Host-specific parasites exhibit close co-evolutionary associations with their hosts. In the case of fragmented/disjunct host distribution, host-specific parasites may reflect the biogeographical history of regions and/or the role played by contacts of hosts. The present study was focused on Dactylogyrus (Monogenea) species almost exclusively parasitizing cyprinoid fishes. We investigated the phylogenetic relationships between Dactylogyrus parasites of Nearctic cyprinoids (Leuciscidae) and Dactylogyrus parasites of Palearctic cyprinoids and used Dactylogyrus phylogeny to explore the biogeography of fish hosts in Europe and North America. Phylogenetic analyses revealed that two Nearctic clades of Dactylogyrus spp. have different origins. Historical contacts between European and North American leuciscids were accompanied by the host switching of Dactylogyrus species. In the Nearctic region, Dactylogyrus parasites also colonized non-leuciscid fishes. Dactylogyrus spp. of three Nearctic leuciscid clades were included in the phylogenetic reconstruction; only Dactylogyrus spp. of the Plagopterinae had a common origin. Dactylogyrus species did not reflect the phylogenetic relationships among leuciscid clades, suggesting that past co-diversification was overshadowed by colonization events mediated by paleogeographic and climatological changes and extensive drainage reorganization. Host-specific monogeneans serve as a supplementary tool to reveal the historical biogeographical contacts between freshwater fish from the North America and Europe and also contemporary contacts of leuciscids in North America.

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

Division of Natural Sciences St Norbert College De Pere WI 54115 USA

Zobrazit více v PubMed

Brooks D.R., Hoberg E.P. Triage for the biosphere: The need and rationale for taxonomic inventories and phylogenetic studies and parasites. Comp. Parasitol. 2000;67:1–25.

Hoberg E.P., Klassen G.J. Revealing the faunal tapestry: Co-evolution and historical biogeography of hosts and parasites in marine systems. Parasitology. 2002;124:S3–S22. doi: 10.1017/S0031182002001841. PubMed DOI

Brooks D.R., McLennan D.A. Parascript: Parasites and the Language of Evolution. Smithsonian Institution Press; Washington, DC, USA: 1993.

Brooks D.R., McLennan D.A. The Nature of Diversity: An Evolutionary Voyage of Discovery. University of Chicago Press; Chicago, IL, USA: 2002.

Řehulková E., Seifertová M., Přikrylová I., Francová K. Monogenea. In: Scholz T., Vanhove M.P.M., Smit N., Jayasundera Z., Gelnar M., editors. A Guide to the Parasites of African Freshwater Fishes. AbcTaxa; Brussels, Belgium: 2018. pp. 185–243.

Rohde K. A non-competitive mechanism responsible for restricting niches. Zool. Anz. 1977;199:164–172.

Rohde K. Simple ecological systems, simple solution to complex problems? Evol. Theor. 1989;8:305–350.

Euzet L., Combes C. The selection of habitats among the monogenea. Int. J. Parasitol. 1998;28:1645–1652. doi: 10.1016/S0020-7519(98)00062-9. PubMed DOI

Šimková A., Ondračková M., Gelnar M., Morand S. Morphology and coexistence of congeneric ectoparasite species: Reinforcement of reproductive isolation? Biol. J. Linn. Soc. 2002;76:125–135. doi: 10.1111/j.1095-8312.2002.tb01719.x. DOI

Šimková A., Verneau O., Gelnar M., Morand S. Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish. Evolution. 2006;60:1023–1037. doi: 10.1111/j.0014-3820.2006.tb01180.x. PubMed DOI

Pariselle A., Boeger W.A., Snoeks J., Bilong Bilong C.F., Morand S., Vanhove M.P.M. The monogenean parasite fauna of cichlids: A potential tool for host biogeography. Int. J. Evol. Biol. 2011;2011:471480. doi: 10.4061/2011/471480. PubMed DOI PMC

Benovics M., Desdevises Y., Vukić J., Šanda R., Šimková A. The phylogenetic relationships and species richness of host-specific Dactylogyrus parasites shaped by the biogeography of Balkan cyprinids. Sci. Rep. 2018;8:13006. doi: 10.1038/s41598-018-31382-w. PubMed DOI PMC

Benovics M., Vukić J., Šanda R., Rahmouni I., Šimková A. Disentangling the evolutionary history of peri-Mediterranean cyprinids using host-specific gill monogeneans. Int. J. Parasitol. 2020;50:969–984. doi: 10.1016/j.ijpara.2020.05.007. PubMed DOI

