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Morphological and Genetic Divergence in a Gill Monogenean Parasitizing Distant Cichlid Lineages of Lake Tanganyika: Cichlidogyrus nshomboi (Monogenea: Dactylogyridae) from Representatives of Boulengerochromini and Perissodini

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Abstract

As hosts constitute the resource for parasites, an adaptive radiation in a host can drive one in a parasite. In Lake Tanganyika, the diversification of cichlids has often led to a diversification of their Cichlidogyrus monogeneans. Hitherto, Cichlidogyrus nshomboi was known only from Boulengerochromis microlepis, the sole member of Boulengerochromini. Surprisingly, we retrieved this monogenean from Perissodus microlepis, P. straeleni and Haplotaxodon microlepis, belonging to Perissodini. We sequenced the nuclear 18S, 28S, ITS1 rDNA, and the mitochondrial COI genes and studied the morphology of the male copulatory organ (MCO) and the anchors of the attachment organ. This confirmed the conspecificity of the specimens. The occurrence of C. nshomboi on unrelated host lineages could be explained by inheritance from a common ancestor, or by host-switching. We further investigated the genetic and morphological variation across taxonomic (host tribes and species) and geographical scales. Results revealed divergence in ITS1 and COI between parasites infecting different tribes, which could indicate incipient speciation. Additionally, morphological differentiation in the shape and size of anchors was found between these groups, which could be attributed to phenotypic plasticity or to adaptation. Monogeneans from large-bodied B. microlepis had significantly larger anchors, whereas only two of the four measurements differed for the MCO. Unexpectedly, no morphological variation was observed between specimens infecting different species of Perissodini from nearby localities. However, differences were found between C. nshomboi infecting P. microlepis from different parts of the lake, which could be linked to the population genetic structure of the host.

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Data Availability

Genetic sequence data is publicly available from the NCBI database or from the author upon request. The voucher specimens of monogeneans are housed in the Royal Museum for Central Africa (RMCA, Belgium) (see ‘Materials and Methods’ for details on repositories and accession numbers).

References

  • Agosta, S. J., Janz, N., & Brooks, D. R. (2010). How specialists can be generalists: Resolving the and “parasite paradox” and implications for emerging infectious disease. Zoologia (Curitiba), 27(2), 151–162.

    Article  Google Scholar 

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403–410.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 and Vectors, 10(1), 547.

  • Birgi, E., & Euzet, L. (1983). Monogènes parasites des poissons des eaux douces du Cameroun. Présence des genres Cichlidogyrus et Dactylogyrus chez Aphyosemion (Cyprinodontidae). Bulletin de la Société Zoologique de France, 108, 101–106.

    Google Scholar 

  • Bonhomme, V., Picq, S., Gaucherel, C., & Claude, J. (2014). Momocs: outline analysis using R. Journal of Statistical Software, 56(13), 1–24.

    Article  Google Scholar 

  • Brooks, D. R. (1979). Testing the context and extent of host-parasite coevolution. Systematic Biology, 28(3), 299–307.

    Article  Google Scholar 

  • Buchmann, K. (1989). Relationship between host size of Anguilla anguilla and the infection level of the monogeneans Pseudodactylogyrus spp. Journal of Fish Biology, 35(4), 599–601.

    Article  Google Scholar 

  • Bueno-Silva, M., Boeger, W. A., & Pie, M. R. (2011). Choice matters: Incipient speciation in Gyrodactylus corydori (Monogenoidea: Gyrodactylidae). International Journal for Parasitology, 41(6), 657–667.

    Article  PubMed  Google Scholar 

  • Bush, A. O., Lafferty, K. D., Lotz, J. M., & Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology, 83(4), 575–583.

  • Charleston, M. A., & Robertson, D. L. (2002). Preferential host switching by primate lentiviruses can account for phylogenetic similarity with the primate phylogeny. Systematic Biology, 51(3), 528–535.

    Article  CAS  PubMed  Google Scholar 

  • Cohen, A. S., Lezzar, K. E., Tiercelin, A. J. J., & Soreghan, M. (1997). New palaeogeographic and lake-level reconstructions of Lake Tanganyika: Implications for tectonic, climatic and biological evolution in a rift lake. Basin Research, 9(2), 107–132.

