A parasitological investigation of Cyprinella venusta and Notropis cf. stramineus sampled in Texas, USA, in the Guadalupe River, revealed the presence of Gyrodactylus crysoleucas Mizelle and Kritsky, 1967 on C. venusta, and Gyrodactylus mediotorus King, Marcogliese, Forest, McLaughlin & Bentzen, 2013 on both fish species. This represents new leuscicid fish hosts and locality records for these two gyrodactylids. Gyrodactylus crysoleucas previously identified from both non-native Californian Notemigonus crysoleucas and from farmed stocks in Minnesota demonstrated intraspecific variability in terms of morphology and genetics as a local adaptation associated with isolation by distance. Results further confirmed G. crysoleucas as alien in the western USA and suggested host-switching involving C. venusta and N. crysoleucas. Conservative morphology and genetics on the part of G. mediotorus from C. venusta and N. cf. stramineus (Guadalupe River) was observed, while higher genetic divergence in the ITS sequences associated with morphological discrepancy was found between the studied G. mediotorus specimens and those of Notropis hudsonius than when considering the parasites of Notropis texanus. The separation of G. mediotorus into geographical subgroups may indicate ongoing speciation linked to the Pleistocene glaciations in North America, and to hydrographic barriers that facilitated separate evolutionary paths leading to speciation. We suggest that deep investigations of Gyrodactylus populations will help to understand the speciation of these parasites and their adaptation to Nearctic fish hosts.

TITLE: Variation intraspécifique chez Gyrodactylus mediotorus et G. crysoleucas (Gyrodactylidae), parasites de ménés néarctiques (Leuciscidae) : preuves d’une spéciation en cours, d’un changement d’hôte et d’une translocation de parasites. ABSTRACT: Une enquête parasitologique sur Cyprinella venusta et Notropis cf. stramineus échantillonnés au Texas, États-Unis, dans la rivière Guadalupe, a révélé la présence de Gyrodactylus crysoleucas Mizelle et Kritsky, 1967 sur C. venusta, et de Gyrodactylus mediotorus King, Marcogliese, Forest, McLaughlin & Bentzen, 2013 sur les deux espèces de poissons. Ceci représente de nouveaux poissons Leuciscidae hôtes et des nouvelles localités pour ces deux Gyrodactylidae. Gyrodactylus crysoleucas, identifié précédemment à partir de Notemigonus crysoleucas californiens non indigènes et de stocks d’élevage du Minnesota a démontré une variabilité intraspécifique en termes de morphologie et de génétique en tant qu’adaptation locale associée à l’isolement par la distance. Les résultats ont en outre confirmé que G. crysoleucas était exotique dans l’ouest des États-Unis et ont suggéré un changement d’hôte impliquant C. venusta et N. crysoleucas. Une morphologie et une génétique conservatrices pour G. mediotorus de C. venusta et N. cf. stramineus (rivière Guadalupe) ont été observées, tandis qu’une divergence génétique plus élevée dans les séquences ITS, associée à une divergence morphologique, a été trouvée chez les spécimens étudiés de G. mediotorus et de Notropis hudsonius lorsque l’on considère les parasites de Notropis texanus. La séparation de G. mediotorus en sous-groupes géographiques peut indiquer une spéciation continue liée aux glaciations du Pléistocène en Amérique du Nord et à des barrières hydrographiques qui ont facilité des chemins évolutifs séparés menant à la spéciation. Nous suggérons que des études approfondies sur les populations de Gyrodactylus aideront à comprendre la spéciation de ces parasites et leur adaptation aux poissons hôtes néarctiques.

