Population genomics of introduced Nile tilapia Oreochromis niloticus (Linnaeus, 1758) in the Democratic Republic of the Congo: Repeated introductions since colonial times with multiple sources.
RAD sequencing; cichlid; genetic integrity; genetic structure; independent introductions; invasive species; Animals; Aquaculture; Democratic Republic of the Congo; Introduced Species; Metagenomics; Cichlids/genetics; Ecology, Evolution, Behavior and Systematics; Genetics
Abstract :
[en] During colonial times, Nile tilapia Oreochromis niloticus (Linnaeus, 1758) was introduced into non-native parts of the Congo Basin (Democratic Republic of the Congo, DRC) for the first time. Currently, it is the most farmed cichlid in the DRC, and is present throughout the Congo Basin. Although Nile tilapia has been reported as an invasive species, documentation of historical introductions into this basin and its consequences are scant. Here, we study the genetic consequences of these introductions by genotyping 213 Nile tilapia from native and introduced regions, focusing on the Congo Basin. Additionally, 48 specimens from 16 other tilapia species were included to test for hybridization. Using RAD sequencing (27,611 single nucleotide polymorphisms), we discovered genetic admixture with other tilapia species in several morphologically identified Nile tilapia from the Congo Basin, reflecting their ability to interbreed and the potential threat they pose to the genetic integrity of native tilapias. Nile tilapia populations from the Upper Congo and those from the Middle-Lower Congo are strongly differentiated. The former show genetic similarity to Nile tilapia from the White Nile, while specimens from the Benue Basin and Lake Kariba are similar to Nile tilapia from the Middle-Lower Congo, suggesting independent introductions using different sources. We conclude that the presence of Nile tilapia in the Congo Basin results from independent introductions, reflecting the dynamic aquaculture history, and that their introduction probably leads to genetic interactions with native tilapias, which could lower their fitness. We therefore urge avoiding further introductions of Nile tilapia in non-native regions and to use native tilapias in future aquaculture efforts.
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Geraerts, Mare ; Research Group Zoology: Biodiversity and Toxicology, Centre for Environmental Sciences, Hasselt University, Diepenbeek, Belgium
Vangestel, Carl ; OD Taxonomy and Phylogeny, Royal Belgian Institute of Natural Sciences, Brussels, Belgium ; Terrestrial Ecology Unit, Ghent University, Ghent, Belgium
Artois, Tom; Research Group Zoology: Biodiversity and Toxicology, Centre for Environmental Sciences, Hasselt University, Diepenbeek, Belgium
Fernandes, Jorge Manuel de Oliveira ; Faculty of Biosciences and Aquaculture, Nord University, Bodø, Norway
Jorissen, Michiel W P; Research Group Zoology: Biodiversity and Toxicology, Centre for Environmental Sciences, Hasselt University, Diepenbeek, Belgium
Chocha Manda, Auguste; Unité de recherche en Biodiversité et Exploitation durable des Zones Humides (BEZHU), Faculté des Sciences Agronomiques, Université de Lubumbashi, Lubumbashi, Democratic Republic of the Congo
Danadu Mizani, Célestin; Département d'Ecologie et Biodiversité des Ressources Aquatique, Centre de Surveillance de la Biodiversité (CSB), Université de Kisangani, Kisangani, Democratic Republic of the Congo
Smeets, Karen ; Research Group Zoology: Biodiversity and Toxicology, Centre for Environmental Sciences, Hasselt University, Diepenbeek, Belgium
Snoeks, Jos; Department of Biology, Royal Museum for Central Africa, Tervuren, Belgium ; Laboratory of Biodiversity and Evolutionary Genomics, KU Leuven, Leuven, Belgium
Sonet, Gontran; OD Taxonomy and Phylogeny, Royal Belgian Institute of Natural Sciences, Brussels, Belgium
Tingbao, Yang; Institute of Aquatic Economic Animals and Key Laboratory for Improved Variety Reproduction of Aquatic Economic Animals, Zhongshan University, Ghangzhou, China
Van Steenberge, Maarten; OD Taxonomy and Phylogeny, Royal Belgian Institute of Natural Sciences, Brussels, Belgium ; Laboratory of Biodiversity and Evolutionary Genomics, KU Leuven, Leuven, Belgium
Vreven, Emmanuel; Department of Biology, Royal Museum for Central Africa, Tervuren, Belgium ; Laboratory of Biodiversity and Evolutionary Genomics, KU Leuven, Leuven, Belgium
Vanhove, Maarten P M; Research Group Zoology: Biodiversity and Toxicology, Centre for Environmental Sciences, Hasselt University, Diepenbeek, Belgium ; Laboratory of Biodiversity and Evolutionary Genomics, KU Leuven, Leuven, Belgium ; Zoology Unit, Finnish Museum of Natural History, University of Helsinki, Helsinki, Finland ; Department of Botany and Zoology, Faculty of Science, Masaryk University, Brno, Czech Republic
Huyse, Tine ; Department of Biology, Royal Museum for Central Africa, Tervuren, Belgium ; Laboratory of Biodiversity and Evolutionary Genomics, KU Leuven, Leuven, Belgium
Population genomics of introduced Nile tilapia Oreochromis niloticus (Linnaeus, 1758) in the Democratic Republic of the Congo: Repeated introductions since colonial times with multiple sources.