    Article  Google Scholar 

  • Cribb, T. H., Chisholm, L. A., & Bray, R. A. (2002). Diversity in the Monogenea and Digenea: Does lifestyle matter? International Journal for Parasitology, 32(3), 321–328.

    Article  PubMed  Google Scholar 

  • Cruz-Laufer, A. J., Artois, T., Koblmüller, S., Pariselle, A., Smeets, K., Van Steenberge, M., & Vanhove, M. P. M. (2021). The role of phylogeny and ecological opportunity in host-parasite interactions: Network metrics, host repertoire, and network link prediction. Authorea. https://doi.org/10.22541/au.163274253.31016446/v1

    Article  Google Scholar 

  • Danley, P. D., Husemann, M., Ding, B., DiPietro, L. M., Beverly, E. J., & Peppe, D. J. (2012). The impact of the geologic history and paleoclimate on the diversification of East African cichlids. International Journal of Evolutionary Biology, 2012, 574851.

  • Dávidová, M., Jarkovský, J., Matějusová, I., & Gelnar, M. (2005). Seasonal occurrence and metrical variability of Gyrodactylus rhodei Žitňan 1964 (Monogenea, Gyrodactylidae). Parasitology Research, 95(6), 398–405.

    Article  PubMed  Google Scholar 

  • Evans, N., & Paulay, G. (2012). DNA barcoding methods for invertebrates. Methods in Molecular Biology, 858, 47–77.

    Article  CAS  PubMed  Google Scholar 

  • Fankoua, S. O., Bitja Nyom, A. R., ne dort Bahanak, D., Bilong Bilong, C., & Pariselle, A. (2017). Influence of preservative and mounting media on the size and shape of monogenean sclerites. Parasitology Research, 116, 2277–2281.

    Article  Google Scholar 

  • Fricke, R., Eschmeyer, W., & Fong, J. D. (2020). Catalogue of fishes: Genera, species, references. Retrieved September 1, 2020, from, http://researcharchive.calacademy.org/research/ichthyology/catalog/SpeciesByFamily.asp

  • Givnish, T. J. (1997). Adaptive radiations and molecular systematics: Issues and approaches. In T. J. Givnish & K. J. Systma (Eds.), Molecular evolution and adaptive radiation (pp. 1–54). Cambridge University Press.

    Google Scholar 

  • Gobbin, T. P., Vanhove, M. P. M., Pariselle, A., Groothuis, T. G. G., Maan, M. E., & Seehausen, O. (2020). Temporally consistent species differences in parasite infection but no evidence for rapid parasite-mediated speciation in Lake Victoria cichlid fish. Journal of Evolutionary Biology, 33(5), 556–575.

    Article  PubMed  PubMed Central  Google Scholar 

  • Good, P. (2001). Permutation tests: A practical guide to resampling methods for testing hypotheses. Springer-Verlag.

  • Gubbins, S., Gilligan, C. A., & Kleczkowski, A. (2000). Population dynamics of plant-parasite interactions: Thresholds for invasion. Theoretical Population Biology, 57(3), 219–233.

    Article  CAS  PubMed  Google Scholar 

  • Gussev, A. V. (1983). The method of collecting and processing of fish parasitic monogenean material (48 pp.). Nauka (in Russian).

  • Gussev, A. V. (1995). Some pathways and factors of monogenean microevolution. Canadian Journal of Fisheries and Aquatic Sciences, 52, 52–56.

    Article  Google Scholar 

  • Hablützel, P. I., Vanhove, M. P. M., Deschepper, P., Grégoir, A. F., Roose, A. K., Volckaert, F. A. M., & Raeymaekers, J. A. M. (2017). Parasite escape through trophic specialization in a species flock. Journal of Evolutionary Biology, 30(7), 1437–1445.

    Article  PubMed  Google Scholar 

  • Hammer, Ø., Harper, D., & Ryan, P. (2001). Past: Paleontological statistics software package for education and data analysis. Paleontologia Electronica, 4(1), 1–9.

    Google Scholar 

  • Hassouna, N., Michot, B., & Bachellerie, J.-P. (1984). 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 Research, 12(8), 3563–3583.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hebert, P. D. N., Ratnasingham, S., & DeWaard, J. R. (2003). Barcoding animal life: Cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society B: Biological Sciences, 270(Suppl 1), S96–S99.