Department of Botany and Zoology Faculty of Science Masaryk University Kotlářská 2 611 37 Brno Czech Republic

Texas Parks and Wildlife Department 5103 Junction Highway Mountain Home TX 78058 USA

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Bakke TA, Cable J, Harris PD. 2007. The biology of gyrodactylid monogeneans: the “Russian-doll killers”. Advances in Parasitology, 64, 161–376. PubMed

Bakke TA, Harris PD, Cable J. 2002. Host specificity dynamics: observations on gyrodactylid monogeneans. International Journal for Parasitology, 32, 281–308. PubMed

Boeger WA, Kritsky DC, Pie MR. 2003. Context of diversification of the viviparous Gyrodactylidae (Platyhelminthes, Monogenoidea). Zoologica Scripta, 32, 437–448. PubMed PMC

Boeger WA, Kritsky DC, Pie MR, Engers KB. 2005. Mode of transmission, host switching, and escape from the Red Queen by viviparous gyrodactylids (Monogenoidea). Journal of Parasitology, 91, 1000–1007. PubMed

Brooks DR, McLennan DA. 1993. Comparative study of adaptive radiations with an example using parasitic flatworms (Platyhelminthes: Cercomeria). American Naturalist, 142, 755–778. PubMed

Brooks DR. 1979. Testing the context and extent of host-parasite coevolution. Systematic Zoology, 28, 299–307.

Bueno-Silva M, Boeger WA, Pie MR. 2011. Choice matters: incipient speciation in Gyrodactylus corydori (Monogenoidea: Gyrodactylidae). International Journal for Parasitology, 41, 657–667. PubMed

Bush AO, Lafferty KD, Lotz JM, Shostak AW. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 575–583. PubMed

Cable J, Harris PD. 2002. Gyrodactylid developmental biology: historical review, current status and future trends. International Journal for Parasitology, 32, 255–280. PubMed

Cable J, Harris PD, Tinsley RC, Lazarus CM. 2011. Phylogenetic analysis of Gyrodactylus spp. (Platyhelminthes: Monogenea) using ribosomal DNA sequences. Canadian Journal of Zoology, 77, 1439–1449.

Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. 2009. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics, 25, 1972–1973. PubMed PMC

Cone DK, Cusack R. 1988. A study of Gyrodactylus colemanensis Mizelle and Kritsky, 1967 and Gyrodactylus salmonis (Yin and Sproston, 1948) (Monogenea) parasitizing captive salmonids in Nova Scotia. Canadian Journal of Zoology, 66, 409–415.

Cone D, Abbott C, Gilmore S, Burt M. 2010. A new genus and species of gyrodactylid (Monogenea) from silver hake, Merluccius bilinearis, in the bay of fundy, New Brunswick, Canada. Journal of Parasitology, 96, 681–684. PubMed

Cone DK, Cusack R. 1989. Infrapopulation Dispersal of Gyrodactylus colemanensis (Monogenea) on Fry of Salmo gairdneri. Journal of Parasitology, 75, 702–706. PubMed

Cribb TH, Chisholm LA, Bray RA. 2002. Diversity in the Monogenea and Digenea: does lifestyle matter? International Journal for Parasitology, 32, 321–328. PubMed

Cunningham CO, McGillivray DM, MacKenzie K, Melvin WT. 1995. Discrimination between Gyrodactylus salaris, G. derjavini and G. truttae (Platyhelminthes: Monogenea) using restriction fragment length polymorphisms and an oligonucleotide probe within the small subunit ribosomal RNA gene. Parasitology, 111, 87–94. PubMed

Cunningham CO. 1997. Species variation within the internal transcribed spacer (ITS) region of Gyrodactylus (Monogenea:Gyrodactylidae) ribosomal RNA genes. Journal of Parasitology, 83, 215–219. PubMed

Cusack R. 1986. Development of infections of Gyrodactylus colemanensis Mizelle and Kritsky, 1967 (Monogenea) and the effect on fry of Salmo gairdneri Richardson. Journal of Parasitology, 72, 663–668. PubMed

Dávidová M, Jarkovský J, Matějusová I, Gelnar M. 2005. Seasonal occurrence and metrical variability of Gyrodactylus rhodei Žitňan 1964 (Monogenea, Gyrodactylidae). Parasitology Research, 95, 398–405. PubMed

Dechtiar AO. 1972. New parasite records for Lake Erie fish. Technical Report 17, Ann Arbor, Michigan: Great Lakes Fishery Commission, 20 p.

