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Hybridization and phylogeography of the Mozambique tilapia Oreochromis mossambicus in southern Africa evidenced by mitochondrial and microsatellite DNA genotyping

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Abstract

Many Oreochromis species utilized in aquaculture were extensively introduced outside their native range in Africa. Given their recent evolutionary radiation, these species hybridize easily, posing a threat to the integrity of local adaptation. The objective of this work was to study the genetic diversity of the Mozambique tilapia (Oreochromis mossambicus) in its native range, southern Africa, and provide a method for identifying hybrids with genetic markers. We genotyped the mitochondrial DNA (mtDNA) control region (385 bp) of wild and farmed O. mossambicus, wild and farmed O. niloticus and morphologic wild hybrids. These data were complemented with published sequences of parapatric and sympatric Oreochromis taxa. Phylogeographic analysis showed the presence of two O. mossambicus lineages, the southernmost representing a recent Holocene radiation. Hybridization of O. mossambicus was indicated by the presence of O. niloticus and O. mortimeri–andersonii mtDNA specimens in the Limpopo basin and of O. karongae mtDNA in specimens from Malawi. We also genotyped seven suspected hybrid individuals from the Limpopo River, and 137 wild and farmed Mozambique and Nile tilapia samples with five microsatellite markers. Factorial Component Analysis, Bayesian clustering and assignment analyses consistently delineated an O. mossambicus and an O. niloticus group, with the putative hybrids positioned in between. Different levels of hybridization were detected by the Bayesian assignment. The complex nature of hybridization and introgression between cichlid species raises major concerns for the long-term integrity of Mozambique tilapia.

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References

  • Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. TREE 16:613–622

    Google Scholar 

  • Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    PubMed  CAS  Google Scholar 

  • Barton NH (2001) The role of hybridization in evolution. Mol Ecol 10:551–568

    Article  PubMed  CAS  Google Scholar 

  • Beerli P (2004) Effect of unsampled populations on the estimation of population sizes and migration rates between sampled populations. Mol Ecol 13:827–836

    Article  PubMed  Google Scholar 

  • Belkhir K (1999) GENETIX, logiciel sous WindowsTM pour la génétique des populations. Laboratoire Génome et Populations, Université de Montpellier II. http://www.univ-montp2.fr/∼genetix

  • Bernatchez L, Guyomard R, Bonhomme F (1992) DNA sequence variation of the mitochondrial control region among geographically and morphologically remote European brown trout Salmo trutta populations. Mol Ecol 1:161–173

    PubMed  CAS  Google Scholar 

  • Cassens I, Van Waerebeek K, Best PB, Crespo EA, Reyes J, Milinkovitch MC (2003) The phylogeography of dusky dolphins (Lagenorhynchus obscurus): a critical examination of network methods and rooting procedures. Mol Ecol 12:1781–1792

    Article  PubMed  CAS  Google Scholar 

  • Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. TREE 15:290–295

    PubMed  Google Scholar 

  • Dollar ESJ (1998) Palaeofluvial geomorphology in southern Africa: a review. Prog Phys Geog 22:325–349

    Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Falk TM, Teugels GG, Abban EK, Villwock W, Renwrantz L (2003) Phylogeographic patterns in populations of the black-chinned tilapia complex (Teleostei, Cichlidae) from coastal areas in West Africa: support for the refuge zone theory. Mol Phylogenet Evol 27:81–92

    Article  PubMed  Google Scholar 

  • Gillmore KS (1978) A fisheries survey of Shashe Dam, Botswana. Unpublished report of the Department of Agriculture and Fisheries, Ministry of Agriculture, Gaborone Botswana, p 26

  • Goodman SJ (1997) Rst Calc: a collection of computer programs for calculating estimates of genetic differentiation from microsatellite data and a determining their significance. Mol Ecol 6:881–885

    Article  CAS  Google Scholar 

  • Gregg RE, Howard JH, Shonhiwa F (1998) Introgressive hybridization of tilapias in Zimbabwe. J Fish Biol 52:1–10

    Article  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Update from Goudet 1995. Available from http://www.unil.ch/izea/softwares/fstat.html.

