Conservation Genetics

, Volume 12, Issue 1, pp 243–255 | Cite as

Genetic structure and gene flow in an endangered native tilapia fish (Oreochromis esculentus) compared to invasive Nile tilapia (Oreochromis niloticus) in Yala swamp, East Africa

  • Paul O. Angienda
  • Hyuk Je Lee
  • Kathryn R. Elmer
  • Romulus Abila
  • Eliud N. Waindi
  • Axel Meyer
Research Article

Abstract

The introduction of invasive Nile tilapia (Oreochromis niloticus), and the rapacious predator Nile perch (Lates niloticus), into Lake Victoria resulted in a decline in population sizes, genetic diversity and even extirpation of native species which were previously the mainstay of local fisheries. However, remnant populations of native fish species, including tilapia, still persist in satellite lakes around Lake Victoria where they may coexist with O. niloticus. In this study we assessed population genetic structure, diversity, and integrity of the native critically endangered Singidia tilapia (O. esculentus) in its refugial populations in the Yala swamp, Kenya, and contrasted this diversity with populations of the invasive tilapia O. niloticus in satellite lakes (Kanyaboli, Namboyo and Sare) and Lake Victoria. Based on mtDNA control region sequences and eight nuclear microsatellite loci, we did not detect any mtDNA introgression between the native and the invasive species in Lakes Kanyaboli and Namboyo, but did find low levels of nuclear admixture, primarily from O. niloticus to O. esculentus. Some genetic signal of O. esculentus in O. niloticus was found in Lake Sare, where O. esculentus is not found, suggesting it has recently been extirpated by the O. niloticus invasion. In both species, populations in the satellite lakes are significantly genetically isolated from each other, with private mtDNA haplotypes and microsatellite alleles. For O. niloticus, genetic diversity in satellite lakes was similar to that found in Lake Victoria. Our data imply a low frequency of immigration exchange between the two populations of O. esculentus and we suggest that the populations of this endangered species and important fisheries resource should be conserved separately in Lakes Kanyaboli and Namboyo and with high priority.

Keywords

Admixture Lake Victoria basin Nile tilapia Population genetic structure Singidia tilapia Yala swamp 

Notes

Acknowledgments

This research was funded by a German Academic Exchange Programme (DAAD) PhD scholarship to POA, an NSERC fellowship to KRE, and DFG grants to AM. We also thank the Maseno University School of Graduate Studies (SGS) for financial assistance. Much gratitude to Anton Omondi and Ben Aketch for assistance both in field and lab work and E. Hespeler for assistance in the lab.