RCN - Research Council of Norway EMBRC Belgium - European Marine Biological Resource Centre UGent - Ghent University FWO - Fonds Wetenschappelijk Onderzoek Vlaanderen BELSPO - Belgian Science Policy Office
Funding text :
We would like to acknowledge the financial support of the Belgian Science Policy (BELSPO) through JEMU (Joint Experimental Molecular Unit), Belgian Federal Science Policy Office (BRAIN-be Pioneer Project BR/132/PI/TILAPIA), EMBRC Belgium—FWO project GOH3817N, European Research Council project (no. 683210), Research Council of Norway (no. 250548/F20), VLIR-UOS South Initiative ZRDC2014MP084, the OCA type II project S1_RDC_TILAPIA and Mbisa Congo project (2013-2018), the last two being framework agreement projects of RMCA with the Belgian Development Cooperation, and the Czech Science Foundation (P505/12/G112—European Centre of Ichtyoparasitology ECIP). M.G. was supported by the Bijzonder Onderzoeksfonds (BOF-project 7NI02) of Hasselt University for the analysis, interpretation of data and writing of the manuscript. M.W.P.J. was supported by a BOF Reserve Fellowship from Hasselt University. M.P.M.V. received travel grant K220314N from the Research Foundation—Flanders (FWO-Vlaanderen) and support from the Belgian Directorate-General for Development Cooperation and Humanitarian Aid (CEBioS programme at the Royal Belgian Institute of Natural Sciences), and was financed by the Special Research Fund of Hasselt University (BOF20TT06). Additionally, we appreciate the help of the people involved in field work and sampling. In particular, we thank Eva Řehulková, Maria Lujza Červenka Kičinja and Andrea Šimková (Masaryk University, Czech Republic), Shevy Rothman (Steinhardt Museum of Natural History, Tel Aviv University, Israel), Stephan Koblmüller (University of Graz, Austria), Antoine Pariselle (Institute de Recherche pour le Développement, University of Montpellier, France; Université Mohammed V de Rabat, Morocco), Jeanne Rasamy Razanabolana, Jean Robertin Rasoloariniaina, Roger Daniel Randrianiana, Sarah Rakotomamonjy and Natacha Rasozolaka (University d’Antananarivo, Madagascar), and Maxwell Barson (University of Zimbabwe, Zimbabwe) for providing valuable samples for our data set. 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. We acknowledge the help of Massimiliano Virgilio in the analyses and interpretation of our results, and of Dirk F. E. Thys van den Audenaerde (Royal Museum for Central Africa/KU Leuven) for sharing his insights on tilapia. Finally, we thank Ria Vanderspikken (Hasselt University) and Natascha Steffanie (Hasselt University) for their technical support in the laboratory.
Agnèse, J. F., Adépo-Gourène, B., Abban, E. K., & Fermon, Y. (1997). Genetic differentiation among natural populations of the Nile tilapia Oreochromis niloticus (Teleostei, Cichlidae). Heredity, 79(1), 88–96. https://doi.org/10.1038/hdy.1997.126
Anane-Taabeah Attu, G., Frimpong, E. A., & Hallerman, E. M. (2022). Defining management units for wild Nile tilapia Oreochromis niloticus from nine river basins in Ghana. Diversity, 14(2), 73. https://doi.org/10.3390/d14020073
Anane-Taabeah, G., Frimpong, E. A., & Hallerman, E. (2019). Aquaculture-mediated invasion of the genetically improved farmed Tilapia (GIFT) into the lower volta basin of ghana. Diversity, 11(10), 188. https://doi.org/10.3390/d11100188
Andrews, S., Lindenbaum, P., Howard, B., & Ewels, P. (2011). FastQC high throughput sequence QC report. www.bioinformatics.babraham.ac.uk/projects/
Angienda, P. O., Lee, H. J., Elmer, K. R., Abila, R., Waindi, E. N., & Meyer, A. (2011). Genetic structure and gene flow in an endangered native tilapia fish (Oreochromis esculentes) compared to invasive Nile tilapia (Oreochromis niloticus) in Yala swamp, East Africa. Conservation Genetics, 12, 243–255.