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportions for multiple alleles. Biometrics 48:361–372

    Article  PubMed  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hey J, Won Y-J, Sivasundar A, Nielsen R, Market JA (2004) Using nuclear haplotypes with microsatellites to study gene flow between recently separated Cichlid species. Mol Ecol 13:909–919

    Article  PubMed  CAS  Google Scholar 

  • Joyce D, Lunt DH, Bills R, Turner GF, Katongo C, Duftner N, Sturmbauer C, Seehausen O (2005) An extant fish radiation␣emerged in an extinct Pleistocene Lake. Nature 435:90–94

    Article  PubMed  CAS  Google Scholar 

  • Klett V, Meyer A (2002) What, if anything, is a Tilapia? Mitochondrial ND2 phylogeny of Tilapiines and the evolution of parental care system in the African cichlid fishes. Mol Biol Evol 19:865–883

    PubMed  CAS  Google Scholar 

  • Kleynhans CJ, Hoffman A (1993) First record of Oreochromis macrochir (Boulenger, 1912) (Pisces: Cichlidae) from the Limpopo River in South Africa. SAJ Aquat Sci 18:104–107

    Google Scholar 

  • Kocher TD (2004) Adaptive evolution as explosive radiation: the cichlid fish model. Nature Rev Genet 5:288–298

    Article  CAS  Google Scholar 

  • Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: Molecular Evolutionary Genetics Analysis software. Bioinformatics 17:1244–1245

    Article  PubMed  CAS  Google Scholar 

  • Lee BY, Lee WJ, Streelman JT, Carleton KL, Howe AE, Hulata G, Slettan A, Stern JE, Terai Y, Kocher TD (2005) A second-generation genetic linkage map of tilapia (Oreochromis spp.). Genetics 170:237–244

    Article  PubMed  CAS  Google Scholar 

  • Lee WJ, Kocher TD (1996) Microsatellite DNA markers for genetic mapping in the tilapia, Oreochromis niloticus. J Fish Biol 49:169–171

    CAS  Google Scholar 

  • Meyer A, Kocher TD, Basasibwaki P, Wilson AC (1990) Monophyletic origin of lake Victoria cichlid fishes suggested by mitochondrial-DNA sequences. Nature 347:550–553

    Article  PubMed  CAS  Google Scholar 

  • Moralee RD, Van der Bank FH, Van der Waal BCW (2000) Biochemical genetic markers to identify hybrids between the endemic Oreochromis mossambicus and the alien species, O. niloticus (Pisces: Cichlidae). Water SA 26:263–268

    CAS  Google Scholar 

  • Nagl S, Tichy H, Mayer WE, Samonte IE, McAndrew BJ, Klein J (2001) Classification and phylogenetic relationships of African tilapiine fishes inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 20:361–374

    Article  PubMed  CAS  Google Scholar 

  • Nagl S, Tichy H, Mayer WE, Takezaki N, Takahata N, Klein J (2000) The origin and age of haplochromine fishes in Lake Victoria, East Africa. Proc R Soc Lond B Biol Sci 267:1049–1061

    Article  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): a population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rognon X, Guyomard R (2003) Large extent of mitochondrial DNA transfer from Oreochromis aureus to O-niloticus in West Africa. Mol Ecol 12:435–445

    Article  PubMed  CAS  Google Scholar 

  • Romana-Eguia MRR, Ikeda M, Basiao ZU, Taniguchi N (2004) Genetic diversity in farmed Asian Nile and red hybrid tilapia stocks evaluated from microsatellite and mitochondrial DNA analysis. Aquaculture 236:131–150

    Article  CAS  Google Scholar 

  • Salzburger C, Baric S, Sturmbauer C (2002) Speciation via introgressive hybridization in East African cichlids? Mol Ecol 11:619–625

    Article  PubMed  CAS  Google Scholar 

  • Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504

    Article  PubMed  CAS  Google Scholar 

  • Schwank EJ (1995) The introduced Oreochromis niloticus is spreading on the Kafue floodplain, Zambia. Hydrobiologia 315:143–147

    Google Scholar 

  • Seehausen O (2004) Hybridization and adaptive radiation. TREE 19:198–207

    PubMed  Google Scholar 

  • Seehausen O, Koetsier E, Schneider MV, Chapman LJ, Chapman CA, Knight ME, Turner GF, van Alphen JJM, Bills R (2003) Nuclear markers reveal unexpected genetic variation and a Congolese-Nilotic origin of the Lake Victoria cichlid species flock. Proc R Soc Lond B 270:129–137

    Article  Google Scholar 

  • Skelton P (1993) A complete guide to the freshwater fishes of Southern Africa. Southern Book Publishers, Halfway House, Harare

    Google Scholar 

  • Skelton P (2001) A complete guide to the freshwater fishes of Southern Africa. Struik, Cape Town

    Google Scholar 

  • Slatkin M (2005) Seeing ghosts: the effect of unsampled populations on migration rates estimated for sampled populations. Mol Ecol 14:67–73