  • Hillis, D. M., & Dixon, M. T. (1991). Ribosomal DNA: Molecular evolution and phylogenetic inference. Quarterly Review of Biology, 66(4), 411–453.

    Article  CAS  PubMed  Google Scholar 

  • Humason, G. L. (1979). Animal tissue techniques. Freeman and Company.

  • Humphery-Smith, I. (1989). The evolution of phylogenetic specificity among parasitic organisms. Parasitology Today, 5(12), 385–387.

    Article  CAS  PubMed  Google Scholar 

  • Huyse, T., Audenaert, V., & Volckaert, F. A. M. (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(14), 1679–1689.

    Article  PubMed  Google Scholar 

  • Irisarri, I., Singh, P., Koblmüller, S., Torres-Dowdall, J., Henning, F., Franchini, P., Fischer, C., Lemmon, A. R., Lemmon, E. M., Thallinger, G. G., Sturmbauer, C., & Meyer, A. (2018). Phylogenomics uncovers early hybridization and adaptive loci shaping the radiation of Lake Tanganyika cichlid fishes. Nature Communications, 9(1), 3159.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jarkovský, J., Morand, S., Šimková, A., & Gelnar, M. (2004). Reproductive barriers between congeneric monogenean parasites (Dactylogyrus: Monogenea): Attachment apparatus morphology or copulatory organ incompatibility? Parasitology Research, 92(2), 95–105.

    Article  PubMed  Google Scholar 

  • Kaci-Chaouch, T., Verneau, O., & Desdevises, Y. (2008). Host specificity is linked to intraspecific variability in the genus Lamellodiscus (Monogenea). Parasitology, 135(5), 607–616.

    Article  CAS  PubMed  Google Scholar 

  • Karvonen, A., & Seehausen, O. (2012). The role of parasitism in adaptive radiations—When might parasites promote and when might they constrain ecological speciation? International Journal of Ecology. https://doi.org/10.1155/2012/280169

    Article  Google Scholar 

  • Khang, T. F., Soo, O. Y. M., Tan, W. B., & Lim, L. H. S. (2016). Monogenean anchor morphometry: Systematic value, phylogenetic signal, and evolution. PeerJ, 4, e1668.

  • Klingenberg, C. P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11(2), 353–357.

    Article  PubMed  Google Scholar 

  • Kmentová, N., Gelnar, M., Mendlová, M., Van Steenberge, M., Koblmüller, S., & Vanhove, M. P. M. (2016). Reduced host-specificity in a parasite infecting non-littoral Lake Tanganyika cichlids evidenced by intraspecific morphological and genetic diversity. Scientific Reports, 6, 39605.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kmentová, N., Koblmüller, S., Van Steenberge, M., Raeymaekers, J. A. M., Artois, T., De Keyzer, E. L. R., Milec, L., Muterezi Bukinga, F., Mulimbwa N'sibula, T., Masilya Mulungula, P., Ntakimazi, G., Volckaert, F. A. M., Gelnar, M., & Vanhove, M. P. M. (2020). Weak population structure and recent demographic expansion of the monogenean parasite Kapentagyrus spp. infecting clupeid fishes of Lake Tanganyika, East Africa. International Journal for Parasitology, 50(6–7), 471–486.

  • Kmentová, N., Van Steenberge, M., Raeymaekers, J. A. M., Koblmüller, S., Hablützel, P. I., Muterezi Bukinga, F., Mulimbwa N’sibula, T., Masilya Mulungula, P., Nzigidahera, B., Ntakimazi, G., Gelnar, M., & Vanhove, M. P. M. (2018). Monogenean parasites of sardines in Lake Tanganyika: Diversity, origin and intraspecific variability. Contributions to Zoology, 87(2), 105–132.

    Article  Google Scholar 

  • Koblmüller, S., Duftner, N., Sefc, K. M., Aigner, U., Rogetzer, M., & Sturmbauer, C. (2009). Phylogeographic structure and gene flow in the scale-eating cichlid Perissodus microlepis (Teleostei, Perciformes, Cichlidae) in southern Lake Tanganyika. Zoologica Scripta, 38(3), 257–268.

    Article  Google Scholar 

  • Koblmüller, S., Egger, B., Sturmbauer, C., & Sefc, K. M. (2007). Evolutionary history of Lake Tanganyika’s scale-eating cichlid fishes. Molecular Phylogenetics and Evolution, 44(3), 1295–1305.