Benovics M., Desdevises Y., Šanda R., Vukić J., Scheifler M., Doadrio I., Sousa-Santos C., Šimková A. High diversity of fish ectoparasitic monogeneans (Dactylogyrus) in the Iberian Peninsula: A case of adaptive radiation? Parasitology. 2000;147:418–430. doi: 10.1017/S0031182020000050. PubMed DOI PMC

Šimková A., Benovics M., Rahmouni I., Vukić J. Host-specific Dactylogyrus parasites revealing new insights on the historical biogeography of Northwest African and Iberian cyprinid fish. Parasit. Vectors. 2017;10:589. doi: 10.1186/s13071-017-2521-x. PubMed DOI PMC

Winfield I.J., Nelson J.S. Cyprinid Fishes: Systematics, Biology and Exploitation. Chapman and Hall; London, UK: 1991. (Fish and Fisheries Series No. 3).

Gibson D.I., Timofeeva T.A., Gerasev P.I. A catalogue of the nominal species of the monogenean genus Dactylogyrus Diesing, 1850 and their host genera. Syst. Parasitol. 1996;35:3–48. doi: 10.1007/BF00012180. DOI

Šimková A., Morand S., Jobet E., Gelnar M., Verneau O. Molecular phylogeny of congeneric monogenean parasites (Dactylogyrus): A case of intrahost speciation. Evolution. 2004;58:1001–1018. doi: 10.1111/j.0014-3820.2004.tb00434.x. PubMed DOI

Benovics M., Kičinjaová M.L., Šimková A. The phylogenetic position of the enigmatic Balkan Aulopyge huegelii (Teleostei: Cyprinidae) from the perspective of host specific Dactylogyrus parasites (Monogenea), with a description of Dactylogyrus omenti n. sp. Parasit. Vectors. 2017;10:547. doi: 10.1186/s13071-017-2491-z. PubMed DOI PMC

Kuchta R., Řehulková E., Francová K., Scholz T., Morand S., Šimková A. Diversity of monogeneans and tapeworms in cypriniform fishes across two continents. Int. J. Parasitol. 2020;50:771–786. doi: 10.1016/j.ijpara.2020.06.005. PubMed DOI

Schönhuth S., Vukić J., Šanda R., Yang L., Mayden R.L. Phylogenetic relationships and classification of the Holarctic family Leuciscidae (Cypriniformes: Cyprinoidei) Mol. Phyl. Evol. 2018;127:781–799. doi: 10.1016/j.ympev.2018.06.026. PubMed DOI

Imoto J.M., Saitoh K., Sasaki T., Yonezawa T., Adachi J., Kartavtsev Y.P., Miya M., Nishida M., Hanzawa N. Phylogeny and biogeography of highly diverged freshwater fish species (Leuciscinae, Cyprinidae, Teleostei) inferred from mitochondrial genome analysis. Gene. 2013;514:112–124. doi: 10.1016/j.gene.2012.10.019. PubMed DOI

Banarescu P. Some reconsiderations of the zoogeography of the euro-Mediterranean freshwater fish fauna. Rev. Romane Biol. Zool. 1973;8:257–264.

Doadrio I. Phylogenetic relationships and classification of western Palearctic species of the genus Barbus (Osteichthyes, Cyprinidae) Aquat. Living Resour. 1990;3:265–282. doi: 10.1051/alr:1990028. DOI

Benovics M., Nejat F., Abdoli A., Šimková A. Molecular and morphological phylogeny of host-specific Dactylogyrus parasites (Monogenea) sheds new light on the puzzling Middle Eastern origin of European and African lineages. Parasit. Vectors. 2021;14:372. doi: 10.1186/s13071-021-04863-7. PubMed DOI PMC

Mizelle J.D. Ectoparasites of the blunt-nosed minnow (Hyborhynchus notatus) Am. Midl. Nat. 1937;18:612–621. doi: 10.2307/2420654. DOI

Mizelle J.D. New species of monogenetic flukes from Illinois fishes. Am. Midl. Nat. 1938;19:465–470. doi: 10.2307/2422987. DOI

Mueller J.F. Additional species of North American Gyrodactyloidea (Trematoda) Am. Midl. Nat. 1938;19:220–235. doi: 10.2307/2420432. DOI