Baird, N. A., Etter, P. D., Atwood, T. S., Currey, M. C., Shiver, A. L., Lewis, Z. A., Selker, E. U., Cresko, W. A., & Johnson, E. A. (2008). Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One, 3(10), e3376. https://doi.org/10.1371/journal.pone.0003376
Balirwa, J. S. (1992). The evolution of the fishery of Oreochromis niloticus (Pisces: Cichlidae) in Lake Victoria. Hydrobiologia, 232, 85–89. https://doi.org/10.1007/BF00014616
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, 57(1), 289–300.
Bezault, E., Balaresque, P., Toguyeni, A., Fermon, Y., Araki, H., Baroiller, J.-F., & Rognon, X. (2011). Spatial and temporal variation in population genetic structure of wild Nile tilapia (Oreochromis niloticus) across Africa. BMC Genetics, 12(1), https://doi.org/10.1186/1471-2156-12-102
Bezault, E., Rognon, X., Clota, F., Gharbi, K., Baroiller, J.-F., & Chevassus, B. (2012). Analysis of the meiotic segregation in intergeneric hybrids of Tilapias. International Journal of Evolutionary Biology, 2012, 1–10. https://doi.org/10.1155/2012/817562
Blackwell, T., Ford, A. G. P., Ciezarek, A. G., Bradbeer, S. J., Gracida Juarez, C. A., Smith, A. M., Ngatunga, B. P., Shechonge, A., Tamatamah, R., Etherington, G., Haerty, W., Di Palma, F., Turner, G. F., & Genner, M. J. (2020). Newly discovered cichlid fish biodiversity threatened by hybridization with non-native species. Molecular Ecology, 30(4), 895–911. https://doi.org/10.1111/mec.15638
Bradbeer, S. J., Harrington, J., Watson, H., Warraich, A., Shechonge, A., Smith, A., Tamatamah, R., Ngatunga, B. P., Turner, G. F., & Genner, M. J. (2019). Limited hybridization between introduced and critically endangered indigenous tilapia fishes in northern Tanzania. Hydrobiologia, 832, 257–268. https://doi.org/10.1007/s10750-018-3572-5
Brummett, R. E., Angoni, D. E., & Pouomogne, V. (2004). On-farm and on-station comparison of wild and domesticated Cameroonian populations of Oreochromis niloticus. Aquaculture, 242(1–4), 157–164. https://doi.org/10.1016/j.aquaculture.2004.01.036
Brummett, R. E., Lazard, J., & Moehl, J. (2008). African aquaculture: Realizing the potential. Food Policy, 33(5), 371–385. https://doi.org/10.1016/j.foodpol.2008.01.005
Brummett, R. E., & Ponzoni, R. W. (2009). Concepts, alternatives, and environmental considerations in the development and use of improved strains of tilapia in African aquaculture. Reviews in Fisheries Science, 17(1), 70–77. https://doi.org/10.1080/10641260802083174
Brummett, R., Stiassny, M., & Harrison, I. (2011). Chapter 1. Background. In: E. G. E. Brooks, D. J. Allen, & W. R. T. Darwall (Eds.), The status and distribution of freshwater biodiversity in Central Africa. IUCN.
Canonico, G. C., Arthington, A., McCrary, J. K., & Thieme, M. L. (2005). The effects of introduced tilapias on native biodiversity. Aquatic Conservation: Marine and Freshwater Ecosystems, 15, 463–483. https://doi.org/10.1002/aqc.699
Catchen, J., Amores, A., Hohenlohe, P., Cresko, W., & Postlethwait, J. (2011). Stacks: Building and Genotyping Loci De Novo from short-read Sequences, G3, 1, 171–182.
Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A., & Cresko, W. A. (2013). Stacks: An analysis tool set for population genomics. Molecular Ecology, 22(11), 3124–3140. https://doi.org/10.1111/mec.12354
Charpy, B. (1954). La pisciculture du tilapia en Afrique Equatoriale Française. Revue Bois Et Forêts Des Tropiques, 38, 27–30.