    Article  CAS  PubMed  Google Scholar 

  • Koblmüller, S., Odhiambo, E. A., Sinyinza, D., Sturmbauer, C., & Sefc, K. M. (2015). Big fish, little divergence: Phylogeography of Lake Tanganyika’s giant cichlid, Boulengerochromis microlepis. Hydrobiologia, 748, 29–38.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Koblmüller, S., Sefc, K. M., & Sturmbauer, C. (2008). The Lake Tanganyika cichlid species assemblage: Recent advances in molecular phylogenetics. Hydrobiologia, 91(6), 277–290.

    Google Scholar 

  • Kocher, T. D. (2004). Adaptive evolution and explosive speciation: The cichlid fish model. Nature Reviews Genetics, 5(4), 288–298.

    Article  CAS  PubMed  Google Scholar 

  • Kocher, T. D., Conroy, J. A., Mckaye, K. R., Stauffer, J. R., & Lockwood, S. F. (1995). Evolution of NADH dehydrogenase subunit 2 in East African cichlid fish. Molecular Phylogenetics and Evolution, 4(4), 420–432.

    Article  CAS  PubMed  Google Scholar 

  • Konings, A. (2019). Tanganyika cichlids in their natural habitat. Hollywood Import & Export Inc.

  • Kornfield, I., & Smith, P. F. (2000). African cichlid fishes: Model systems for evolutionary biology. Annual Review of Ecology and Systematics, 31, 163–196.

    Article  Google Scholar 

  • Krasnovyd, V., Vetešník, L., Gettová, L., Civáňová, K., & Šimková, A. (2017). Patterns of parasite distribution in the hybrids of non-congeneric cyprinid fish species: Is asymmetry in parasite infection the result of limited coadaptation? International Journal for Parasitology, 47(8), 471–483.

    Article  PubMed  Google Scholar 

  • Krasnovyd, V., Vetešník, L., & Šimková, A. (2020). Distribution of host-specific parasites in hybrids of phylogenetically related fish: The effects of genotype frequency and maternal ancestry? Parasites & Vectors, 13(1), 402.

    Article  CAS  Google Scholar 

  • Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Librado, P., & Rozas, J. (2009). DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25(11), 1451–1452.

    Article  CAS  PubMed  Google Scholar 

  • Lim, L. H. S., & Gibson, D. I. (2009). A new monogenean genus from an ephippid fish off Peninsular Malaysia. Systematic Parasitology, 73(1), 13–25.

    Article  CAS  PubMed  Google Scholar 

  • Littlewood, D. T., Rohde, K., & Clough, K. A. (1997). Parasite speciation within or between host species? –phylogenetic evidence from site-specific polystome monogeneans. International Journal for Parasitology, 27(11), 1289–1297.

    Article  CAS  PubMed  Google Scholar 

  • Malmberg, G. (1957). On the occurrence of Gyrodactylus on Swedish fishes. Skrifter utgivna av Södra Sveriges Fiskeriföreningen, 1956, 19–76 (in Swedish).

    Google Scholar 

  • Mendlová, M., Desdevises, Y., Civáňová, K., Pariselle, A., & Šimková, A. (2012). Monogeneans of West African cichlid fish: Evolution and cophylogenetic interactions. PLoS ONE, 7(5), e37268.

  • Mendlová, M., & Šimková, A. (2014). Evolution of host specificity in monogeneans parasitizing African cichlid fish. Parasites and Vectors, 14(7), 69.

    Article  Google Scholar 

  • Messu Mandeng, F. D., Bilong Bilong, C. F., Pariselle, A., Vanhove, M. P. M., Bitja Nyom, A. R., & Agnèse, J. F. (2015). A phylogeny of Cichlidogyrus spp. (Monogenea, Dactylogyridea) clarifies a host-switch between fish families and reveals an adaptive component to attachment organ morphology of this parasite genus. Parasites and Vectors, 10(8), 582.

  • Meyer, B. S., Matschiner, M., & Salzburger, W. (2015). A tribal level phylogeny of Lake Tanganyika cichlid fishes based on a genomic multi-marker approach. Molecular Phylogenetics and Evolution, 83, 56–71.