Seamster A. Two new Dactylogyridae (Trematoda: Monogenea) from the golden shiner. J. Parasitol. 1948;34:111–113. doi: 10.2307/3273403. PubMed DOI

Mizelle J.D., Klucka A.R. Studies on monogenetic trematodes XIV. Dactylogyridae from Wisconsin fishes. Am. Midl. Nat. 1953;49:720–733. doi: 10.2307/2485203. DOI

Monaco L.H., Mizelle J.D. Studies on monogenetic trematodes XVII. The genus Dactylogyrus. Am. Midl. Nat. 1955;53:455–477. doi: 10.2307/2422083. DOI

Wood R.A., Mizelle J.D. Studies on monogenetic trematodes. XXI. North American Gyrodactylinae, Dactylogyrinae and a new host record for Urocleidus dispar (Mueller, 1936) Am. Midl. Nat. 1957;57:183–202. doi: 10.2307/2422530. DOI

Rogers W.A. Studies on Dactylogyrinae (Monogenea) with descriptions of 24 new species of Dactylogyrus, 5 new species of Pellucidhaptor, and the proposal of Aplodiscus gen. n. J. Parasitol. 1967;53:501–524. doi: 10.2307/3276709. PubMed DOI

Chien S.-M. Dactylogyrids from North American cyprinids of the genus Nocomis. The reciprocus species group. J. Parasitol. 1971;57:1211–1214. doi: 10.2307/3277968. PubMed DOI

Chien S.-M. Dactylogyrids from North American cyprinids of the genus Nocomis: The bellicus group. J. Parasitol. 1974;60:585–594. doi: 10.2307/3278712. PubMed DOI

Chien S.-M. Dactylogyrids from North American cyprinids of the genus Nocomis: The Limulus and the Mollis groups. J. Parasitol. 1974;60:773–776. doi: 10.2307/3278898. PubMed DOI

Hanek G., Molnár K., Fernando C.H. New and previously known Dactylogyrus spp. from southern Ontario fishes. J. Parasitol. 1975;61:421–426. doi: 10.2307/3279317. DOI

Mayes M.A. New species of Gyrodactylus and Dactylogyrus (Trematoda: Monogenea) from fishes of Nebraska. J. Parasitol. 1977;63:805–809. doi: 10.2307/3279882. PubMed DOI

Cloutman D.G. Dactylogyrus boopsi sp. n. (Monogenea: Dactylogyridae) from the bigeye shiner, Notropis boops Gilbert (Pisces: Cyprinidae) J. Helminthol. Soc. Washingt. 1994;61:219–220.

Cloutman D.G., Rogers W.A. Determination of the Dactylogyrus banghami complex (Monogenea: Dactylogyridae) from North American Gulf of Mexico coastal drainages with descriptions of three new species. Comp. Parasitol. 2005;72:10–16. doi: 10.1654/4045. DOI

Sinnappah N.D., Lim L.H., Rohde K., Tinsley R., Combes C., Verneau O. A Paedomorphic parasite associated with a neotenic amphibian host: Phylogenetic evidence suggests a revised systematic position for Sphyranuridae within anuran and turtle Polystomatoineans. Mol. Phyl. Evol. 2001;18:189–201. doi: 10.1006/mpev.2000.0877. PubMed DOI

Hassouna N., Michot B., Bachellerie J.P. The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucleic Acids Res. 1984;12:3563–3583. doi: 10.1093/nar/12.8.3563. PubMed DOI PMC

Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol. Biol. Evol. 2018;35:1547–1549. doi: 10.1093/molbev/msy096. PubMed DOI PMC

Katoh K., Standley D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC

Talavera G., Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 2007;56:564–577. doi: 10.1080/10635150701472164. PubMed DOI

Darriba D., Taboada G.L., Doallo R., Posada D. jModelTest 2: More models, new heuristics and parallel computing. Nat. Methods. 2012;9:772. doi: 10.1038/nmeth.2109. PubMed DOI PMC

Nguyen L.T., Schmidt H.A., Von Haeseler A., Minh B.Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 2015;32:268–274. doi: 10.1093/molbev/msu300. PubMed DOI PMC

Trifinopoulos J., Nguyen L.T., von Haeseler A., Minh B.Q. W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 2016;44:W232–W235. doi: 10.1093/nar/gkw256. PubMed DOI PMC