    Article  PubMed  Google Scholar 

  • Stewart KM (2001) The freshwater fish of Neogene Africa (Miocene–Pleistocene): systematics and biogeography. Fish Fisheries 2:177–230

    Article  Google Scholar 

  • Sturmbauer C, Baric S, Salzburger W, Rüber L, Verheyen E (2001) Lake level fluctuations synchronize genetic divergences of cichlid fishes in African Lakes. Mol Biol Evol 18:144–154

    PubMed  CAS  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    PubMed  CAS  Google Scholar 

  • Trewavas E (1983) Tilapiine fishes of the genera Sarotherodon, Oreochromis and Danakilia. Cornell University Press, Ithaca New York, p 583

    Google Scholar 

  • Turner GF (2003) Oreochromis (Nyasalapia) karongae (Trewavas). http://malawicichlids.com/mw10001a.htm. In: “The Cichlid Fishes of Lake Malawi, Africa” (M. K. Oliver, webmaster), http://malawicichlids.com. Accessed September 2005

  • Tweddle D, Willoughby NG (1979) Part 2: An annotated checklist of the fish fauna of the river Shire south of Kapachira Falls, Malawi. Ichthyol Bull JLB Smith Inst Ichthyol 39:10–12

    Google Scholar 

  • Tweddle D, Lewis DSC (1979) Part1: the nature of the barrier separating the Lake Malawi and Zambezi fish faunas. Ichthyol Bull JLB Smith Instit Ichthyol 39:1–9

    Google Scholar 

  • Van Houdt JKJ, Pinceel J, Flamand M-C, Briquet M, Dupont E, Volkaert FAM, Baret PV (2005) Migration barriers protect indigenous brown trout (Salmo trutta) population from introgressions with stocked hatchery fish. Conserv Genet 6:175–191

    Article  Google Scholar 

  • Van der Waal BCW, Bills R (2000) Oreochromis niloticus (Teleostei: Cichlidae) now in the Limpopo River System. S Afr J Sci 96:47–48

    Google Scholar 

  • Waples RS, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439

    Article  PubMed  CAS  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Welcomme R (1967) Observations on the biology of the introduced species of Tilapia in Lake Victoria. Revue Zool Bot Afr 76:249–279

    Google Scholar 

  • Wohlfarth GW, Hulata GI (1981) Applied genetics of tilapias. ICLARM Stud Rev 6:1–26

    Google Scholar 

  • Yang ZH (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol 39:306–314

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This project was funded by the Department of International Development (DFID, UK) and benefited from a Bilateral Scientific Cooperation Grant between the Republic of South Africa—Flanders (Belgium) (Project BIL/00/30). H. Heyns of the farm Samaria is sincerely thanked for permission to collect samples, and G. Maes, D.␣Tweddle, J. Snoeks, two anonymous reviewers and Editor␣E. Nielsen for providing useful comments on the manuscript. We also thank N. Leat for critically reading the manuscript.

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  1. María Eugenia D’Amato

    Present address: Department of Biotechnology, University of the Western Cape, Private Bag X17, 7535, Bellville, Cape Town, South Africa

Authors and Affiliations

  1. Department of Genetics, University of Stellenbosch, Private Bag X1, 7602, Stellenbosch, South Africa

    María Eugenia D’Amato, Maria M. Esterhuyse & D. Brink

  2. Department of Biological Sciences, University of Venda, PO Bag X 5050, Thohoyandou, 0950, South Africa

    Ben C. W. van der Waal

  3. Laboratory of Aquatic Ecology, Katholieke Universiteit Leuven, Ch. Deberiotstraat 32, B-3000, Leuven, Belgium

    Filip A. M. Volckaert

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  1. María Eugenia D’Amato
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Correspondence to María Eugenia D’Amato.

Appendices

Appendices

Appendix 1 Variable sites of the 385 bp fragment of the mitochondrial control region among the 38 recognized Oreochromis haplotypes. The haplotype tags correspond to Table 3 and Fig. 3a
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Appendix 2 Average TrN93 + Γ genetic distance between clusters (below diago nal) and SE (above diagonal). On the diagonal: within group mean distance with SE between brackets
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Appendix 3 F st values (Weir and Cockerham 1984) and Nm between samples
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D’Amato, M.E., Esterhuyse, M.M., van der Waal, B.C. et al. Hybridization and phylogeography of the Mozambique tilapia Oreochromis mossambicus in southern Africa evidenced by mitochondrial and microsatellite DNA genotyping. Conserv Genet 8, 475–488 (2007). https://doi.org/10.1007/s10592-006-9186-x

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