle Scholar
Cable, J, Harris, PD, Tinsley, RC and Lazarus, CM (1999) Phylogenetic analysis of Gyrodactylus spp. (Platyhelminthes: Monogenea) using ribosomal DNA sequences. Canadian Journal of Zoology 77, 1439–1449.CrossRefGoogle Scholar
Cossu, P, Dedola, GL, Scarpa, F, Sanna, D, Lai, T, Maltagliati, F, Curini-Galletti, M and Casu, M (2015) Patterns of spatial genetic variation in Patella ulyssiponensis: insights from the western Mediterranean marine ecoregion. Hydrobiologia 755(1), 39–55.CrossRefGoogle Scholar
Dmitrieva, EV (2003) Transmission triggers and pathways in Gyrodactylus sphinx (Monogenea, Gyrodacylidae). Vestnik Zoologii 37, 67–72.Google Scholar
Dmitrieva, E and Dimitrov, G (2002) Variability in the taxonomic characters of Black Sea gyrodactylids (Monogenea). Systematic Parasitology 51, 199–206.CrossRefGoogle Scholar
Dmitrieva, EV and Gerasev, PI (1997) [To the fauna of Gyrodactylus (Gyrodactylidae, Monogenea) on the Black Sea fishes]. Zoologicheskii Zhurnal 76, 979–984 (in Russian).Google Scholar
Dmitrieva, EV, Gerasev, PI, Garippa, G, Piras, MC and Merella, P (2015) The first record of Gyrodactylus corleonis Paladini, Cable, Fioravanti, Faria & Shinn, 2010 (Monogenea: Gyrodactylidae) from the wild. Systematic Parasitology 92, 65–72.CrossRefGoogle Scholar
Ergens, RR (1985) [Order Gyrodactylidea.]. pp. 269–347 in Bauer, ON (Eds) [Key to parasites of freshwater fish of the fauna of the USSR. Vol. 2. Parasitic metazoans]. Leningrad, Nauka (in Russian).Google Scholar
Euzet, L, Combes, C and Caro, A (1993) A checklist of Monogenea of Mediterranean fish in Second International Symposium on Monogenea. Montpellier/Sète, 5–8 July 1993.Google Scholar
Geets, A, Appleby, C and Ollevier, F (1999) Host-dependent and seasonal variation in opisthaptoral hard parts of Gyrodactylus cf. arcuatus from three Pomatoschistus spp. and G. arcuatus from Gasterosteus aculeatus: a multivariate approach. Parasitology 119, 27–40.CrossRefGoogle Scholar
Gelman, A and Rubin, DB (1992) Inference from iterative simulation using multiple sequences. Statistical Science 7, 457–472.CrossRefGoogle Scholar
Gerasev, PI and Dmitrieva, EV (2004) [A redescription of Gyrodactylus atherinae Bychowsky, 1933 based on the collection of В.E. Bychowsky of 1947 from Atherina boyeri pontica in the Black Sea]. Parazitologiya 38, 562–565 (in Russian).Google Scholar
Gerasev, PI and Dmitrieva, EV (2005) [The description of Gyrodactylus mulli sp. n. (Monogenea: Gyrodactylidae) from the Black Sea blunt-snouted mullet Mullus barbatus ponticus]. Parazitologiya 39, 327–331 (in Russian).Google Scholar
Gusev, AV (1983) [Methods of collection and processing material of monogeneans parasitizing fish]. Leningrad, Nauka (in Russian).Google Scholar
Hahn, C, Bakke, TA, Bachmann, L, Weiss, S and Harris, PD (2011) Morphometric and molecular characterization of Gyrodactylus teuchis Lautraite, Blanc, Thiery, Daniel & Vigneulle, 1999 (Monogenea: Gyrodactylidae) from an Austrian brown trout population. Parasitology International 60, 480–487.CrossRefGoogle ScholarPubMed
Hall, TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Harris, PD (1998) Extreme morphological variation between related individuals of Gyrodactylus pungitti Malmberg, 1964 (Monogenea). Systematic Parasitology 39, 137–140.CrossRefGoogle Scholar
