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Masaryk University Faculty of Science Department of Botany and Zoology Masaryk University Faculty of Science Department of Botany and Zoology Species diversity and phylogenetic relationships among gill-specific monogenean parasites (Platyhelminthes: Dactylogyridae) of cichlids (Cichlidae) from Lake Tanganyika Ph.D. Thesis by Chahrazed Rahmouni Supervisor prof. RNDr. Andrea Vetešníková Šimková, Ph.D. Consultant Maarten Vanhove, Ph.D. Brno 2021 Bibliographic Entry Author Chahrazed Rahmouni, MSc. Masaryk University, Faculty of Science Department of Botany and Zoology Title of Thesis: Species diversity and phylogenetic relationships among gill-specific monogenean parasites (Platyhelminthes: Dactylogyridae) of cichlids (Cichlidae) from Lake Tanganyika Degree programme: Ecological and Evolutionary Biology Specialization: Parasitology Supervisor: prof. RNDr. Andrea Vetešníková Šimková, Ph.D. Academic Year: 2020/2021 Number of Pages: 296 Keywords: Cichlidae, gill parasites, Monogenea, Cichlidogyrus, Lake Tanganyika, phylogeny, host-parasite associations, host specificity, host range Bibliografický záznam Author Chahrazed Rahmouni, MSc. Masarykova Univerzita, Přírodovědecká Fakulta Ústav Botaniky a Zoologie Název práce: Druhová diverzita a fylogenetické vztahy hostitelsky specifických žaberních monogeneí parazitujícich ryby čeledi Cichlidae v jezeře Tanganyika Studijní program: Ekologická a Evoluční Biologie Specializace: Parazitologie Vedoucí práce: prof. RNDr. Andrea Vetešníková Šimková, Ph.D. Akademický rok: 2020/2021 Počet stran: 296 Klíčová slova: Cichlidae, žaberní parazité, Monogenea, Cichlidogyrus, jezero Tanganyika, fylogeneze, hostitelsko-parazitické asociace Abstract This Ph.D. thesis focuses on the gill-specific monogenean parasites of cichlids inhabiting the oldest of the East African Great Lakes, the Tanganyika. This system is one of the main hotspots of the cichlid diversity worldwide counting 241 species of 16 highly diverse lineages (tribes). Lake Tanganyika cichlids are considered as one of the most successful vertebrate adaptive radiations, however, the knowledge on their parasite fauna is still limited. Herein, the gill monogeneans (Platyhelminthes, Dactylogyridae) infecting cichlids from most endemic tribes of Lake Tanganyika were studied using morphometrics, geomorphometrics and phylogenetics. The main objectives of this thesis were to study (i) the species and morphological diversity of the monogeneans belonging to Cichlidogyrus from cichlids inhabiting Lake Tanganyika (study A, B), (ii) the morphological and molecular intraspecific variabilities in selected species of Cichlidogyrus parasitizing cichlid species with contrasting dispersal capacities (study C), and phylogenetically closely related cichlid species (congeneric representatives) versus representatives of phylogenetically distant lineages (study D), and finally (iii) the phylogeny of Cichlidogyrus parasitizing cichlids and the history of host-parasite associations in this system (study E). Cichlid species representing the majority of Lake Tanganyika tribes were collected from various locations along the lake shorelines and nearby smaller freshwater bodies. In total, 31 Cichlidogyrus species were identified, of which 25 species were recognised as new for science. This includes 15 species that were formally described within this doctoral thesis from 11 cichlid hosts of six tribes (Cyprichromini, Cyphotilapiini, Ectodini, Eretmodini, Tropheini, and Tylochromini). The remaining species are awaiting formal description. Morphological similarities in Cichlidogyrus species parasitizing closely related hosts along the lake were identified. A checklist of the species of Cichlidogyrus from Lake Tanganyika and outside of the lake highlighted the importance of morphological diversity of the sclerotized part of the vagina, and that of the heel (part of the male copulatory organ), a feature missing in many species. Additionally, it was shown that species of Cichlidogyrus cluster in more than the previously recognised four groups (studies A, B) defined based on the morphology of the hook pairs. In the second chapter (study C), we hypothesised an association between the host dispersal capacity and the intraspecific variability of sclerotized parts of the haptor of their host specific monogeneans. Two Cichlidogyrus species were studied, C. gistelincki parasitizing a cichlid species with good dispersal capacity (‘Ctenochromis’ horei, Tropheini) and C. 4 milangelnari parasitizing a cichlid species with poor dispersal capacity (Cyprichromis microlepidotus, Cyprichromini). Populations of C. milangelnari parasitizing the poor dispersers were more differentiated in their anchor shape when compared to populations of C. gistelincki parasitizing well-dispersing hosts. Next study (study D) was focused