    Article  PubMed  PubMed Central  Google Scholar 

  • Meyer, B. S., Matschiner, M., & Salzburger, W. (2017). Disentangling incomplete lineage sorting and introgression to refine species-tree estimates for Lake Tanganyika cichlid fishes. Systematic Biology, 66(4), 531–550.

    CAS  PubMed  Google Scholar 

  • Moszczynska, A., Locke, S. A., McLaughlin, J. D., Marcogliese, D. J., & Crease, T. J. (2009). Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Molecular Ecology Resources, 9(Suppl s1), 75–82.

  • Musilová, N., Řehulková, E., & Gelnar, M. (2009). Dactylogyrids (Platyhelminthes: Monogenea) from the gills of Labeo (Teleostei: Cyprinidae) from West Africa. Zootaxa, 2241, 47–68.

    Article  Google Scholar 

  • Muterezi Bukinga, F., Vanhove, M. P. M., Van Steenberge, M., & Pariselle, A. (2012). Ancyrocephalidae (Monogenea) of Lake Tanganyika: III: Cichlidogyrus infecting the world’s biggest cichlid and the non-endemic tribes Haplochromini, Oreochromini and Tylochromini (Teleostei, Cichlidae). Parasitology Research, 111(5), 2049–2061.

    Article  PubMed  Google Scholar 

  • Ochi, H., & Yanagisawa, Y. (1998). Commensalism between cichlid fishes through differential tolerance of guarding parents toward intruders. Journal of Fish Biology, 52(5), 985–996.

    Article  Google Scholar 

  • Pariselle, A., & Euzet, L. (2009). Systematic revision of dactylogyridean parasites (Monogenea) from cichlid fishes in Africa, the Levant and Madagascar. Zoosystema, 31(4), 849–898.

    Article  Google Scholar 

  • Plaisance, L., Littlewood, D. T. J., Olson, P. D., & Morand, S. (2005). Molecular phylogeny of gill monogeneans (Platyhelminthes, Monogenea, Dactylogyridae) and colonization of Indo-West Pacific butterflyfish hosts (Perciformes, Chaetodontidae). Zoologica Scripta, 34(4), 425–436.

    Article  Google Scholar 

  • Poll, M. (1986). Classification des Cichlidae du lac Tanganika. Tribus, genres et espèces. Académie Royale de Belgique Mémoires de la Classe de Sciences, Collection in‐8°–2e série, XLV—Fascicule 2.

  • Poulin, R. (2002). The evolution of monogenean diversity. International Journal for Parasitology, 32(3), 245–254.

    Article  PubMed  Google Scholar 

  • Poulin, R., & Mouillot, D. (2003). Parasite specialization from a phylogenetic perspective: A new index of host specificity. Parasitology, 126(Pt 5), 473–480.

    Article  CAS  PubMed  Google Scholar 

  • Pouyaud, L., Desmarais, E., Deveney, M., & Pariselle, A. (2006). Phylogenetic relationships among monogenean gill parasites (Dactylogyridea, Ancyrocephalidae) infesting tilapiine hosts (Cichlidae): Systematic and evolutionary implications. Molecular Phylogenetics and Evolution, 38(1), 242–249.

    Article  CAS  Google Scholar 

  • Rahmouni, C., Van Steenberge, M., Vanhove, M. P. M., & Šimková, A. (2020). Intraspecific morphological variation in Cichlidogyrus (Monogenea) parasitizing two cichlid hosts from Lake Tanganyika exhibiting different dispersal capacities. Hydrobiologia. https://doi.org/10.1007/s10750-020-04429-1

    Article  Google Scholar 

  • Rahmouni, C., Vanhove, M. P. M., & Šimková, A. (2017). Underexplored diversity of gill monogeneans in cichlids from Lake Tanganyika: Eight new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) from the northern basin of the lake, with remarks on the vagina and the heel of the male copulatory. Parasites and Vectors, 10(1), 591.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rahmouni, C., Vanhove, M. P. M., & Simkova, A. (2018). Seven new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) parasitizing the gills of Congolese cichlids from northern Lake Tanganyika. PeerJ, 23, e560.

  • Řehulková, E., Seifertová, M., Přikrylová, I., & Francová, K. (2018). Monogenea. In T. Scholz, M. P. M. Vanhove, N. Smit, Z. Jayasundera, & M. Gelnar (Eds.), A guide to the parasites of African freshwater fishes (pp. 185–243). AbcTaxa.