References

  1. Abila R, Barluenga M, Engelken J, Meyer A, Salzburger W (2004) Population-structure and genetic diversity in a haplochromine fish cichlid of a satellite lake of Lake Victoria. Mol Ecol 13:2589–2602CrossRefPubMedGoogle Scholar
  2. Abila R, Salzburger W, Ndonga MF, Owiti DO, Barluenga M, Meyer A (2008) The role of the Yala swamp lakes in the conservation of Lake Victoria region haplochromine cichlids: evidence from genetic and trophic ecology studies. Lakes Reservoirs: Res Manage 13:95–104CrossRefGoogle Scholar
  3. Agnèse JF, Adépo-Gourène B, Pouyaud L (1998) Natural hybridization in tilapias. In: Agnèse JF (ed) Genetics and aquaculture in Africa. ORSTOM, Paris, pp 125–133Google Scholar
  4. Agnèse JF, Adépo-Gourène B, Owino J, Pouyaud L, Aman R (1999) Genetic characterization of a relict population of Oreochromis esculentus, an endangered tilapia. J Fish Biol 54:1119–1123Google Scholar
  5. Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell Publishing Ltd, Oxford, UKGoogle Scholar
  6. Aloo PO (2003) Biological diversity of the Yala Swamp lakes, with special emphasis on fish species composition, in relation to changes in the Lake Victoria Basin (Kenya): threats and conservation measures. Biodivers Conserv 12:905–920CrossRefGoogle Scholar
  7. Balirwa JS, Chapman CA, Chapman LJ, Cowx IG, Heheb K, Kaufman L, Lowe-McConnell RH, Seehausen O, Wanink JH, Welcomme RL, Witte F (2003) Biodiversity and fishery sustainability in the Lake Victoria basin: an unexpected marriage? Bioscience 53:703–715CrossRefGoogle Scholar
  8. Barel CDN, Dorit R, Greenwood PH, Fryer G, Hughes N, Jackson PBN, Kawanabe H, Lowe-McConnell RH, Nagoshi M, Ribbink AJ et al (1985) Destruction of fisheries in Africa’s Lakes. Nature 315:19–20CrossRefGoogle Scholar
  9. Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Annu Rev Ecol Syst 16:113–148CrossRefGoogle Scholar
  10. Batjakas IE, RKand Edgar, Kaufman LS (1997) Comparative feeding efficiency of indigenous and introduced phytoplanktivores from Lake Victoria: experimental studies on Oreochromis esculentus and Oreochromis niloticus. Hydrobiologia 347:75–82CrossRefGoogle Scholar
  11. Beauchamp RSA (1958) Utilising the natural resources of Lake Victoria for the benefit of fisheries and agriculture. Nature 181:1634–1636CrossRefGoogle Scholar
  12. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996) Genetix 4.05, logiciel sous Windows pour la génétique de populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000. Université de Montpellier II, Montpellier, FranceGoogle Scholar
  13. Bishop WW, Trendall AF (1966) Erosion-surfaces, tectonics and volcanic activity in Uganda. Quart J Geol Soc 122:385–420CrossRefGoogle Scholar
  14. Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5:453–455PubMedGoogle Scholar
  15. Bruford MW, Hanotte O, Brookfield JFY, Burke T (1998) Multilocus and single locus DNA fingerprinting. In: Hoelzel AR (ed) Molecular genetics analysis of populations: a practical approach. Oxford University Press, Oxford, pp 287–336Google Scholar
  16. Canonico CG, Arthington A, McCrary JK, Thieme ML (2005) The effect of introduced tilapias on native biodiversity. Aquat Conserv: Mar Freshwat Ecosyst 15:463–483CrossRefGoogle Scholar
  17. Chapman LJ, Chapman CA, Nordlie FG, Rosenberger AE (2002) Physiological refugia: swamps, hypoxia tolerance and maintenance of fish diversity in the Lake Victoria region. Comp Biochem Physiol A 133:421–437CrossRefGoogle Scholar
  18. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefPubMedGoogle Scholar
  19. Crafter SA, Njuguna SG, Howard GW (1992) Wetlands of Kenya. In: Proceedings of the KWWG Seminar on Wetlands of Kenya. National Museums of Kenya. Nairobi, Kenya, 3–5 July 1991, IUCNGoogle Scholar
  20. Crandall KA, Templeton AR (1993) Empirical tests of some predictions from coalescent theory with applications to intra-specific phylogeny reconstruction. Genetics 134:959–969PubMedGoogle Scholar
  21. Crispo E, Chapman LJ (2008) Population genetic structure across dissolved oxygen regimes in an African cichlid fish. Mol Ecol 17:2134–2148CrossRefPubMedGoogle Scholar
  22. D’Amato ME, Esterhuyse MM, van der Waal BCW, Brink D, Volckaert FAM (2007) Hybridization and phylogeography of the Mozambique tilapia Oreochromis mossambicus in southern Africa evidenced by mitochondrial and microsatellite DNA genotyping. Conserv Genet 8:475–488CrossRefGoogle Scholar
  23. Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504–509CrossRefPubMedGoogle Scholar
