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Host-Specific Parasites (Dactylogyrus, Monogenea) As Indicator of Evolution and Historical Dispersion of Their Cyprinid Fish Hosts in the Mediterranean Region Ph.D

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Host-Specific Parasites (Dactylogyrus, Monogenea) As Indicator of Evolution and Historical Dispersion of Their Cyprinid Fish Hosts in the Mediterranean Region Ph.D FACULTY OF SCIENCE Host-specific parasites (Dactylogyrus, Monogenea) as indicator of evolution and historical dispersion of their cyprinid fish hosts in the Mediterranean region Ph.D. Thesis MICHAL BENOVICS Supervisor: prof. RNDr. Andrea Vetešníková Šimková, Ph.D. Department of Botany and Zoology Brno 2020 Bibliographic entry Author: Mgr. Michal Benovics Faculty of Science, Masaryk University Department of Botany and Zoology Title of Thesis: Host-specific parasites (Dactylogyrus, Monogenea) as indicator of evolution and historical dispersion of their cyprinid fish hosts in the Mediterranean region Degree programme: D-EKEB Ecological and Evolutionary Biology Specialization: PARA Parasitology Supervisor: prof. RNDr. Andrea Vetešníková Šimková, Ph.D. Faculty of Science, Masaryk University Department of Botany and Zoology Academic Year: 2019/2020 Number of Pages: 87 + 186 Keywords: Monogenea; Cyprinoidei; Parasitism; Host-specificity; Coevolution; Cophylogeny; Dactylogyrus; Phylogeography Bibliografický záznam Autor: Mgr. Michal Benovics Přírodovědecká fakulta, Masarykova Univerzita Ústav botaniky a zoologie Název práce: Hostitelsky-specifičtí paraziti (Dactylogyrus, Monogenea) jako indikátor evoluce a historické disperze kaprovitých ryb v oblastech Mediteránu Studijní program: D-EKEB Ekologická a evoluční biologie Specializace: PARA Parazitologie Vedoucí práce: prof. RNDr. Andrea Vetešníková Šimková, Ph.D. Přírodovědecká fakulta, Masarykova Univerzita Ústav botaniky a zoologie Akademický rok: 2019/2020 Počet stran: 87 + 186 Klíčová slova: Monogenea; Cyprinoidei; Parasitismus; Hostitelská specifita; Koevoluce; Kofylogeneze; Dactylogyrus; Fylogeografie Abstract One of the fundamentals of evolutionary biology is the study of host-parasite coevolutionary relationships. Due to intertwined evolutionary history of two interacting species and on-going coadaptation processes of hosts and parasites we can expect that studying parasites will shed more light into evolutionary processes of their hosts. Monogeneans (ectoparasitic Platyhelminthes) and their fish hosts represent one of the best model for studying host-parasite evolutionary relationships using cophylogenetic approach. These parasites developed remarkably high host specificity, where each host species often serves as potential host for its own host-specific monogenean species. This thesis is focussed on the host-parasite system of Dactylogyrus (gill monogeneans) and their freshwater fish hosts in the peri-Mediterranean region. Dactylogyrus are almost exclusively parasites of cyprinoid fish and exhibit remarkable species diversity. This diversity is the most likely linked with the high diversity of their fish hosts, where Cyprinoidei represent highly diverse freshwater fish taxon. However, the historical dispersion of the cyprinoids in the peri-Mediterranean is not clearly resolved and is far more complex than could be explained by single dispersal model. Therefore, in this Ph.D thesis, the Dactylogyrus parasites were used as additional tool to investigate evolutionary history of their hosts. Communities of endemic Dactylogyrus in the peri-Mediterranean appear to be species poorer in comparison to Central Europe. However, their diversity is still weakly explored, as thesis eight new species were described in the Euro-Mediterranean region in this. Moreover, numerous species complexes appear to be present among Dactylogyrus parasites in the peri- Mediterranean, suggesting even higher species diversity of these monogeneans. Cophylogenetic methods revealed strong coevolutionary structure between phylogenies of Dactylogyrus and their respective cyprinoid hosts in peri-Mediterranean area with host switch as common coevolutionary event. Many host-parasite links significantly contributed into the global coevolutionary structure suggesting the strong coevolutionary link between associated hosts and parasites. The results presented in this thesis demonstrated usefulness of investigating the host- specific parasites phylogenetic relationships for uncovering evolutionary relationships between host lineages. Moreover, host-specific Dactylogyrus were shown as good marker to reveal historical and even more recent contacts (detecting introduction of non-native fish hosts into new regions) between cyprinoid host lineages. Abstrakt Jedním ze základních stavebních kamenů evoluční biologie je studium parazito-hostitelských koevolučních vztahů. Jelikož evoluční historie parazitů a jejich hostitelů je obvykle úzce spjatá, je