    Google Scholar 

  • Ribbink, A. J. (1984). Is the species flock concept tenable? In A. A. Echelle, & I. Kornfield (Eds.), Evolution of fish species flocks (pp. 21–25). Orono Press.

  • Roberts, L., & Janovy, J. (2009). Foundations of parasitology. Mc Graw Hill.

  • Rodríguez-González, A., Míguez-Lozano, R., Llopis-Belenguer, C., & Balbuena, J. A. (2015). Phenotypic plasticity in haptoral structures of Ligophorus cephali (Monogenea: Dactylogyridae) on the flathead mullet (Mugil cephalus): A geometric morphometric approach. International Journal for Parasitology, 45(5), 295–303.

    Article  PubMed  Google Scholar 

  • Rohde, K., & Watson, N. (1985). Morphology, microhabitats and geographical variation of Kuhnia spp. (Monogenea: Polyopisthocotylea). International Journal for Parasitology, 15(5), 569–586.

  • Rohlf, F. J. (2006). tpsDig2, digitize landmarks and outlines version 2.10. Department of Ecology and Evolution, State University.

  • Ronco, F., Büscher, H. H., Indermaur, A., & Salzburger, W. (2020). The taxonomic diversity of the cichlid fish fauna of ancient Lake Tanganyika, East Africa. Journal of Great Lakes Research, 46(5), 1067–1078.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ronco, F., Matschiner, M., Böhne, A., Boila, A., Büscher, H. H., El Taher, A., Indermauer, A., Malinsky, M., Ricci, V., Kahmen, A., Jentoft, S., & Salzburger, W. (2021). Drivers and dynamics of a massive adaptive radiation in cichlid fishes. Nature, 589, 78–81.

    Google Scholar 

  • Salzburger, W., Van Bocxlaer, B., & Cohen, A. S. (2014). Ecology and evolution of the African Great Lakes and their faunas. Annual Review of Ecology, Evolution, and Systematics, 46(5), 1067–1078.

    Google Scholar 

  • Schwarzer, J., Shabani, N., Esmaeili, H. R., Mwaiko, S., & Seehausen, O. (2017). Allopatric speciation in the desert: Diversification of cichlids at their geographical and ecological range limit in Iran. Hydrobiologia, 791(1), 193–207.

    Article  CAS  Google Scholar 

  • Seehausen, O. (2015). Process and pattern in cichlid radiations—Inferences for understanding unusually high rates of evolutionary diversification. New Phytologist, 207(2), 304–312.

    Article  PubMed  Google Scholar 

  • 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 and Vectors, 10(1), 589.

    Article  PubMed  PubMed Central  Google Scholar 

  • Šimková, A., Ondráčková, M., Gelnar, M., & Morand, S. (2002). Morphology and coexistence of congeneric ectoparasite species: Reinforcement of reproductive isolation? Biological Journal of the Linnean Society, 76(1), 125–135.

    Google Scholar 

  • Šimková, A., Plaisance, L., Matejusová, I., Morand, S., & Verneau, O. (2003). Phylogenetic relationships of the Dactylogyridae Bychowsky, 1933 (Monogenea: Dactylogyridea): The need for the systematic revision of the Ancyrocephalinae Bychowsky, 1937. Systematic Parasitology, 54(1), 1–11.

    Article  PubMed  Google Scholar 

  • Šimková, A., Verneau, O., Gelnar, M., & Morand, S. (2006). Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish. Evolution, 60(5), 1023–1037.

    Article  PubMed  Google Scholar 

  • Snoeks, J. (2000). How well known is the ichthyodiversity of the large East African lakes? Advances in Ecological Research, 31, 17–38.

    Article  Google Scholar 

  • Sturmbauer, C., Husemann, M., & Danley, P. (2011). Explosive speciation and adaptive radiation of East African cichlid fishes. In F. Zachos, & J. Habel (Eds.), Biodiversity hotspots. Springer.

  • Takahashi, R., Watanabe, K., Nishida, M., & Hori, M. (2007). Evolution of feeding specialization in Tanganyikan scale-eating cichlids: A molecular phylogenetic approach. BMC Evolutionary Biology, 18(7), 195.