Dechtiar AO, Collins JJ, Reckahn JA. 1988. Survey of the parasite fauna of Lake Ontario fishes, 1961 to 1971. Great Lakes Fishery Commission, Technical Report, 51, 19–48.

Dechtiar AO, Collins JJ, Reckhan JA. 1988. Survey of the parasite fauna of Lake Huron fishes, 1961 to 1971. Parasites of fishes in the Canadian waters of the Great Lakes, Technical Report 51, Nepszy SJ, Editor. Great Lakes Fishery Commission: Ann Arbor, Michigan. p. 19–48.

Dechtiar AO, Maclean JA, Nepszy SJ. 1989. Parasites of fishes from Algonquin Park lakes. Ontario Fisheries Technical Report Series, 29, 19.

Dechtiar AO, Nepszy SJ. 1988. Survey of the parasite fauna of selected fish species from Lake Erie, 1970–1975, in Parasites of fishes in the Canadian waters of the Great Lakes, Technical Report 51. Nepszy SJ, Editor. Great Lakes Fishery Commission: Ann Arbor, Michigan. p. 49–65.

Desdevises Y, Morand S, Jousson O, Legendre P. 2002. Coevolution between Lamellodiscus (Monogenea: Diplectanidae) and Sparidae (Teleostei): the study of a complex host-parasite system. Evolution, 56, 2459–2471. PubMed

Dill WA, Cordone AJ. 1997. History and Status of Introduced Fishes in California, 1871–1996, Bulletin 178. California Department of Fish and Game.

Dove ADM, Ernst I. 1998. Concurrent invaders – four exotic species of Monogenea now established on exotic freshwater fishes in Australia. International Journal for Parasitology, 28, 1755–1764. PubMed

Fildani A, Hessler AM, Mason CC, McKay MP, Stockli DF. 2018. Late Pleistocene glacial transitions in North America altered major river drainages, as revealed by deep-sea sediment. Scientific Reports, 8, 13839. PubMed PMC

Fricke R, Eschmeyer W, Fong JD. 2023. Catalogue of fishes: genera, species. Available at http://researcharchive.calacademy.org/research/ichthyology/catalog/speciesbyfamily.asp.

Froese R, Pauly D. 2023. FishBase. World Wide Web electronic publication. https://www.fishbase.org (access date: 10/10/2023).

García-Vásquez A, Hansen H, Christison KW, Bron JE, Shinn AP. 2011. Description of three new species of Gyrodactylus von Nordmann, 1832 (Monogenea) parasitising Oreochromis niloticus niloticus (L.) and O. mossambicus (Peters) (Cichlidae). Acta Parasitologica, 56, 20–30.

Gidmark NJ, Simons AM. 2014. Cyprinidae, in Freshwater fishes of North America: Carps and Minnows. Warren MLJ, Buur BM, Editors. Johns Hopk: Baltimore. p. 334–450.

Gilmore SR, Cone DK, Lowe G, King SK, Jones SRM, Abbott CL. 2012. Molecular phylogeny of Gyrodactylus (Monogenea) parasitizing fishes in fresh water, estuarine, and marine habitats in Canada. Canadian Journal of Zoology, 90, 776–786.

Glennon V, Perkins EM, Chisholm LA, Whittington ID. 2008. Comparative phylogeography reveals host generalists, specialists and cryptic diversity: hexabothriid, microbothriid and monocotylid monogeneans from rhinobatid rays in southern Australia. International Journal for Parasitology, 38, 1599–1612. PubMed

Hanek G, Fernando CH. 1971. Monogenetic trematodes from the Bay of Quinte area, Ontario. II. Genus Gyrodactylus Nordmann, 1832. Canadian Journal of Zoology, 49, 1331–1341. PubMed

Harris PD, Shinn AP, Cable J, 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. PubMed

Hathaway RP, Herlevich JC. 1973. Gyrodactylus stableri sp. n., with new host and locality records for species of Gyrodactylus. Journal of Parasitology, 59, 801–802.