Harris, PD, Shinn, AP, Cable, J and Bakke, TA (2004) Nominal species of the genus Gyrodactylus von Nordmann 1832 (Monogenea: Gyrodactylidae), with a list of principal host species. Systematic Parasitology 59, 1–27.CrossRefGoogle Scholar
Hsiu-Chin, L and Hastings, PA (2013) Phylogeny and biogeography of a shallow water fish clade (Teleostei: Blenniiformes). BMC Evolutionary Biology 13, 210.Google Scholar
Huyse, T and Volckaert, FAM (2002) Identification of a host-associated species complex using molecular and morphometric analyses, with description of Gyrodactylus rugiensoides n. sp. (Gyrodactylidae, Monogenea). International Journal for Parasitology 32, 907–919.CrossRefGoogle Scholar
Huyse, T, Audenaert, V and Volckaert, FA (2003) Speciation and host-parasite relationships in the parasite genus Gyrodactylus (Monogenea, Platyhelminthes) infecting gobies of the genus Pomatoschistus (Gobiidae, Teleostei). International Journal for Parasitology 33, 1679–1689.CrossRefGoogle Scholar
Huyse, T, Malmberg, G and Volckaert, FAM (2004) Four new species of Gyrodactylus von Nordmann, 1832 (Monogenea, Gyrodactylidae) on gobiid fishes: combined DNA and morphological analyses. Systematic Parasitology 59, 103–120.CrossRefGoogle ScholarPubMed
Huyse, T, Pampoulie, C, Audenaert, V and Volckaert, FAM (2006) First report of Gyrodactylus spp. (Platyhelminthes: Monogenea) in the western Mediterranean Sea: molecular and morphological descriptions. Journal of Parasitology 92, 682–690.CrossRefGoogle ScholarPubMed
Jones, MK, Ernst, E and Whittington, ID (1997) Variation in the egg cell forming region of Gyrodactylus kobayashii Hukuda, 1940 (Monogenea: Gyrodactylidae). International Journal for Parasitology 27, 507–516.CrossRefGoogle Scholar
Kimura, M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.CrossRefGoogle ScholarPubMed
Korotaev, G (2003) Seasonal, interannual, and mesoscale variability of the Black Sea upper layer circulation derived from altimeter data. Journal of Geophysical Research 108(C4), 3122.CrossRefGoogle Scholar
Kritsky, DC, Ali, AH and Khamees, NR (2013) Gyrodactylus aff. Mugili Zhukov, 1970 (Monogenoidea: Gyrodactylidae) from the gills of mullets (Mugiliformes: Mugilidae) collected from the inland waters of southern Iraq, with an evaluation of previous records of Gyrodactylus spp. on mullets in Iraq. Folia Parasitologica 60(5), 441–447.CrossRefGoogle Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Kvach, Y, Ondračková, M, Seifertová, M and Hulak, B (2019) Gyrodactylus ginestrae n. sp. (Monogenea: Gyrodactylidae), a parasite of the big-scale sand smelt, Atherina boyeri Risso, 1810 (Actinopterygii: Atherinidae) from the Black Sea. Parasitology Research 118, 3315–3325.CrossRefGoogle Scholar
Lebedeva, D, Muñoz, G and Lumme, J (2021) New salinity tolerant species of Gyrodactylus (Platyhelminthes, Monogenea) on intertidal and supratidal fish species from the Chilean coast. Acta Parasitologica 66, 1021–1030.CrossRefGoogle ScholarPubMed
Librado, P and Rozas, J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.CrossRefGoogle ScholarPubMed
Lumme, J, Ziętara, MS and Lebedeva, D (2017) Ancient and modern genome shuffling: reticulate mitonuclear phylogeny of four related allopatric species of Gyrodactylus von Nordmann, 1832 (Monogenea: Gyrodactylidae), ectoparasites on the Eurasian minnow Phoxinus phoxinus (L.) (Cyprinidae). Systematic Parasitology 94, 183–200.CrossRefGoogle Scholar