    Article  Google Scholar 

  • Takahashi, T. (2003). Systematics of Tanganyikan cichlid fishes (Teleostei: Perciformes). Ichthyological Research, 50, 367–382.

    Article  Google Scholar 

  • Theisen, S., Palm, H. W., Al-Jufaili, S. H., & Kleinertz, S. (2017). Pseudempleurosoma haywardi sp. nov. (Monogenea: Ancyrocephalidae (sensu lato) Bychowsky & Nagibina, 1968): An endoparasite of croakers (Teleostei: Sciaenidae) from Indonesia. PLoS ONE, 12(9), e0184376.

  • Thompson, J. D., Higgins, D. G., & Gibson, T. J. (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(22), 4673–4680.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Steenberge, M., Pariselle, A., Huyse, T., Volckaert, F., Snoeks, J., & Vanhove, M. P. M. (2015). Morphology, molecules, and monogenean parasites: An example of an integrative approach to cichlid biodiversity. PLoS ONE, 10(4), e0124474.

  • Van Steenberge, M., Vanhove, M. P. M., Muzumani Risasi, D., Mulimbwa N’sibula, T., Muterezi Bukinga, F., Pariselle, A., Gillardin, C., Vreven, E., Raeymaekers, J. A. M., Huyse, T., Volckaert, F. A. M., Nshombo Muderhwa, V., & Snoeks, J. (2011). A recent inventory of the fishes of the north-western and centrtal western coast of Lake Tanganyika (Democratic Republic Congo). Acta Ichthyologica et Piscatoria, 41(3), 201–214.

    Article  Google Scholar 

  • Vanhove, M. P. M., Pariselle, A., Van Steenberge, M., Raeymaekers, J. A. M., Hablützel, P. I., Gillardin, C., Hellemans, B., Breman, F. C., Koblmüller, S., Sturmbauer, C., Snoeks, J., Volckaert, F. A. M., & Huyse, T. (2015). Hidden biodiversity in an ancient lake: Phylogenetic congruence between Lake Tanganyika tropheine cichlids and their monogenean flatworm parasites. Scientific Reports, 5, 13669.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vanhove, M. P. M., Tessens, B., Schoelinck, C., Jondelius, U., Littlewood, D. T. J., Artois, T., & Huyse, T. (2013). Problematic barcoding in flatworms: A case-study on monogeneans and rhabdocoels (Platyhelminthes). ZooKeys, 365, 355–379.

    Article  Google Scholar 

  • Vázquez, D. P., Poulin, R., Krasnov, B. R., & Shenbrot, G. I. (2005). Species abundance and the distribution of specialization in host-parasite interaction networks. Journal of Animal Ecology, 74, 946–955.

    Article  Google Scholar 

  • Vignon, M., & Sasal, P. (2010). The use of geometric morphometrics in understanding shape variability of sclerotized haptoral structures of monogeneans (Platyhelminthes) with insights into biogeographic variability. Parasitology International, 59(2), 183–191.

    Article  PubMed  Google Scholar 

  • Whittington, I. D., Chisholm, L. A., & Rohde, K. (2000). The larvae of Monogenea (Platyhelminthes). Advances in Parasitology, 44, 139–232.

    Article  Google Scholar 

  • Windsor, D. A. (1998). Most of the species on Earth are parasites. International Journal for Parasitology, 28(12), 1939–2410.

    Article  CAS  PubMed  Google Scholar 

  • Yanagisawa, Y., Nshombo Muderhwa, V., Nishida, M., & Niimura, Y. (1990). Sexual dichromatism and feeding habits of the scale-eater Plecodus straeleni (Cichlidae, Teleostei) in Lake Tanganyika. Journal of Ethology, 8, 25–28.

    Article  Google Scholar 

  • Zelditch, M. L., Swiderski, D. L., & Sheets, H. D. (2012). Geometric morphometrics for biologists: A primer. Academic Press Inc.

  • Ziętara, M. S., & Lumme, J. (2002). Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea, Gyrodactylidae). Evolution, 56(12), 2445–2458.

    Article  PubMed  Google Scholar 

  • Ziȩtara, M. S., & 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.