on C. nshomboi widely reported in Boulengerochromis microlepis representing an ancient tribe in Lake Tanganyika (Boulengerochromini), and surprisingly retrieved also from representatives of a distant lineage, Perissodini (Perissodus microlepis, P. straeleni and Haplotaxodon microlepis). An inheritance from a common ancestor, host switching event or incipient speciation were suggested to explain the presence of C. nshomboi on unrelated hosts. The later scenario was supported by genetic divergence in the nuclear and mitochondrial genes. The intertribal shape and size variations of anchors were attributed to phenotypic plasticity or to adaptation. The lack of morphological and genetic differentiations among the populations of C. nshomboi parasitizing three cichlid species of Perissodini was related to their population genetic structure. Moreover, our results supported the correlation between host body size, intensity of infection and anchors size. In the last chapter of the present Ph.D. thesis (study E), we presented the first comprehensive phylogenetic study of Cichlidogyrus parasitizing members of most cichlid tribes from LT, including dactylogyridean representatives from the rest of African freshwater systems. Cichlidogyrus parasitizing mainly West African cichlid tribes revealed to be paraphyletic with respect to species parasitizing hosts belonging to the East African cichlid radiation, which constituted a well-supported monophylum. Cichlidogyrus belonging to Tylochromini and Oreochromini hosts that have colonised Lake Tanganyika only recently, cluster with their non-Lake Tanganyika relatives. The diversification of Cichlidogyrus in the lake seems to be driven by failure to diverge in old lineages of cichlids, cospeciation in more recently evolved ones, and host switching followed by parasite duplication at various host tribal level. Evaluation of host specificity and structural evolution of haptoral and reproductive organs in Lake Tanganyika Cichlidogyrus revealed that strict specialist species with larval hook size and lacking sclerotized vagina represent the most ancestral states of haptor configuration and vagina sclerotization characters, suggesting that Cichlidogyrus in this system evolved from a very simple form to a more complex one like their West African congeners. Generalist species among Cichlidogyrus with a sclerotized vagina parasitizing ancient Lake Tanganyika host lineages seem to have developed a different hook configuration, most probably to ensure successful colonization of new hosts, so far phylogenetically unrelated. 5 Abstrakt Předložená disertační práce se zaměřuje na žaberní parazity taxonu Monogenea, které infikují cichlidy obývající nejstarší z východoafrických Velkých jezer, Tanganiku. Tento systém je jedním z hlavních světových hotspotů diversity cichlid, čítá 241 druhů 16 vysoce rozmanitých linií (tribů). Cichlidy jezera Tanganika jsou považovány za jednu z nejúspěšnějších adaptivních radiací obratlovců, avšak znalosti o jejich parazitofauně jsou stále limitovány. Pomocí morfometrie, geomorfometrie a fylogenetiky byli studováni žaberní paraziti taxonu Monogenea (Platyhelminthes, Dactylogyridae) infikující cichlidy z většiny endemických tribů jezera Tanganika. Hlavním cílem dizertační práce bylo studium (i) druhové a morfologické diverzity monogeneí náležících do rodu Cichlidogyrus parazitující cichlidy obývající jezero Tanganika (studie A, B), (ii) morfologické a molekulární vnitrodruhové variability u vybraných druhů rodu Cichlidogyrus parazitující druhy čeledi Cichlidae s kontrastními disperzními schopnostmi (studie C), nebo fylogeneticky blízce příbuzné druhy cichlid (kongeneričtí zástupci) versus druhy fylogeneticky vzdálených linií (studie D), a nakonec (iii) fylogeneze monogeneí rodu Cichlidogyrus parazitující ryby čeledi Cichlidae a evoluční historie parazito-hostitelských vztahů v tomto systému (studie E). Druhy cichlid představující většinu tribů jezera Tanganika byly vzorkovány na různých lokalitách podél břehů jezera a v blízkých menších vodních zdrojích. Celkem bylo identifikováno 31 druhů rodu Cichlidogyrus, z nichž 25 druhů bylo identifikováno jako druhy nové pro vědu. Z tohoto počtu bylo 15 druhů formálně popsaných v rámci předložené disertační práce, jedná se o druhy zaznamenané na 11 hostitelích šesti tribů Cichlidae (Cyprichromini, Cyphotilapiini, Ectodini, Eretmodini, Tropheini a Tylochromini). Zbývající druhy čekají na formální popis. Byly identifikovány morfologické podobnosti u druhů rodu Cichlidogyrus parazitující na blízce příbuzných hostitelích podél jezera. Checklist druhů rodu Cichlidogyrus z jezera Tanganika i mimo jezero naznačuje význam morfologické rozmanitosti sklerotizovaných části samičích a samčích reprodukčních orgánů. Dále bylo prokázáno, že druhy rodu Cichlidogyrus formují více
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