Malmberg, G (1970) The excretory systems and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, Monogenea). Arkiv för Zoologi 23, 1–235.Google Scholar
Maltsev, V and Miroshnichenko, A (1998) On transcontinental transfer of parasites from the Far East into the Black and Azov seas in the process of haarder (Mugil soiuy) acclimatization [ICOPA IX abstract]. Parasitology International 47, 32.Google Scholar
Matějusová, I, Gelnar, M, McBeath, AJA, Collins, CM and Cunningham, CO (2001) Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). International Journal for Parasitology 31, 738–745.CrossRefGoogle Scholar
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. pp. 1–8 in Proceedings of the gateway computing environments workshop (GCE). New Orleans, LA.CrossRefGoogle Scholar
Mo, TA (1991a) Variations of opisthaptoral hard parts of Gyrodactylus salaries Malmberg, 1957 (Monogenea: Gyrodactylidae) on parr of Atlantic salmon Salmo salar L. in laboratory experiments. Systematic Parasitology 20, 11–19.CrossRefGoogle Scholar
Mo, TA (1991b) Variations of opisthaptoral hard parts of Gyrodactylus salaries Malmberg, 1957 (Monogenea: Gyrodactylidae) on rainbow trout Oncorhynchus mykiss (Walbaum, 1792) in a fish farm, with comments on the spreading of the parasite in south-eastern Norway. Systematic Parasitology 20, 1–9.CrossRefGoogle Scholar
Olstad, K, Bachmann, L and Bakke, TA (2009) Phenotypic plasticity of taxonomic and diagnostic structures in gyrodactylosis-causing flatworms (Monogenea, Platyhelminthes). Parasitology 136, 1305–1315.CrossRefGoogle Scholar
Ondračková, M (2016) Gyrodactylus proterorhini in its non-native range: distribution and ability to host-switch in freshwaters. Parasitology Research 115, 3135–3162.CrossRefGoogle ScholarPubMed
Paladini, G, Cable, J, Fioravanti, ML, Faria, PJ, Di Cave, D and Shinn, AP (2009) Gyrodactylus orecchiae sp. n. (Monogenea: Gyrodactylidae) from farmed population of gilthead seabream (Sparus aurata) in the Adriatic Sea. Folia Parasitologica 56, 21–28.CrossRefGoogle Scholar
Paladini, G, Cable, J, Fioravanti, ML, Faria, PJ and Shinn, AP (2010) The description of Gyrodactylus corleonis sp. n. and G. Neretum sp. n. (Platyhelminthes: Monogenea) with comments on other gyrodactylids parasitizing pipefish (Pisces: Sygnathidae). Folia Parasitologica 57, 17–30.CrossRefGoogle Scholar
Paladini, G, Hansen, H, Fioravanti, ML and Shinn, AP (2011) Gyrodactylus longipes n. sp. (Monogenea: Gyrodactylidae) from farmed population of gilthead seabream (Sparus aurata L.) from the Mediterranean. Parasitology International 60, 410–418.CrossRefGoogle Scholar
Posada, D (2008) Jmodeltest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.CrossRefGoogle ScholarPubMed
Puillandre, N, Lambert, A, Brouillet, S and Achaz, G (2012) ABGD, automatic barcode Gap discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.CrossRefGoogle ScholarPubMed
Razo-Mendivil, U, García-Vásquez, A and Rubio-Godoy, M (2016) Spot the difference: two cryptic species of Gyrodactylus von Nordmann, 1832 (Platyhelminthes: Monogenea) infecting Astyanax aeneus (Actinopterygii, Characidae) in Mexico. Parasitology International 65, 389–400.CrossRefGoogle Scholar
Ronquist, F and Huelsenbeck, JP (2003) Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Ronquist, F, Teslenko, M, van der Mark, P, et al. (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Scarpa, F, Sanna, D, Cossu, P, Lai, T, Casu, M and Curini-Galletti, M (2019) How to achieve internal fertilization without a vagina: the study case of the genus Archilina Ax, 1959 (Platyhelminthes, Proseriata) from Canary Islands. Marine Biodiversity 49, 2057–2073.CrossRefGoogle Scholar