Ciezarek, A., Ford, A. G. P., Etherington, G. J., Kasozi, N., Malinsky, M., Mehta, T., Penso-Dolfin, L., Ngatunga, B. P., Shechonge, A., Tamatamah, R., Haerty, W., Di Palma, F., Genner, M. J., & Turner, G. F. (2021). Whole genome resequencing data enables a targeted SNP panel for conservation and aquaculture of Oreochromis cichlid fishes. bioRxiv. https://doi.org/10.1101/2021.03.24.436760
Conte, M. A., Gammerdinger, W. J., Bartie, K. L., Penman, D. J., & Kocher, T. D. (2017). A high quality assembly of the Nile tilapia (Oreochromis niloticus) genome reveals the structure of two sex determination regions. BMC Genomics, 18(314), 1–19. https://doi.org/10.1186/s12864-017-3723-5
D’Amato, M. E., Esterhuyse, M. M., van der Waal, B. C. W., Brink, D., & Volckaert, F. A. M. (2007). Hybridization and phylogeography of the Mozambuque tilapia Oreochromis mossambicus in southern Africa evidenced by mitochrondrial and microsatellite DNA genotyping. Conservation Genetics, 8, 475–488. https://doi.org/10.1007/s10592-006-9186-x
Danecek, P., Auton, A., Abecasis, G., Albers, C. A., Banks, E., DePristo, M. A., Handsaker, R. E., Lunter, G., Marth, G. T., Sherry, S. T., McVean, G., & Durbin, R. (2011). The variant call format and VCFtools. Bioinformatics, 27(15), 2156–2158. https://doi.org/10.1093/bioinformatics/btr330
Decru, E., Vreven, E., Danadu, C., Walanga, A., Mambo, T., & Snoeks, J. (2017). Ichthyofauna of the Itimbiri, Aruwimi, and Lindi/Tshopo rivers (Congo Basin): diversity and distribution patterns. Acta Ichthyologica Et Piscatoria, 47(3), 225–247. https://doi.org/10.3750/AIEP/02085
Decru, E., Vreven, E., & Snoeks, J. (2017). The occurences of an Eastern African haplochromine cichlid in the Ituri River (Aruwimi, Congo basin): Adaptive divergence in an introduced species? Hydrobiologia, 791(1), 209–220.
Deines, A. M., Bbole, I., Katongo, C., Feder, J. L., & Lodge, D. M. (2014). Hybridisation between native Oreochromis species and introduced Nile tilapia O. niloticus in the Kafue River, Zambia. African Journal of Aquatic Science, 39(1), 23–34. https://doi.org/10.2989/16085914.2013.864965
Deines, A. M., Wittmann, M. E., Deines, J. M., & Lodge, D. M. (2016). Tradeoffs among ecosystem services associated with global tilapia introductions. Reviews in Fisheries Science & Aquaculture, 24(2), 178–191. https://doi.org/10.1080/23308249.2015.1115466
Dias, M. A. D., de Freitas, R. T. F., Arranz, S. E., Villanova, G. V., & Hilsdorf, A. W. S. (2016). Evaluation of the genetic diversity of microsatellite markers among four strains of Oreochromis niloticus. Animal Genetics, 47, 345–353.
Dugan, P., Delaporte, A., Andrew, N., O’Keefe, M., & Welcomme, R. (2010). Blue harvest: Inland fisheries as an ecosystem service. WorldFish Center.
Dunz, A. R., & Schliewen, U. K. (2013). Molecular phylogeny and revised classification of the haplotilapiine cichlid fishes formerly referred to as “Tilapia”. Molecular Phylogenetics and Evolution, 68(1), 64–80. https://doi.org/10.1016/j.ympev.2013.03.015
Earl, D. A., & vonHoldt, B. M. (2012). STRUCTURE HARVESTER: A website and program visualizing STRUCTURE output and implementing the Evanno method. Conservation of Genetics Resources, 4(2), 359–361. https://doi.org/10.1007/s12686-011-9548-7
Eknath, A. E., & Hulata, G. (2009). Use and exchange of genetic resources of Nile tilapia (Oreochromis niloticus). Rev Aquacult, 1(3–4), 197–213. https://doi.org/10.1111/j.1753-5131.2009.01017.x
El-Sayed, A.-F.-M. (2013). Tilapia feed management practices in sub-Saharian Africa. In M. R. Hasan, & M. B. New (Eds.), On-farm feeding and feed management in aquaculture, Vol. 583 (pp. 377–405).
Etter, P. D., Bassham, S., Hohenlohe, P. A., Johnson, E. A., & Cresko, W. A. (2011). SNP discovery and genotyping for evolutionary genetics using RAD sequencing. Methods in Molecular Biology, 772, 157–178.
Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14(8), 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Facon, B., Jarne, P., Pointier, J. P., & David, P. (2005). Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: Hybrid vigour is more important than increase in genetic variance. Journal of Evolutionary Biology, 18(3), 524–535. https://doi.org/10.1111/j.1420-9101.2005.00887.x
FAO. (2016). The State of World Fisheries and Aquaculture 2016. http://www.fao/org/3/a-i5555e.pdf
FAO (2020). The state of world fisheries and aquaculture 2020. Sustainablilty in Action. https://doi.org/10.4060/ca9229en
Firmat, C., Alibert, P., Losseau, M., Baroiller, J.-F., & Schliewen, U. K. (2013). Succesive invasion-mediated interspecific hybridizations and populations structure in the endangered cichlid Oreochromis mossambicus. PLoS One, 8(5), https://doi.org/10.1371/journal.pone.0063880
Fitzpatrick, B. M. (2012). Estimating ancestry and heterozygotsity of hybrids using molecular markers. BMC Evolutionary Biology, 12, 1–14. https://doi.org/10.1186/1471-2148-12-131
Froese, R., & Pauly, D. (2021). Fishbase. World Wide Web electronic publication. version (08/2021). http://www.fishbase.org
Fuerst, P. A., Mwanja, W. W., & Kaufman, L. (2000). The genetic history of the introduced Nile tilapia in Lake Victoria (Uganda - E. Africa): The population structure of Oreochromis niloticus (Pisces: Cichlidae) revealed by DNA microsatellite markers. In K. Fitzsimmons, & J. C. Filho (Ed.), Tilapia aquaculture in the 21st century: Proceedings from the fifth international symposium on Tilapia aquaculture (pp. 30–40). Panorama da Aquicultura Magazine.
Gaskin, J. F., & Schaal, B. A. (2002). Hybrid Tamarix widespread in U.S. invasion and undetected in native Asian range. Proceedings of the National Academy of Sciences, 99(17), 11256–11259.
Gibson, I., Welsh, A. B., Welsh, S. A., & Cincotta, D. A. (2019). Genetic swamping and possible species collapse: tracking introgression between the native Candy Darter and introduced Variegate Darter. Conservation Genetics, 20, 287–298. https://doi.org/10.1007/s10592-018-1131-2
Goudswaard, P. C., Witte, F., & Katunzi, E. F. B. (2002). The tilapiine fish stock of Lake Victoria before and after the Nile perch upsurge. Journal of Fish Biology, 60, 838–856. https://doi.org/10.1006/jfbi.2002.1888
Hassanien, H. A., & Gilbey, J. (2005). Genetic diversity and differentiation of Nile tilapia (Oreochromis niloticus) revealed by DNA microsatellites. Aquaculture Research, 36, 1450–1457. https://doi.org/10.1111/j.1365-2109.2005.01368.x
Hohenlohe, P. A., Day, M. D., Amish, S. J., Miller, M. R., Kamps-Hughes, N., Boyer, M. C., Muhlfeld, C. C., Allendorf, F. W., Johnson, E. A., & Luikart, G. (2013). Genomic patterns of introgression in rainbow and westslope cutthroat trout illuminated by overlapping paired-end RAD sequencing. Molecular Ecology, 22(11), 3002–3013. https://doi.org/10.1111/mec.12239
Hornsby, M. A., Sabbah, S., Robertson, R. M., & Hawryshyn, C. W. (2013). Modulation of environmental light alters reception and production of visual signals in Nile tilapia. Journal of Experimental Biology, 216, 3110–3122. https://doi.org/10.1242/jeb.081331
Hosseinnia, Z., Shabany, A., & Kolangi-Miandare, H. (2014). Comparison of genetic variation of wild and farmed bream (Abramis brama orientalis; Berg, 1905) using microsatellite markers. Molecular Biology Research Communications, 3(3), 187–195.
Huet, M. (1957). Dix années de pisciculture au Congo belge et au Ruanda-Urundi: compte rendu de mission piscicole. Direction de l’Agriculture, des Forêts et de l’Elevage.
Huet, M. (1959). Aperçu de la pisciculture dans les régions tropicales en Extrême-Orient et en Afrique Centrale. Bulletin Français De Pisciculture, 193, 129–144.
Jakobsson, M., & Rosenberg, N. A. (2007). CLUMPP: A cluster matching and permutation program for dealing with switching and multimodality in analysis of population structure. Bioinformatics, 23(14), 1801–1806.
Jombart, T. (2008). Adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics, 24(11), 1403–1405.
