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MASARYK UNIVERSITY FACULTY OF SCIENCE The parasite fauna of economically important pelagic fishes in Lake Tanganyika Ph.D. Thesis NIKOL KMENTOVÁ Supervisor: Maarten Vanhove, Ph.D. Department of Botany and Zoology Brno 2019 Bibliographic Entry Author Mgr. Nikol Kmentová Faculty of Science, Masaryk University Department of Botany and Zoology Title of Thesis: The parasite fauna of economically important pelagic fishes in Lake Tanganyika Degree programme: Ecological and Evolutionary Biology Specialization: Parasitology Supervisor: Maarten Vanhove, Ph.D. Academic Year: 2019/2020 Number of Pages: 350 + 72 Keywords: Kapentagyrus, Dolicirrolectanum, Cryptogonimidae, Clupeidae, Latidae, Bathybatini Bibliografický záznam Autor: Mgr. Nikol Kmentová Přírodovědecká fakulta, Masarykova univerzita Ústav botaniky a zoologie Název práce: Parazité ekonomicky významných ryb pelagické zóny jezera Tanganika Studijní program: Ekologická a evoluční biologie Specializace: Parazitologie Vedoucí práce: Maarten Vanhove, Ph.D. Akademický rok: 2019/2020 Počet stran: 350 + 72 Klíčová slova: Kapentagyrus, Dolicirrolectanum, Cryptogonimidae, Clupeidae, Latidae, Bathybatini ABSTRACT Biodiversity is a well-known term characterising the variety and variability of life on Earth. It consists of many different levels with species richness as the most frequently used measure. Despite its generally lower species richness compared to littoral zones, the global importance of the pelagic realm in marine and freshwater ecosystems lies in the high level of productivity supporting fisheries worldwide. In terms of endemicity, Lake Tanganyika is one of the most exceptional freshwater study areas in the world. While dozens of studies focus on this lake’s cichlids as model organisms, our knowledge about the economically important fish species is still poor. Despite their important role in speciation processes, parasite taxa have been vastly ignored in the African Great Lakes including Lake Tanganyika for many years. In the framework of this PhD thesis, the fauna of parasitic flatworms (Platyhelminthes, Neodermata) infecting economically important pelagic fish species in Lake Tanganyika (bathybatine cichlids, clupeids and lates perches) was characterised to analyse parasites’ host-specificity, population structure and historical origin. Overall, a low parasite host-specificity in the lake’s pelagic zone was documented in all examined fish taxa. While clupeids and bathybatine cichlids are infected by representatives of the dactylogyrid monogenean genera Kapentagyrus and Cichlidogyrus, respectively, three of the four latid species are parasitized by the same diplectanid monogenean species of Dolicirroplectanum. The origin of the primarily marine diplectanids in African freshwaters is proposed to be connected with their hosts’ marine ancestry. Interestingly, the digenean diversity recovered from three species of lates perches clearly surpassed the single monogenean species retrieved from these host species. Parasite populations were analysed by means of combined morphological and molecular approaches. Their genetic population structure does not show a clear north-south gradient. The observed geographically dependent phenotypic plasticity in monogenean species is therefore assumed to be induced by environmental differences during ontogenetic development. Nevertheless, incipient speciation related to host species identity is assumed for Kapentagyrus tanganicanus. Host size related infection dynamics of two species of Kapentagyrus were proposed to explain their contrasting success of co-introduction to non-native areas. Recent demographic expansion in monogenean species infecting clupeid and cichlid hosts was detected and can be linked with paleogeographic events and climate change, respectively. Finally, this thesis showed the importance of a combined approach in order to correctly discern between phenotypic