Hewitt G. 2000. The genetic legacy of the Quaternary ice ages. Nature, 405, 907–913. PubMed

Hubbs C, Edwards R, Garrett G. 1991. An annotated checklist of the freshwater fishes of Texas, with keys to identification of species, 2nd edn. Texas Journal of Science, 43.

Hurvich CM, Tsai CL. 1989. Regression and time series model selection in small samples. Biometrika, 76, 297–307.

Huyse T, Audenaert V, Volckaert FAM. 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. PubMed

Huyse T, Volckaert FAM. 2002. Identification of a host-associated species complex using molecular and morphometric analyses, with the description of Gyrodactylus rugiensoides n. sp. (Gyrodactylidae, Monogenea). International Journal for Parasitology, 15, 907–919. PubMed

Jogunoori W, Kritsky DC, Venkatanarasaiah J. 2004. Neotropical Monogenoidea. 46. Three new species from the gills of introduced aquarium fishes in India, the proposal of Heterotylus n. g. and Diaphorocleidus n. g., and the reassignment of some previously described species of Urocleidoides Mizelle & Price. Systematic Parasitology, 58, 115–124. PubMed

Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. PubMed PMC

Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. PubMed PMC

Kearn GC. 1994. Evolutionary expansion of the Monogenea. International Journal for Parasitology, 24, 1227–1271. PubMed

Kim J-H, Hayward CJ, Joh S-J, Heo G-J. 2002. Parasitic infections in live freshwater tropical fishes imported to Korea. Diseases of Aquatic Organisms, 52, 169–173. PubMed

King S, Marcogliese D, Forest J, McLaughlin J, Bentzen P. 2013. Description of Gyrodactylus mediotorus n. sp. (Monogenea: Gyrodactylidae) infecting spottail shiner (Notropis hudsonius) from the St. Lawrence River. Canada. Journal of Parasitology, 99, 1062–1066. PubMed

Kirby JM. 1981. Seasonal occurrence of the ectoparasite Gyrodactylus atratuli on spotfin shiners. Transactions of the American Fisheries Society, 110, 462–464.

Kritsky DC, Thatcher VE. 1977. Phanerothecium gen. nov. and Fundulotrema gen. nov, two new genera of viviparous monogenoidea (Gyrodactylidae) with a description of P. caballeroi and a key to the subfamilies and genera of the family. Exerta Parasitologica En Memoria Del Doctor Eduardo Caballero y Caballero, Instituto de Biologie (Mexico). Publicaciones Especiales, 4, 53–60.

Kritsky DC, Boeger WA. 2003. Phylogeny of the gyrodactylidae and the phylogenetic status of Gyrodactylus Nordmann, 1832 (Platyhelminthes: Monogenoidea), in Livre Hommage à Louis Euzet, tome 2. Combes C, Jourdane J, Editors. PUP: Perpignan, France. p. 37–58.

Kritsky DC, Mizelle JD. 1968. Studies on monogenetic trematodes. XXXV. Some new and previously described North American species of Gyrodactylus. American Midland Naturalist, 79, 205–215.

Kritsky DC. 2007. Heteropriapulus nom. nov. (Monogenoidea: Dactylogyridae) for Heterotylus Jogunoori, Kritsky & Venkatanarasaiah, 2004, a junior homonym of Heterotylus Kirsch in Reitter, 1913 (Coleoptera: Curculionidae). Systematic Parasitology, 68, 233. PubMed

Krueger RF. 1954. A survey of the helminth parasites of fishes from Van Buren Lake and Rocky Ford Creek. Ohio Journal of Science, 54, 277–279.

Leis E, King S, Leis S, Cone D. 2016. Infections of Gyrodactylus crysoleucas and Gyrodactylus sp. (Monogenea) at a golden shiner (Notemigonus crysoleucas) farm in Minnesota. Comparative Parasitology, 83, 105–110.