možné předpokládat, že studium parazitů přispěje k poznání evolučních procesů jejich hostitelů. Monogenea (Platyhelminthes) a jejich rybí hostitelé představují jeden z nejzajímavějších systémů pro studium parazito-hostitelských evolučních vztahů. U zástupců této skupiny parazitů se vyvinula velice úzká hostitelská specifita, kdy je jeden druh parazita často schopen cizopasit pouze na jednom druhu hostitele. Předložená dizertační práce je zaměřena na parazito-hostitelský systém Dactylogyrus (žaberní ektoparazité) a jejich rybí hostitele v Mediteránní oblasti. Studovaný rod cizopasníků se vyznačuje vysokou druhovou diverzitou a jednotliví zástupci jsou téměř výhradně paraziti kaprovitých ryb. Fascinující druhová diverzita parazitů rodu Dactylogyrus je s největší pravděpodobností důsledkem druhové bohatosti kaprovitých ryb, neboť tato skupina představuje nejvíce diverzifikovanou skupinu mezi sladkovodními rybami. Evoluční historie a historická disperze kaprovitých ryb v Mediteránu však není zcela objasněna a je pravděpodobně složitější, než se na první pohled může zdát. Právě proto se v této dizertační práci využívají paraziti jako nástroj pro objasnění evoluční historie rybích hostitelů. Ve všeobecnosti se jeví, že společenstva zástupců rodu Dactylogyrus jsou ve srovnání se střední Evropou druhově chudší v oblasti Mediteránu. Avšak celková diverzita parazitů je evidentně i nadále málo prozkoumaná, jelikož v rámci řešení problematiky dizertační práce bylo popsáno osm nových druhů Dactylogyrus. Navíc, molekulární analýzy naznačují existenci mnoha komplexů kryptických druhů, které mohou být klasickým taxonomickým přístupem, založeném na morfologii, jenom těžko identifikovatelné. Kofylogenetické metody odhalily statisticky významnou koevoluční strukturu mezi evolučními historiemi parazitů rodu Dactylogyrus a jejich rybími hostiteli. Více než polovina paraziticko-hostitelských asociací významně přispívala k celkové kofylogenetické struktuře. Výsledky předložené práce demonstrují užitečnost hostitelsko-specifických parazitů pro účely studia evoluční historie a biogeografie jejich hostitelů. Navíc, studiem parazitů rodu Dactylogyrus je možné detekovat historické kontakty mezi evolučně vzdálenými liniemi ryb, které recentně žijí v alopatrii. Acknowledgement First and foremost, I would like to honestly and with the greatest admiring thank my supervisor Andrea Vetešníková Šimková for accepting me as her student, providing me with everything I needed for purposes of research and developing myself, and neverending critical evaluation which formed outputs of my research into present form. Furthermore, I would like to thank all people who helped me with the collection of material for purposes of the thesis and especially Radek Šanda and Jasna Vukić for providing all the necessary input regarding fish, and Yves Desdevises for introduction to wonders of cophylogenetics, and his help with several phylogenetic analyses. The last, but not least, sincere gratitude and all my respect goes to my colleagues who shared the office with me and provided all-necessary distraction during the course of study. And of course I have to thank my grandmother for all her support, despite that she still have no idea what I am doing with my life. The research within Ph.D. thesis was financially supported by Czech Science Foundation – project No. GA15-19382S and marginally from No. GA20-13539S. Substantial financial support was also provided from project No. GBP505/15/G112. Original publications linked to the thesis The results of presented Ph.D thesis are composed of seven research papers. Papers are ordered chronologically by publication or submission date. Paper I Benovics M., Kičinjaová M. L. & Šimková A. (2017) 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. Parasites & Vectors 10: 547. doi: 10.1186/s13071-017-2491-z [IF2017 = 3.031, Q1] MB actively participated on the processing of fish and parasitological material, identified parasite species, performed all laboratory procedures and phylogenetic analyses, and wrote the manuscript. Overall contribution = ~70%. Paper II Šimková A., Benovics M., Rahmouni I. & Vukić J. (2017) Host-specific Dactylogyrus parasites revealing new insights on the historical biogeography of Northwest African and Iberian cyprinid fish. Parasites & Vectors 10: 589. doi: 10.1186/s13071-017-2521-x [IF2017 = 3.031, Q1] MB actively participated on the processing of fish and parasitological material, and identification of parasites species collected during field work. He participated on data analyses. Overall contribution = ~10%. Paper III Benovics M., Desdevises Y., Vukić J., Šanda R. & Šimková A. (2018) The phylogenetic relationships and species richness of host-specific Dactylogyrus parasites shaped by the biogeography of Balkan cyprinids. Scientific Reports 8: 13006. doi: 10.1038/s41598-018-31382-w [IF2018 = 4.011, Q1] MB
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