Jorissen, M. W. P., Huyse, T., Pariselle, A., Lunkayilakio, S. W., Bukinga, F. M., Manda, A. C., Kasembele, G. K., Vreven, E. J., Decru, E., Artois, T., & Vanhove, M. P. M. (2020). Historical museum collections help detect parasite species jumps after tilapia introductions in the Congo Basin. Biological Invasions, 22, 2825–2844. https://doi.org/10.1007/s10530-020-02288-4
Kajungiro, R. A., Palaiokostas, C., Lopes Pinto, F. A., Mmochi, A. J., Mtolera, M., Houston, R. D., & de Koning, D. J. (2019). Population structure and genetic diversity of Nile tilapia (Oreochromis niloticus) strains cultured in Tanzania. Frontiers in Genetics, 10, 1–12. https://doi.org/10.3389/fgene.2019.01269
Kalinowski, S. T. (2005). HP-Rare 1.0: A computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes, 5, 187–189.
Keenan, K., McGinnity, P., Cross, T. F., Crozier, W. W., & Prodöhl, P. A. (2013). diveRsity: An R package for the estimation and exploration of population genetics parameters and their associated errors. Methods in Ecology and Evolution, 4, 782–788.
Khadher, S. B., Fontaine, P., Milla, S., & Agnèse, J.-F. (2016). Genetic characterization and relatedness of wild and farmed Eurasian perch (Perca fluviatilis): possible implications for aquaculture practices. Aquaculture Reports, 3, 136–146.
Kisekelwa, T., Snoeks, J., & Vreven, E. (2020). An annotated checklist of the fish fauna of the river systems draining the Kahuzi-Biega National Park (Upper Congo: Eastern DR Congo). Fish Biology, 96, 700–721.
Lazard, J. (1990). Transferts de poissons et développement de la production piscicole: exemple de trois pays d’Afrique subsaharienne. Revue D’hydrobiologie Tropicale, 23(3), 251–265.
Lederoun, D., Snoeks, J., Lalèyè, P., Vandewalle, P., & Vreven, E. (2018). An updated checklist of the ichthyofauna of the Mono River basin (Benin and Togo: West Africa). Ichthyological Exploration of Freshwaters, 28(2), 135–156.
Lemasson, J. (1958). Chronique piscicole. La pisciculture en Afrique équatoriale française et au Cameroon. Revue Bois Et Forêts Des Tropiques, 57, 57–61.
Li, H., & Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25(14), 1754–1760.
Lind, C. E., Agyakwah, S. K., Attipoe, F. Y., Nugent, C., Crooijmans, R. P. M. A., & Toguyeni, A. (2019). Genetic diversity of Nile tilapia (Oreochromis niloticus) throughout West Africa. Scientific Reports, 9, 1–12 https://doi.org/10.1038/s41598-019-53295-y
Lind, C. E., Brummett, R. E., & Ponzoni, R. W. (2012). Exploitation and conservation of fish genetic resources in Africa: Issues and priorities for aquaculture development and research. Reviews in Aquaculture, 4(3), 125–141. https://doi.org/10.1111/j.1753-5131.2012.01068.x
Lunkayilakio, S. W., Vreven, E., Vandewalle, P., Mutambue, S., & Snoeks, J. (2010). Contribution à la connaissance de l’ichtyofaune de l’Inkisi au Bas-Congo (RD du Congo). Cybium, 34(1), 83–91.
Makeche, M. C., Muleya, W., & Nhiwatiwa, T. (2020). Characterization of Oreochromis niloticus strains of Lake Kariba culture fisheries using morphological and meristic methods. American Scientific Research Journal for Engineering, Technology, and Sciences, 74(1), 31–40.
Marshall, B. (1988). The status of wild and cultured tilapia genetic resources in various countries: Africa: Zimbabwe. In R. S. V. Pullin (Ed.), Tilapia Genetic Resources for Aquaculture. ICLARM Conference Proceedings 16. International Center for Living Aquatic Resources Management.
McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., & DePristo, M. A. (2010). The Genome analysis toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research, 20(9), 1297–1303.
Micha, J.-C. (2013). Fish farming in the Congo Basin: past, present and future. In Nutrition and food production in the Congo Basin (pp. 147–171). Royal Academies for Science and the Arts of Belgium.
Mireku, K. K., Kassam, D., Changadeya, W., Attipoe, F. Y. K., & Adinortey, C. A. (2017). Assessment of genetic variations of Nile tilapia (Oreochromis niloticus L.) in the Volta Lake of Ghana using microsatellite markers. African Journal of Biotechnology, 16(7), 312–321.