  24. EAFFRO (1964) East African Freshwater Fisheries Research Organization (EAFFR)–annual report for 1962/63. East African Common Services Organization, Jinja, UgandaGoogle Scholar
  25. Elmer KR, Van Houdt JK, Meyer A, Volckaert FAM (2008) Population genetics of North American burbot (Lota lota maculosa) across the Nearctic and at its contact zone with Eurasian burbot (Lota lota lota). Can J Fish Aquat Sci 65:2412–2426CrossRefGoogle Scholar
  26. Elmer KR, Reggio C, Wirth T, Verheyen E, Salzburger W, Meyer A (2009) Pleistocene desiccation in East Africa bottlenecked but did not extirpate the adaptive radiation of Lake Victoria haplochromine cichlid fishes. Proc Natl Acad Sci USA 106:13404–13409CrossRefPubMedGoogle Scholar
  27. Ewens WJ (1972) The sampling theory of selectively neutral haplotypes. Theor Pop Biol 3:87–112CrossRefGoogle Scholar
  28. Excoffier L, Laval G, Schneider S (2005) ARLEQUIN, version 3: an intergrated software package for population genetics data analysis. Evol Bioinform online 1:47–50PubMedGoogle Scholar
  29. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedGoogle Scholar
  30. Frankham R, Ballou JD, Briscoe DA (2004) A primer of conservation genetics. Cambridge University Press, New YorkGoogle Scholar
  31. Genner MJ, Nichols P, Carvalho GR, Robinson RL, Shaw PW, Smith A, Turner GF (2007) Evolution of a cichlid fish in a Lake Malawi satellite lake. Proc R Soc Lond B 22:2249–2257CrossRefGoogle Scholar
  32. Goudswaard PC, Witte F, Katunzi EFB (2002) The tilapiine fish stock of Lake Victoria before and after the Nile perch upsurge. J Fish Biol 60:838–856CrossRefGoogle Scholar
  33. Hänfling B (2007) Understanding the establishment success of non-indigenous fishes: lessons from population genetics. J Fish Biol 71(Supplement D):115–135CrossRefGoogle Scholar
  34. Hauser L, Adcock GJ, Smith PJ, Ramírez JHB, Carvalho GR (2002) Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proc Natl Acad Sci USA 18:11742–11747CrossRefGoogle Scholar
  35. Herborg LM, Weetman D, Oosterhout CV, Hänfling B (2007) Genetic population structure and contemporary dispersal patterns of a recent European invader, the Chinese mitten crab, Eriocheir sinensis. Mol Ecol 16:231–242CrossRefPubMedGoogle Scholar
  36. Jembe BT, Boera PN, Okeyo Owuor JB (2006) Distribution and association of Tilapine unit stocks in the Lake Victoria catchment (Kenya). In: Odada E, Olago DO (eds) Proceedings of the 11th World Lakes Conference. Ministry of Water and Irrigation, Nairobi, Kenya, pp 210–216Google Scholar
  37. Johnson TC, Scholz CA, Talbot MR, Kelts K, Ricketts RD, Ngobi G, Beuning K, Ssemmanda I, McGill JW (1996) Late Pleistocene desiccation of Lake Victoria and rapid evolution of cichlid fishes. Science 273:1091–1093CrossRefPubMedGoogle Scholar
  38. Kaufman LS (1992) Catastrophic change in species-rich fresh water ecosystems: the lessons of Lake Victoria. Bioscience 42:846–858CrossRefGoogle Scholar
  39. Kaufman LS, Ochumba P (1993) Evolutionary and conservation biology of cichlid fishes as revealed by faunal remnants in northern Lake Victoria. Conserv Biol 7:719–730CrossRefGoogle Scholar
  40. Klett V, Meyer A (2002) What, if anything, is a tilapia? Mitochondrial ND2 phylogeny of tilapiines and the evolution of parental care systems in the African cichlid fishes. Mol Biol Evol 19:865–883PubMedGoogle Scholar
  41. Kudhongania AW, Cordone AJ (1974) Batho-spatial distribution pattern and biomass estimate of the major demersal fishes in Lake Victoria. Afr J Trop Hydrobiol Fish 3:15–31Google Scholar
  42. Loiselle PV (1996) ‘Fulu’ of the Yala Swamp–part I: overview of the fishes. Cichlid News 5:11–18Google Scholar
  43. Lowe-McConnell RH (2000) The roles of tilapias in ecosystems. In: Beveridge MCM, Andrews BJ (eds) Tilapias: biology and exploitation. Kluwer Press, Dordrecht, pp 129–162Google Scholar
  44. Maithya J (1998) A survey of ichthyofauna of Lake Kanyaboli and other small water bodies in Kenya: alternative refugia for endangered fish species. Naga, the ICLARM Quarterly 1:54–56Google Scholar
  45. Mavuti KM (1989) An account of some important freshwater wetlands of Kenya. In: Crafter SA, Njuguna SG, Howard GW (eds) IUCN Conference Proceedings on Wetlands of Kenya. IUCN, pp 23–35Google Scholar
  46. Meyer A, Morrissey JM, Schartl M (1994) Recurrent origin of a sexually selected trait in Xiphophorous fishes inferred from molecular phylogeny. Nature 368:539–542CrossRefPubMedGoogle Scholar
  47. Mwanja WW (2004) The role of satellite water bodies in the evolution and conservation of Lake Victoria Region fishes. Afr J Ecol 42:14–20CrossRefGoogle Scholar