Minh B.Q., Nguyen M.A.T., von Haeseler A. Ultrafast approximation for phylogenetic bootstrap. Mol. Biol. Evol. 2013;30:1188–1195. doi: 10.1093/molbev/mst024. PubMed DOI PMC

Ronquist F., Teslenko M., Van Der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A., Huelsenbeck J.P. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012;61:539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC

Rambaut A., Drummond A.J., Xie D., Baele G., Suchard M.A. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 2018;67:901. doi: 10.1093/sysbio/syy032. PubMed DOI PMC

Rambaut A. FigTree. 2018. [(accessed on 15 June 2021)]. Version 1.4.4. Available online: http://tree.bio.ed.ac.uk/software/figtree/

Maddison W., Maddison D. Mesquite 3.2. A Modular System for Evolutionary Analysis. 2019. [(accessed on 15 June 2021)]. Available online: http://mesquiteproject.org.

Marincovich L., Gladenkov A.Y. Evidence for an early opening of the Bering Strait. Nature. 1999;397:149–151. doi: 10.1038/16446. DOI

Marincovich L., Gladenkov A.Y. New evidence for the age of Bering Strait. Quatr. Sci. Rev. 2001;20:20,329–335. doi: 10.1016/S0277-3791(00)00113-X. DOI

McKenna M.C. Cenozoic paleontology of North Atlantic land bridges. In: Bott M.H.P., Saxov S., Talwani M., Thiede J., editors. Structure and Development of the Greenland-Scotland Bridge: New Concepts and Methods. Plenum; New York, NY, USA: 1983.

Tiffney B.H. The Eocene North Atlantic land bridge: Its importance in tertiary and modern phytogeography of the northern hemisphere. J. Arnold Arbor. 1985;66:243–273. doi: 10.5962/bhl.part.13183. DOI

Banarescu P. The zoogeographical position of the East Asian freshwater fish fauna. Rev. Roumanie Biol. Ser. Zool. 1972;17:315–323.

Briggs J.C. Ostariophysan zoogeography: An alternative hypothesis. Copeia. 1979;1:111–118. doi: 10.2307/1443735. DOI

Cavender T.M. The fossil record of the Cyprinidae. In: Winfield I.J., Nelson J.S., editors. Cyprinid Fishes, Systematics, Biology and Exploitation. Chapman and Hall; London, UK: 1991. pp. 34–54.

Harris P.M., Hubbard G., Sandel M. Catostomidae: Suckers. In: Warren M.L., Burr B.M., editors. Freshwater Fishes of North America: Volume 1: Petromyzontidae to Catostomidae. Johns Hopkins University Press; Baltimore, MD, USA: 2014. pp. 451–502.

Smith G.R. Phylogeny and biogeography of the Catostomidae, freshwater fishes of North America and Asia. In: Mayden R.L., editor. Systematics, Historical Ecology, and North American Freshwater Fishes. Stanford University Press; Stanford, CA, USA: 1992. pp. 778–813.

Bagley J.C., Mayden R.L., Harris P.M. Phylogeny and divergence times of suckers (Cypriniformes: Catostomidae) inferred from Bayesian total evidence analyses of molecules, morphology, and fossils. Peer J. 2018;6:e5168. doi: 10.7717/peerj.5168. PubMed DOI PMC

Cavender T. Review of the fossil history of North American freshwater fishes. In: Hocutt C.H., Wiley E.O., editors. The Zoogeography of North American Freshwater Fishes. John Wiley and Sons; New York, NY, USA: 1986. pp. 699–724.

Froese R., Pauly D. FishBase. World Wide Web Electronic Publication. [(accessed on 15 June 2021)]. Available online: www.fishbase.org.

Raney E.C., Lachner E.A. Age, growth, and habits of the hog sucker, Hypentelium nigricans (LeSueur) N. Y. Am. Midl. Nat. 1946;36:76–86. doi: 10.2307/2421622. DOI

Host-specific monogeneans parasitizing freshwater fish: The ecology and evolution of host-parasite associations

Uncovering the monogenean species diversity of cyprinoid fish in Iraq using an integrative approach

Nearctic Dactylogyrus species (Platyhelminthes, Monogenea) parasitizing cypriniform fishes in the context of morphology and phylogeny, with descriptions of seven new species

Dactylogyrus spp. (Dactylogyridae, Monogenea) from tinfoil barb, Barbonymus schwanenfeldii imported into South Africa: morphometric and molecular characterisation