Montcho, S. A., Agadjihouèdé, H., Montchowui, E., Lalèyè, P. A., & Moreau, J. (2015). Population parameters of Oreochromis niloticus (Cichlidae) recently introduced in Lake Toho (Benin, West Africa). International Journal of Fisheries and Aquatic Studies, 2(3), 141–145.
Moralee, R. D., van der Bank, F. H., & van der Waal, B. C. W. (2000). Biochemical genetic markers to identify hybrids between the endemic Oreochromis mossambicus and the alien species, O. niloticus (Pisces: Cichlidae). Water SA, 26(2), 263–268.
Morgan, M. (2021). BiocManager: access the bioconductor project package repository. https://CRAN.R-project.org/package=BiocManager
Moses, M., Mtolera, M. S. P., Chauka, L., Lopes, F. A., de Koning, D. J., Houston, R. D., & Palaiokostas, C. (2020). Characterizing the genetic structure of introduced Nile tilapia (Oreochromis niloticus) strains in Tanzania using double digest RAD sequencing. Aquaculture International, 28, 477–492. https://doi.org/10.1007/s10499-019-00472-5
Naylor, R. L., Williams, S. L., & Strong, D. R. (2001). Aquaculture - A gateway for exotic species. Science, 294, 1655–1656.
Peakall, R., & Smouse, P. E. (2006). GENALEX 6: Genetic analyses in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288–295.
Peakall, R., & Smouse, P. E. (2012). GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research - an update. Bioinformatics, 28, 2537–2539.
Philippart, J., & Ruwet, J. (1982). Ecology and distribution of tilapias. In R. S. V. Pullin, & R. H. Lowe-McConnell (Eds.), The biology and culture of Tilapias. ICLARM Conference Proceedings 7(pp. 15–59). International Center for Living Aquatic Resources Management.
Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155(2), 945–959.
Pullin, R. S. V., & Capili, J. B. (1988). Genetic improvement of tilapias: problems and prospects. In R. S. V. Pullin, T. Bhukasawan, K. Tonguthai, & J. L. Maclean (Eds.), The Second International Symposium on Tilapia in Aquaculture. ICLARM Conference Proceedings 15. Department of Fisheries, Bankok, Thailand, and International Center for Living Resources Management.
Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M. A. R., Bender, D., Maller, J., Sklar, P., de Bakker, P. I. W., Daly, M. J., & Sham, P. C. (2007). PLINK: A tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics, 81(3), 559–575. https://doi.org/10.1086/519795
R Core Team (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/
Rhymer, J. M., & Simberloff, D. (1996). Extinction by hybridization and introgression. Annual Review of Ecology and Systematics, 27, 83–109.
Robert, R. (1976). La pisciculture du tilapia a la Réunion. Revue Forestière Française, 378–387.
Roberts, T. R., & Stewart, D. J. (1976). An ecological and systematic survey of fishes in the rapids of the Lower Zaïre or Congo River. Bulletin of the Museum of Comparative Zoology, 147(6), 239–317.
Romana-Eguia, M. R. R., Ikeda, M., Basiao, Z. U., & Taniguchi, N. (2005). Genetic changes during mass selection for growth in Nile tilapia, Oreochromis niloticus), assessed by microsatellites. Aquaculture Research, 36, 69–78.
Rosenberg, N. A. (2004). Distruct: A program for the geographical display of population structure. Molecular Ecology Notes, 4, 137–138.
Runge, J. (2007). The Congo River, Central Africa. In A. Gupta (Ed.), Large rivers: Geomorpohology and management (pp. 293–309). John Wiley & Sons.
Rutten, M. J. M., Komen, H., Deerenberg, R. M., Siwek, M., & Bovenhuis, H. (2004). Genetic characterization of four strains of Nile tilapia (Oreochromis niloticus L.) using mircosatellite markers. International Society for Animal Genetics, 35, 93–97.
Satia, B. P. (2017). Regional review on status and trends in aquaculture development in sub-Saharan Africa - 2017. FAO Fisheries and Aquaculture Circular, 1135/2. https://www.fao.org/3/i6873e/i6873e.pdf
Seyoum, S., & Kornfield, I. (1992). Taxonomic notes of the Oreochromis niloticus subspecies-complex (Pisces: Cichlidae), with a description of a new subspecies. Canadian Journal of Zoology, 70(11), 2161–2165. https://doi.org/10.1139/z92-291
Shechonge, A., Ngatunga, B. P., Tamatamah, R., Bradbeer, S. J., Harrington, J., Ford, A. G. P., Turner, G. F., & Genner, M. J. (2018). Losing cichlid fish biodiversity: Genetic and morphological homogenization of tilapia following colonization by introduced species. Conservation Genetics, 19, 1199–1209. https://doi.org/10.1007/s10592-018-1088-1
Snoeks, J., Harrison, I. J., & Stiassny, M. L. J. (2011). The status and distribution of freshwater fishes. In W. R. T. Darwall, K. Smith, D. Allen, R. Holland, I. Harrison, & E. Brooks (Eds.), The diversity of life in African freshwaters: Underwater, under threat. An analysis of the status and distribution of freshwater species throughout mainland Africa. IUCN.