Leis E, Easy R, Cone D. 2021. A variant of Gyrodactylus mediotorus King, Marcogliese, Forest, McLaughlin and Bentzen, 2013 (Monogenea) identified from weed shiner (Notropis texanus) in Wisconsin portions of the upper Mississippi River. Systematic Parasitology, 98, 247–253. PubMed

Machordom A, 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. On the occurrence of Gyrodactylus on Swedish fishes. Skrifter Utgivna Av Södra Sveriges Fiskeriföreningen, 1956, 19–76. [in Swedish].

Malmberg G. 1970. The excretory systems and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, Monogenea). Arkiv för Zoologi, 23, 1–237.

Matějusova I, Gelnar M, McBeath AJ, Collins CM, Cunningham CO. 2001. Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). International Journal for Parasitology, 31, 738–745. PubMed

Mayden RL. 1989. Phylogenetic studies of North American minnows: with emphasis on the genus Cyprinella (Teleostei, Cypriniformes), Miscellaneous publication, No. 80. University of Kansas, Museum of Natural History.

Mayes MA. 1977. New species of Gyrodactylus and Dactylogyrus (Trematoda: Monogenea) from fishes of Nebraska. Journal of Parasitology, 63, 805–809. PubMed

Meinilä M, Kuusela J, Ziȩtara MS, Lumme J. 2004. Initial steps of speciation by geographic isolation and host switch in salmonid pathogen Gyrodactylus salaris (Monogenea: Gyrodactylidae). International Journal for Parasitology, 34, 515–526. PubMed

Minh BQ, Nguyen MAT, Von Haeseler A. 2013. Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution, 30, 1188–1195. PubMed PMC

Mizelle JD, Kritsky DC. 1967. Studies on monogenetic trematodes. XXXIII. New species of Gyrodactylus and a key to the North American species. Transactions of the American Microscopical Society, 86, 390–401.

Mo TA. 1997. Seasonal occurrence of Gyrodactylus derjavini (Monogenea) on brown trout, Salmo trutta, and Atlantic salmon, S. salar, in the Sandvikselva river, Norway. Journal of Parasitology, 83, 1025–1029. PubMed

Moyle PB. 1976. Fish introductions in California: history and impact on native fishes. Biological Conservation, 9, 101–118.

Mueller JF. 1936. Studies on North American gyrodactyloidea. Transactions of the American Microscopical Society, 55, 55–72.

Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274. PubMed PMC

Nico L, Fuller P. 2023. Cyprinella venusta Girard, 1856: U.S, Geological Survey. Gainesville, FL: Nonindigenous Aquatic Species Database. Available at https://nas.er.usgs.gov/queries/FactSheet.aspx?speciesID=521 (access date: 11/01/2023).

Nico L, Neilson ME. 2023. Notemigonus crysoleucas (Mitchill, 1814): U.S. Geological Survey. Gainesville, FL: Nonindigenous Aquatic Species Database. Available at https://nas.er.usgs.gov/queries/factsheet.aspx?SpeciesID=579 (access date: 10/01/2023).

Ondračková M. 2016. Gyrodactylus proterorhini in its non-native range: distribution and ability to host-switch in freshwaters. Parasitology Research, 115, 3153–3162. PubMed

Ondračková M, Seifertová M, Bryjová A, Leis E, Jurajda P. 2020. Morphometric and genetic evidence for cryptic diversity in Gyrodactylus (Monogenea) infecting non-native European populations of Ameiurus nebulosus and A. melas. Parasitology, 147, 1700–1711. PubMed PMC

Page LM, Burr BM. 2011. Peterson field guide to freshwater fishes of North America North of Mexico, 2nd edn. USA: Houghton Mifflin Harcourt.