plasticity and interspecific boundaries and highlighted the potential of parasites in better understanding the pelagic ecosystem. ABSTRAKT Biodiverzita je globálně používaný termín charakterizující rozmanitost a variabilitu života na Zemi. Doposud bylo popsáno mnoho různých úrovní a definic biodiverzity, avšak nejvíce rozšířeným ukazatelem biologické rozmanitosti je počet druhů. I přes nižší úroveň biodiverzity oproti litorálu, globální význam pelagické zóny mořských i sladkovodních ekosystémů tkví především v její vysoké produktivitě, která je hnací silou celosvětového rybářského průmyslu. Jezero Tanganika je se svou vysokou úrovní endemismu jedním z nejvíce studovaných sladkovodních ekosystémů na Zemi. Zatímco nespočet prací byl věnován cichlidám, jakožto známému modelu pro studium evolučních mechanismů, znalosti o ekonomicky významnějších skupinách ryb jsou stále nedostačující. Též parazitické organismy ve Velkých afrických jezerech, včetně jezera Tanganiky, i přes jejich důležitou úlohu v diverzifikačních procesech svých hostitelů, jsou stále přehlíženy. Předložená dizertační práce se zabývá parazitickými ploštěnci (Platyhelminthes, Neodermata) infikující ekonomicky významné druhy ryb v jezeře Tanganika z čeledí Clupeidae (sleďovití) a Latidae (latesovití), a cichlidy ze skupiny Bathybatini, za účelem studia jejich hostitelské specificity, populační struktury a historického původu. Snížená hostitelská specifita parazitů oproti litorální zóně byla prokázána u všech tří vybraných skupin hostitelů. Zatímco studované druhy cichlid a sleďovitých ryb jsou parazitovány rody Kapentagyrus a Cichlidogyrus (Monogenea, Dactylogyridae), tři ze čtyř druhů latesovitých ryb jsou hostitelé druhu rodu Dolicirroplectanum, patřící do skupiny Diplectanidae. Původ této primárně mořské skupiny parazitů v jezeře Tanganika je s největší pravděpodobností spojen s mořským původem hostitelů. Druhová diverzita motolic infikující latesovité ryby (šest druhů čeledi Cryptogonimidae) převyšuje jediný druh výše zmíněné skupiny žábrohlístů. Genetická populační struktura vybraných parazitických druhů se zdá být zcela nezávislá na gradientu zeměpisné šířky nebo hostitelském druhu. Zjištěná vnitrodruhová fenotypová plasticita je tedy je pravděpodobně ovlivněna podmínkami prostředí během ontogeneze. Nicméně, počáteční speciace poháněná vzájemnou izolací hostitelských druhů byla zjištěna druhu K. tanganicanus. Míra parazitace podmíněná velikostí hostitele byla navržena jako důvod absence jednoho z druhů Kapentagyrus v nepůvodních oblastech výskytu hostitele. Zaznamenaná expanze vybraných parazitických druhů v demografickém měřítku je pravděpodobně spjata s paleogeografickou historií oblasti jezera, včetně klimatických změn. Předložená dizertační práce zdůrazňuje důležitost využití multidisciplinárního přístupu pro studium mezidruhových rozdílů a populační struktury, a možnost využití parazitů k lepšímu porozumění pelagického ekosystému. ACKNOWLEDGEMENTS I would like to express my sincere gratitude to Maarten Vanhove, a supervisor full of patience who kept me motivated for all these years and whose selfless time and care were sometimes all that kept me going. My deepest appreciation goes to Milan Gelnar who introduced me to the fascinating world full of ingenious parasitological strategies and ignited the profound love for parasites in my heart. A very special gratitude goes out to Stephan Koblmüller from the University of Graz for help with population genetic analyses, greatly tolerant to all my questions. I was more than lucky having such experienced ichthyologists as Maarten Van Steenberge from the Royal Museum for Central Africa in Tervuren, Pascal Masilya Mulungula and Théophile Mulimbwa N’sibula from the Centre de Recherche en Hydrobiologie in Uvira, mentoring me through the biological aspects of different fish groups. I am very grateful to Tom Artois, my mentor at the University of Hasselt, who gave me the opportunity to be