Sukmanomon, S., Senanan, W., Kapuscinski, A. R., & Na-Nakorn, U. (2012). Genetic diversity of feral populations of Nile tilapia (Oreochromis niloticus) in Thailand and evidence of genetic introgression. Aquaculture and Natural Resources, 46(2), 200–216.
Thys van den Audenaerde, D. F. E. (1964). Revision systematique des especes congolaises du genre Tilapia (Pisces, Cichlidae). Annalen Koninklijk Museum Voor Midden-Afrika Zoologische Wetenschappen, 124, 1–155.
Thys van den Audenaerde, D. F. E. (1988). Resource papers on tilapias in Africa: Natural distribution of tilapias and its consequences for the possible protection of genetic resources. In R. S. V. Pullin (Ed.), Tilapia Genetic Resources for Aquaculture. ICLARM Conference Proceedings 16 (p. 108). International Center for Living Aquatic Resources Management.
Tibihika, P. D., Curto, M., Alemayehu, E., Waidbacher, H., Masembe, C., Akoll, P., & Meimberg, H. (2020). Molecular genetic diversity and differentiation of Nile tilapia (Oreochromis niloticus, L. 1758) in East African natural and stocked populations. BMC Evolutionary Biology, 20, 1–20. https://doi.org/10.1186/s12862-020-1583-0
Tibihika, P. D., Curto, M., Dornstauder-Schrammel, E., Winter, S., Alemayehu, E., Waidbacher, H., & Meimberg, H. (2019). Application of microsatellite genotyping by sequencing (SSR-GBS) to measure genetic diversity of the East African Oreochromis niloticus. Conservation Genetics, 20, 357–372.
Tibihika, P. D., Waidbacher, H., Masembe, C., Curto, M., Sabatino, S., Alemayehu, E., Meulenbroek, P., Akoll, P., & Meimberg, H. (2018). Anthropogenic impacts on the contextual morphological diversification and adaptation of Nile tilapia (Oreochromis niloticus, L. 1758) in East Africa. Environmental Biology of Fishes, 101, 363–381.
Todesco, M., Pascual, M. A., Owens, G. L., Ostevik, K. L., Moyers, B. T., Hübner, S., Heredia, S. M., Hahn, M. A., Caseys, C., Bock, D. G., & Rieseberg, L. H. (2016). Hybridization and extinction. Evolutionary Applications, 9(7), 892–908. https://doi.org/10.1111/eva.12367
Toguyeni, A. (2004). Tilapia production and its global impacts in Central African countries. In R. Bolivar, G. Mair, & K. Fitzsimmons (Eds.), 6th International Symposium on Tilapia in Aquaculture. ICLARM.
Trewavas, E. (1983). Tilapiine Fishes of the Genera Sarotherodon. Oreochromis and Danakilia. British Museum (Natural History).
Vreven, E. J., Adépo-Gourène, B., Agnèse, J.-F., & Teugels, G. G. (1998). Morphometric and allozyme variation in natural populations and cultured strains of the Nile tilapia Oreochromis niloticus (Teleostei, Cichlidae). Belgian Journal of Zoology, 128(1), 23–34.
Wasonga, A. G., Daniel, W. A., & Brian, O. (2017). Interspecific hybridization of tilapiines in Lake Victoria, Kenya. Journal of Fisheries and Livestock. Production, 5(2), https://doi.org/10.4172/2332-2608.1000235
Welcomme, R. L. (1988). International introductions of inland aquatic species. FAO Fisheries Technical Paper, 294, 318.
Wohlfarth, G. W., & Hulata, G. I. (1981). Applied genetics of Tilapias, Vol. 6. International Center for Living Aquatic Resources Management.
Zengeya, T. A., Robertson, M. P., Booth, A. J., & Chimimba, C. T. (2012). Ecological niche modeling of the invasive potential of Nile tilapia Oreochromis niloticus in African river systems: Concerns and implications for the conservation of indigenous congenerics. Biological Invasions, 15(7), 1507–1521. https://doi.org/10.1007/s10530-012-0386-7