Pinacho-Pinacho CD, Calixto-Rojas M, García-Vásquez A, Guzmán-Valdivieso I, Barrios-Gutiérrez JJ, Rubio-Godoy M. 2021. Species delimitation of Gyrodactylus (Monogenea: Gyrodactylidae) infecting the southernmost cyprinids (Actinopterygii: Cyprinidae) in the New World. Parasitology Research, 120, 831–848. PubMed

Price CE, McMahon TE. 1967. The monogenetic trematodes of North American freshwater fishes. Rivista di Parassitologia, 28, 177–220. PubMed

Pugachev ON. 1980. Parasite fauna of the sucker (Catostomus catostomus) from the Kolyma river. Parasitologiya, 14, 511–513.

Pugachev ON, Gerasev PI, Gussev AV, Ergens R, Khotenowsky I. 2010. Guide to Monogenoidea of freshwater fish of Palaearctic and Amur regions. Milan, Italy: Ledizioni LediPublishing.

Putz RE, Hoffman GL. 1963. Two new Gyrodactylus (Trematoda: Monogenea) from cyprinid fishes with synopsis of those found on North American fishes. Journal of Parasitology, 49, 559–566. PubMed

De Queiroz K. 2007. Species concepts and species delimitation. Systematic Biology, 56, 879–886. PubMed

Rahmouni C, Seifertová M, Simková A. 2023. Diversity and phylogeny of Gyrodactylus spp. (Monogenea: Gyrodactylidae) across the Strait of Gibraltar: parasite speciation and historical biogeography of West Mediterranean cyprinid hosts. Diversity, 15, 1152.

Rahmouni C, Seifertová M, Simková A. 2023. Revealing the hidden diversity of Gyrodactylus communities (Monogenea: Gyrodactylidae) from Nearctic Catostomidae and Leuciscidae fish hosts (Teleostei: Cypriniformes), with description of ten new species. Parasite, 30, 40. PubMed PMC

Rahmouni I, Řehulková E, Pariselle A, Rkhami OB, Šimková A. 2017. Four new species of Dactylogyrus Diesing, 1850 (Monogenea: Dactylogyridae) parasitising the gills of northern Moroccan Luciobarbus Heckel (Cyprinidae): morphological and molecular characterisation. Systematic Parasitology, 94, 575–591. PubMed

Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67, 901–904. PubMed PMC

Řehulková E, Seifertová M, Přikrylová I, Francová K. 2018. Monogenea, in A guide to the parasites of African freshwater fishes. Scholz T, Vanhove MPM, Smit N, Jayasundera Z, Gelnar M, Editors. AbcTaxa: Brussels, Belgium. p. 185–243.

Rogers WA. 1968. Eight new species of Gyrodactylus (Monogenea) from the southeastern U.S. with redescriptions of G. fairporti Van Cleave, 1921, and G. cyprini Diarova, 1964. Journal of Parasitology, 54, 490–495.

Rogers WA. 1967. Six new species of Gyrodactylus (Monogenea) from the southeastern US. Journal of Parasitology, 53, 747–751. PubMed

Rogers WA. 1975. Four new species of Gyrodactylus from fishes of Alabama. Journal of Parasitology, 61, 51–53. PubMed

Rogers WA, Wellborn TL. 1965. Studies on Gyrodactylus (Trematoda: Monogenea) with descriptions of five new species from the southeastern US. Journal of Parasitology, 51, 977–982. PubMed

Rokicka M, Lumme J, Ziętara MS. 2007. Identification of Gyrodactylus ectoparasites in Polish salmonid farms by PCR-RFLP of the nuclear ITS segment of ribosomal DNA (Monogenea, Gyrodactylidae). Acta Parasitologica, 52, 185–195.

Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. Mrbayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542. PubMed PMC

Rubio-Godoy M, Paladini G, Freeman MA, García-Vásquez A, Shinn AP. 2012. Morphological and molecular characterisation of Gyrodactylus salmonis (Platyhelminthes, Monogenea) isolates collected in Mexico from rainbow trout (Oncorhynchus mykiss Walbaum). Veterinary Parasitology, 186, 289–300. PubMed

Schönhuth S, Vukić J, Šanda R, Yang L, Mayden RL. 2018. Phylogenetic relationships and classification of the Holarctic family Leuciscidae (Cypriniformes: Cyprinoidei). Molecular Phylogenetics and Evolution, 127, 781–799. PubMed

Shapiro BJ, Leducq J-B, Mallet J. 2016. What is speciation? PLoS Genetics, 12. PubMed PMC

Šimková A, Verneau O, Gelnar M, Morand S. 2006. Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish. Evolution, 60, 1023–1037. PubMed

Stout C, Schonhuth S, Mayden R, Garrison NL, Armbruster JW. 2022. Phylogenomics and classification of Notropis and related shiners (Cypriniformes: Leuciscidae) and the utility of exon capture on lower taxonomic groups. PeerJ, 10. PubMed PMC

Sugiura N. 1978. Further analysis of the data by Anaike’ s information criterion and the finite corrections. Communications in Statistics – Theory and Methods, 7, 13–26.

Swift CC, Haglund TR, Ruiz M, Fisher RN. 1993. The status and distribution of the freshwater fishes of southern California. Bulletin of the Southern California Academy of Sciences, 92, 101–167.

Tamura K, Stecher G, Kumar S. 2021. MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38, 3022–3027. PubMed PMC

Tan M, Armbruster JW. 2018. Phylogenetic classification of extant genera of fishes of the order Cypriniformes (Teleostei: Ostariophysi). Zootaxa, 4476, 6–39. PubMed

Thompson JD, Higgins DG, 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. PubMed PMC

Threlfall W. 1974. New and previously described species of monogenetic trematodes from Labrador catostomids and cyprinids. Folia Parasitologica, 21, 205–214. PubMed

Wellborn TL, Rogers WA. 1967. Five new species of Gyrodactylus (Trematoda: Monogenea) from the southeastern US. Journal of Parasitology, 53, 10–14. PubMed

Wells PR, Cone DK. 1990. Experimental studies on the effect of Gyrodactylus colemanensis and G. salmonis (Monogenea) on density of mucous cells in the epidermis of fry of Oncorhynchus mykiss. Journal of Fish Biology, 37, 599–603.

Whittington ID, Cribb BW, Hamwood TE, Halliday JA. 2000. Host-specificity of monogenean (Platyhelminth) parasites: a role for anterior adhesive areas? International Journal for Parasitology, 30, 305–320. PubMed

Whittington ID, Kearn GC. 2011. Hatching strategies in monogenean (Platyhelminth) parasites that facilitate host infection. Integrative and Comparative Biology, 51, 91–99. PubMed

Xavier R, Faria PJ, Paladini G, van Oosterhout C, Johnson M, Cable J. 2015. Evidence for cryptic speciation in directly transmitted gyrodactylid parasites of Trinidadian guppies. PLoS One, 10, e0117096. PubMed PMC

Xiang C-Y, Gao F, Jakovlić I, Lei H-P, Hu Y, Zhang H, Zou H, Wang G-T, Zhang D. 2023. Using PhyloSuite for molecular phylogeny and tree-based analyses. IMeta, 2, e87.

You P, MacMillan J, Cone D. 2011. Local patchiness of Gyrodactylus colemanensis and G. salmonis parasitizing salmonids in the South River watershed, Nova Scotia, Canada. Diseases of Aquatic Organisms, 96, 137–143. PubMed

Zhang D, Gao F, Jakovlić I, Zou H, Zhang J, Li WX, Wang GT. 2020. PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources, 20, 348–355. PubMed

Ziȩtara MS, 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. PubMed

Ziętara MS, Lumme J. 2002. Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea, Gyrodactylidae). Evolution, 56, 2445–2458. PubMed

Ziętara M, Lumme J. 2004. Comparison of molecular phylogeny and morphological systematics in fish parasite genus Gyrodactylus Nordmann, 1832 (Monogenea, Gyrodactylidae). Zoologica Poloniae, 49, 5–28.