Shinn, AP, Gibson, DI and Sommerville, C (2001) Morphometric discrimination of Gyrodactylus salaries Malmberg (Monogenea) from species of Gyrodactylus parasitising British salmonids using novel parameters. Journal of Fish Diseases 24, 83–97.CrossRefGoogle Scholar
Shinn, AP, Hansen, H, Olstad, K, Bachmann, L and Bakke, T (2004) The use of morphometric characters to discriminate specimens of laboratory-reared and wild populations of Gyrodactylus salaris and G. Thymalli (Monogenea). Folia Parasitologica 51, 239–252.CrossRefGoogle Scholar
Sokolov, SG (2010) New data on helminths of juvenile starry flounder Platichthys stellatus (Pallas, 1787) (Osteichthyes, Pleuronectidae) inhabiting Western Kamchatka rivers. Inland Water Biology 3(1), 79–84.CrossRefGoogle Scholar
Stoyanov, B, Huyse, T, Pankov, P and Georgiev, BB (2016) Morphological and molecular identification of Gyrodactylus bubyri Osmanov, 1965 (Monogenea: Gyrodactylidae) from Caucasian dwarf goby, Knipowitschia caucasica (Berg) (Actinopterygii: Gobionellidae) from a Black Sea lagoon. Parasitology Research 115(4), 1617–1625.CrossRefGoogle Scholar
Strona, G, Stefani, F and Galli, P (2010) Monogenoidean parasites of Italian marine fish: an updated checklist. Italian Journal of Zoology 77, 419–437.CrossRefGoogle Scholar
Thompson, JD, Higgins, DG and Gibson, TJ (1994) CLUSTAL w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Vanhove, MPM, Economou, AN, Zogaris, S, Giakoumi, S, Zanella, D, Volckaert, FAM and Huyse, T (2013) The Gyrodactylus (Monogenea, Gyrodactylidae) parasite fauna of freshwater sand gobies (Teleostei, Gobioidei) in their centre of endemism, with description of seven new species. Parasitology Research 113, 653–668.CrossRefGoogle ScholarPubMed
Xavier, R, Faria, PJ, Paladini, G, van Oosterhout, C, Johnson, M and Cable, J (2015) Evidence for cryptic speciation in directly transmitted gyrodactylid parasites of Trinidadian guppies. PLoS One 10(1), e0117096.CrossRefGoogle ScholarPubMed
Zhukov, EV (1960) [Parasitic fauna of fishes of chukotka. I. Monogenetic Trematoda of marine and freshwater fishes]. Parazitologicheskij Sbornik 19, 308–332 (in Russian).Google Scholar
Ziętara, MS and Lumme, J (2003) The crossroads of molecular, typological and biological species concepts: two new species of Gyrodactylus Nordmann, 1832 (Monogenea: Gyrodactylidae). Systematic Parasitology 55, 39–52.CrossRefGoogle Scholar
Ziętara, MS, Arndt, A, Geets, A, Hellemans, B and Volckaert, FAM (2000) The nuclear rDNA region of Gyrodactylus arcuatus and G. Branchicus (Monogenea: Gyrodactylidae). Journal of Parasitology 86, 1368–1373.CrossRefGoogle Scholar
Ziętara, MS, Huyse, T, Lumme, J and Volckaert, FA (2002) Deep divergence among subgenera of gyrodactylus inferred from rDNA ITS region. Parasitology 124, 39–52.CrossRefGoogle ScholarPubMed
Ziętara, MS, Lebedeva, D, Muñoz, G and Lumme, J (2012) A monogenean fish parasite, Gyrodactylus chileani n. sp., belonging to a novel marine species lineage found in the South-eastern Pacific and the Mediterranean and North Seas. Systematic Parasitology 83, 59–67.CrossRefGoogle Scholar
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