part of the zoology lab and thought me to look at flatworms and taxonomy in general from a very different perspective. I have greatly benefited from the introduction to digenean taxonomy and leading through morphological descriptions given by Simona Georgieva from the University of Valencia and Rodney A. Bray from the Natural History in London. I appreciate the feedback on statistical analyses offered by Joost A. Raeymaekers from the University of Oslo and Pascal Hablützel from the Flanders Marine Institute. With a special mention to all my colleagues in Brno, it was great sharing laboratory with all of you during last four years full of fruitful discussions with Jiří Vorel, Michal Benovics, Tomáš Pakosta, Jana Ilgová, Magdaléna Kováčiková, Šárka Mašová, Eliška Jirounková, Radka Pecková, Chahrazed Rahmouni, Lucie Škorpíková and Nikol Reslová. I would like also to acknowledge my colleagues at the University of Hasselt, namely Michiel Jorissen, Marlies Monnens, Armando Cruz Laufer, Mare Geraerts. as well as at the Katholieke Universiteit Leuven, namely my mentor Filip Volckaert, Els De Keyzer, Henrik Christiansen and Federico Calboli. My research would have been impossible without the financial support of Czech Grant Agency, projects P505/12/G112 and GA19-13573S, and University of Hasselt. Last but not least, my deepest thanks go to my partner for his patience and mental support and my parents who encouraged me during all the years of studying. Contents 1 INTRODUCTION ........................................................................................................ 3 2 AIMS............................................................................................................................
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  • Morphology, Molecules, and Monogenean Parasites: an Example of an Integrative Approach to Cichlid Biodiversity

    Morphology, Molecules, and Monogenean Parasites: an Example of an Integrative Approach to Cichlid Biodiversity

    RESEARCH ARTICLE Morphology, Molecules, and Monogenean Parasites: An Example of an Integrative Approach to Cichlid Biodiversity Maarten Van Steenberge1,2,3*, Antoine Pariselle4¤a, Tine Huyse1,2, Filip A. M. Volckaert2, Jos Snoeks1,2, Maarten P. M. Vanhove1,2,5¤b 1 Biology Department, Royal Museum for Central Africa, Tervuren, Belgium, 2 Laboratory of Biodiversity and Evolutionary Genomics, Department of Biology, University of Leuven, Leuven, Belgium, 3 Institute of Zoology, University of Graz, Graz, Austria, 4 Institut des Sciences de l'Évolution, IRD-CNRS-Université Montpellier, Montpellier, France, 5 Institute of Marine Biological Resources and Inland Waters, Hellenic Centre for Marine Research, Anavyssos, Greece ¤a Current address: IRD, ISE-M, Yaoundé, Cameroon ¤b Current address: Capacities for Biodiversity and Sustainable Development, Operational Directorate Natural Environment, Royal Belgian Institute of Natural Sciences, Brussels, Belgium * [email protected] OPEN ACCESS Citation: Van Steenberge M, Pariselle A, Huyse T, Abstract Volckaert FAM, Snoeks J, Vanhove MPM (2015) Morphology, Molecules, and Monogenean Parasites: The unparalleled biodiversity of Lake Tanganyika (Africa) has fascinated biologists for over An Example of an Integrative Approach to Cichlid a century; its unique cichlid communities are a preferred model for evolutionary research. Biodiversity. PLoS ONE 10(4): e0124474. doi:10.1371/journal.pone.0124474 Although species delineation is, in most cases, relatively straightforward, higher-order clas- sifications were shown not to agree with monophyletic groups. Here, traditional morphologi- Academic Editor: Robert Guralnick, University of Colorado, UNITED STATES cal methods meet their limitations. A typical example are the tropheine cichlids currently belonging to Simochromis and Pseudosimochromis. The affiliations of these widespread Received: August 19, 2014 and abundant cichlids are poorly understood.