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors are grateful to C. Sturmbauer and S. Koblmüller (University of Graz, Austria), W. Salzburger (University of Basel, Switzerland), D. Muzumani Risasi (CRH-Uvira, DR Congo) for their precious help with cichlid collection and identification; M. Reichard and R. Blažek (Czech Academy of Sciences, Czech Republic) for their help with fish collection, dissection and providing us the photographs of cichlid species during the field trip; A. Meyer (University of Konstanz, Germany), G. Banyankimbona (University of Burundi), the Schreyen-Brichard family (Fishes of Burundi) and T. Veall and O.R. Mangwangwa (Rift Valley Tropicals) for the sample collection and fish identification; P. Masilya Mulungula, T. Mulimbwa N’sibula, V. Lumami Kapepula, E. Bahane Byaragi, S. Kambale Mukeranya and F. Muterezi Bukinga (CRH-Uvira, DR Congo) for co-organising the field work and their scientific contribution on Tanganyikan cichlids; Š. Mašová, V. Michálková, E. Řehulková, I. Přikrylová, L. Raisingerová, N. Kmentová, K. Civáňová, E. Jirounková, K. Koukalová, and M. Seifertová (Masaryk University, Brno, Czech Republic) for their help with fish dissection, parasite isolation and fixation and genetics. Finally, the authors would like to thank E. Verheyen, T. Backeljau, and all the colleagues working at the Royal Belgian Institute of Natural Sciences (RBINS, Brussels), M. Parrent from the Royal Museum for Central Africa (RMCA, Tervuren), T. Artois and his team (Hasselt University, Diepenbeek, Belgium) for their kind hospitality and for the precious help they provided during the stay in Belgium. This research was funded by the Czech Science Foundation Project No. P505/12/G112—European Centre of Ichtyoparasitology (ECIP) and further supported by standard project GA19-13573S (to M.V.S. and M.P.M.V.) and the Special Research Fund of Hasselt University (BOF20TT06, to M.P.M.V.). Fieldwork was partly supported by the Research Foundation—Flanders (FWO-Vlaanderen) (travel grants V.4.096.10.N.01 and K.2.032.08.N.01 to M.P.M.V., Research Programme G.0553.10) and two travel grants from the King Leopold III Fund for Nature Conservation and Exploration (to M.P.M.V. and M.V.S.). Sampling happened in accordance with research Permit No. 2007-258-CC-2006-151 from the Tanzania Commission for Science and Technology (COSTECH), and Mission Statement No. 013/MNRST/CRHU/2010 from the Ministère de la Recherche Scientifique et Technologique–CRH-Uvira. The funders had no role in study design, data collection and analyses, decision to publish, or preparation of the manuscript.

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Authors and Affiliations

  1. Department of Botany and Zoology, Faculty of Science, Masaryk University, Brno, Czech Republic

    Chahrazed Rahmouni, Maarten P. M. Vanhove, Andrea Šimková & Maarten Van Steenberge

  2. Centre for Environmental Sciences, Research Group Zoology: Biodiversity & Toxicology, Hasselt University, Diepenbeek, Belgium

    Maarten P. M. Vanhove

  3. Laboratory of Biodiversity and Evolutionary Genomics, Department of Biology, University of Leuven, Leuven, Belgium

    Maarten P. M. Vanhove & Maarten Van Steenberge

  4. Operational Directorate Taxonomy and Phylogeny, Royal Belgian Institute of Natural Sciences, Brussels, Belgium

    Maarten Van Steenberge

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  1. Chahrazed Rahmouni
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  2. Maarten P. M. Vanhove
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  3. Andrea Šimková
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  4. Maarten Van Steenberge
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Contributions

CR, MVS, MPMV and AŠ designed the study. MVS, MPMV and AŠ supervised the work. MPMV co-organised the fieldtrips, parasite collection, preparation of specimens and provided scientific background in the field. CR performed the lab work and data analysis, CR and MVS wrote the manuscript. All authors read and approved the final manuscript.

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Correspondence to Chahrazed Rahmouni.

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Rahmouni, C., Vanhove, M.P.M., Šimková, A. et al. Morphological and Genetic Divergence in a Gill Monogenean Parasitizing Distant Cichlid Lineages of Lake Tanganyika: Cichlidogyrus nshomboi (Monogenea: Dactylogyridae) from Representatives of Boulengerochromini and Perissodini. Evol Biol 49, 221–238 (2022). https://doi.org/10.1007/s11692-022-09564-2

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