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Molecular footprint of parasite co-introduction with Nile tilapia in the Congo Basin

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Abstract

Nile tilapia, one of the most popular aquaculture species worldwide, has been introduced into the Congo Basin several times for aquaculture purposes. Previous studies based on morphological features showed that some of the monogenean gill parasites were co-introduced with Nile tilapia and some spilled over to native Congolese cichlids. In this study, we genetically investigated the co-introduced monogeneans of Nile tilapia from three major parts of the Congo Basin: Upper, Middle and Lower Congo. We sequenced 214 specimens belonging to 16 species of Monogenea, collected from native and introduced tilapia species from Congo, Madagascar and Burundi. We evaluate their position in a phylogeny including 38 monogenean species in total. Our results confirm the co-introductions in the Congo Basin and suggest one unreported parasite transmission from introduced Nile tilapia to native Mweru tilapia in Upper Congo, which was undetectable with a morphological study alone. Shared parasite COI haplotypes between Madagascar and the Congo Basin illustrate how anthropogenic introduction events homogenize parasite communities across large geographical distances and thereby disrupt isolation by distance patterns. Contrary to our expectation, the parasite populations co-introduced in the Congo Basin reveal a high COI diversity, probably resulting from multiple Nile tilapia introductions from different geographic origins. Additionally, we tested the barcoding gap and the performance of mitochondrial COI and nuclear ribosomal ITS-1, 28S and 18S markers. We found a significant barcoding gap of 15% for COI, but none for the other markers. Our molecular results reveal that Cichlidogyrus halli, C. papernastrema, C. tiberianus, C. cirratus and C. zambezensis are in need of taxonomic revision.

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Data availability

All data generated or analysed during this study is included in this manuscript and its supplementary files. All generated sequences can be found on GenBank (see Addendum 1).

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Acknowledgements

We thank B Vanschoenwinkel (VUBrussels), I Schön (Royal Belgian Institute for Natural Sciences) and J-L Justine (Musée National d’histoire Naturelle) for independently reviewing this manuscript before submission. We thank S Koblmüller (University of Graz), E Abwe, BK Manda, C Mukweze Mulelenu, M Kasongo Ilunga Kayaba and C Kalombo Kabalika (Université de Lubumbashi), M Collet and P N’Lemvo (Institut Congolais pour la Conservation de la Nature), D Kufulu-ne-Kongo (Ecole Muilu Kiawanga), L Matondo Mbela (Université Kongo), P Nguizani Bimbundi, B Boki Fukiakanda, P Ntiama Nsiku (Institut Supérieur Pédagogique de Mbanza-Ngungu), P Nzialu Mahinga (Institut National pour l’Etude et la Recherche Agronomiques – Mvuazi/Institut Supérieur d’études agronomiques – Mvuazi), M Katumbi Chapwe, E Řehulková, N Kmentová (Masaryk University), the Schreyen-Brichard family (Fishes of Burundi), and JR Rasoloariniaina, J Rasamy Razanabolana and S Rakotomamonjy (Université d’Antananarivo) for administrative, field and lab support, making this study possible. We thank M Barson and T Dubé for the field samplings in Lake Kariba.

Funding

This research was supported by the Belgian Federal Science Policy Office (BRAIN-be Pioneer Project (BR/132/PI/TILAPIA), research grant 1513419 N of the Research Foundation – Flanders (FWO-Vlaanderen), the University Development Cooperation of the Flemish Interuniversity Council (VLIR-UOS) South Initiative ZRDC2014MP084, the OCA type II project S1_RDC_TILAPIA and the Mbisa Congo project (2013–2018), the latter two being framework agreement projects of the RMCA with the Belgian Development Cooperation, and the Czech Science Foundation project no. P505/12/G112–European Centre of Ichtyoparasitology (ECIP). MWPJ was supported by a BOF Reserve Fellowship from Hasselt University. MPMV is receiving support from the special research fund (BOF20TT06). MPMV received travel grant K220314N from the Research Foundation – Flanders (FWO-Vlaanderen), support from the Belgian Directorate-General for Development Cooperation and Humanitarian Aid (CEBioS programme at the Royal Belgian Institute of Natural Sciences), and is financed by the Special Research Fund of Hasselt University (BOF20TT06). The research leading to results presented in this publication was carried out with infrastructure funded by EMBRC Belgium – FWO project GOH3817N.

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Authors and Affiliations

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

    Michiel Jorissen, Maarten P. M. Vanhove & Tom Artois

  2. Department of Biology, Royal Museum for Central Africa, Tervuren, Belgium

    Michiel Jorissen, Jos Snoeks, Emmanuel Vreven & Tine Huyse

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

    Maarten P. M. Vanhove, Jos Snoeks, Emmanuel Vreven & Tine Huyse

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

    Maarten P. M. Vanhove & Andrea Šimková

  5. ISEM, Université de Montpellier, CNRS, IRD, EPHE, Montpellier, France

    Antoine Pariselle

  6. Laboratory Biodiversity, Ecology and Genome, Research Center Plant and Microbial Biotechnology, Biodiversity and Environment, Faculty of Sciences, Mohammed V University, Rabat, Morocco

    Antoine Pariselle

  7. Institut Supérieur Pédagogique, Mbanza-Ngungu, Democratic Republic of the Congo

    Soleil Wamuini Lunkayilakio

  8. Unité de Recherche en Biodiversité et Exploitation Durable des Zones Humides (BEZHU), Faculté Des Sciences Agronomiques, Université de Lubumbashi, Haut-Katanga, Democratic Republic of the Congo

    Auguste Chocha Manda & Gyrhaiss Kapepula Kasembele

  9. Section de Parasitologie, Département de Biologie, Centre de Recherche en Hydrobiologie-Uvira, Uvira, Democratic Republic of the Congo

    Fidel Muterezi Bukinga

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  1. Michiel Jorissen
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  12. Tine Huyse
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Corresponding authors

Correspondence to Michiel Jorissen or Tine Huyse.

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Ethics approval

The field expedition and sampling in Burundi were approved by Ethics Committee of Masaryk University, approval number CZ01308. Fieldwork was carried out under permission 06/AR.ED./15 from the General Directorate for Fishery Resources and Fisheries, Ministry of Fisheries Resources and Fisheries of Madagascar, and mission statements 863/2014 (Faculté des Sciences Agronomiques, Université de Lubumbashi), C/075/2015/I.S.P./MBNGU/AUT.AC and AC/076/2015/I.S.P./MBNGU/AUT.AC.

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Jorissen, M., Vanhove, M.P.M., Pariselle, A. et al. Molecular footprint of parasite co-introduction with Nile tilapia in the Congo Basin. Org Divers Evol 22, 1003–1019 (2022). https://doi.org/10.1007/s13127-022-00563-x

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