  48. Mwanja WW, Kaufman L (1995) A note on recent advances in the genetic characterization of tilapia stocks in Lake Victoria region. Afr J Trop Hydrobiol Fish 6:51–53Google Scholar
  49. Mwanja WW, Armoudlian AS, Wandera SB, Kaufman L, Wu L, Booton GC, Fuerst PA (2001) The bounty of minor lakes: the role of small water bodies in evolution and conservation of fishes in the Lake Victoria Region, East Africa. Hydrobiologia 458:55–62CrossRefGoogle Scholar
  50. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Proc Natl Acad Sci USA 70:3321–3323CrossRefGoogle Scholar
  51. O’ Connell M, Wright JM (1997) Microsatellite DNA in fishes. Rev Fish Biol Fish 7:331–363CrossRefGoogle Scholar
  52. Ogutu-Ohwayo R (1990) The decline of native fish of Lake Victoria and Kyoga (East Africa) and the impact of the introduced species, especially the Nile perch, Lates niloticus and the Nile tilapia, Oreochromis niloticus. Environ Biol Fishes 27:81–96CrossRefGoogle Scholar
  53. Okumus I, Çiftci Y (2003) Fish population genetics and molecular markers: II-molecular markers and their applications in fisheries and aquaculture. Turk J Fish Aquat Sci 3:51–79Google Scholar
  54. Opiyo SV (1991) Feeding ecology of Oreochromis esculentus (Graham) (Pisces: Cichlidae) in Lake Kanyaboli, Kenya. MSc thesis, University of NairobiGoogle Scholar
  55. Pringle RM (2005) The origins of the Nile Perch in Lake Victoria. Bioscience 55:780–788CrossRefGoogle Scholar
  56. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  57. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283CrossRefGoogle Scholar
  58. Redenbach Z, Taylor EB (2003) Evidence for bimodal hybrid zones between two species of char (Pisces: Salvelinus) in northwestern North America. J Evol Biol 16:1135–1148CrossRefPubMedGoogle Scholar
  59. Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106CrossRefGoogle Scholar
  60. Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies. Trends Ecol Evol 1:9–10CrossRefGoogle Scholar
  61. Sanetra M, Henning F, Fukamachi S, Meyer A (2009) A microsatellite-based genetic linkage map of the cichlid fish, Astatotilapia burtoni (Teleostei): a comparison of genomic architectures among rapidly speciating cichlids. Genetics 182:1–11CrossRefGoogle Scholar
  62. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analyses with cladogram uncertainty and recombination. Genetics 134:659–669Google Scholar
  63. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 11:4673–4680CrossRefGoogle Scholar
  64. Trewavas E (1983) Tilapiine fishes of the genera Sarotherodon, Oreochromis and Danakilia. Brit Museum Nat Hist, LondonGoogle Scholar
  65. Twongo T (1995) Impact of fish species introductions on the tilapias of Lakes Victoria and Kyoga. In: Pitcher TJ, Hart PJB (eds) The impact of species changes in African lakes. Chapman and Hall, London, pp 47–57Google Scholar
  66. Twongo TK, Bayona JDR, Hanssens M (2006) Oreochromis esculentus. In: IUCN 2010. IUCN Red List of Threatened Species. Version 2010.2. www.iucnredlist.org. Accessed 15 Aug 2010
  67. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  68. Weir BS, Cockerham CC (1984) Estimating F–statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  69. Witte F, Goldschmidt T, Goudswaard PC, Ligtvoet W, Van Oijen MJP, Wanink JH (1992a) Species introduction and concomitant ecological changes in Lake Victoria. Neth J Zool 42:214–232CrossRefGoogle Scholar
  70. Witte F, Goldschmidt T, Wanink J, Van Oijen M, Goudswaard K, Witte-Maas E, Bouton N (1992b) The destruction of an endemic species flock: quantitative data on the decline of the haplochromine cichlids of Lake Victoria. Environ Biol Fishes 34:1–28CrossRefGoogle Scholar
  71. Zidana H, Turner GF, Van Oosterhout C, Hänfling B (2009) Elevated mtDNA diversity in introduced populations of Cynotilapia afra (Günther 1894) in Lake Malawi National Park is evidence for multiple source populations and hybridization. Mol Ecol 18:4380–4389CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Paul O. Angienda
    • 1
    • 2
  • Hyuk Je Lee
    • 2
  • Kathryn R. Elmer
    • 2
  • Romulus Abila
    • 3
  • Eliud N. Waindi
    • 1
  • Axel Meyer
    • 2
  1. 1.Department of ZoologyMaseno UniversityMasenoKenya
  2. 2.Lehrstuhl für Zoologie und Evolutionsbiologie, Department of BiologyUniversity of KonstanzKonstanzGermany
  3. 3.Department of Hydrology and Water Resources ManagementSouth Eastern University CollegeKituiKenya

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