Species integrity and origin of Oreochromis hunteri (Pisces: Cichlidae), endemic to crater Lake Chala (Kenya–Tanzania)

  • Jorunn Dieleman
  • Moritz Muschick
  • Wanja Dorothy Nyingi
  • Dirk Verschuren
ADVANCES IN CICHLID RESEARCH III

Abstract

Extensive transfer of tilapia between lakes throughout East Africa has often led to hybridisation with indigenous fish populations. The endemic Oreochromis hunteri of Lake Chala, an isolated crater lake near Mount Kilimanjaro, is potentially susceptible to introgression from a species formerly identified as Oreochromis korogwe, introduced ~ 30 years ago. We combined whole-body geometric morphometry on 104 specimens of both taxa with molecular phylogenetic analysis of mitochondrial loci from 15 O. hunteri and 9 O. cf. korogwe specimens to assess whether hybridisation has occurred. Using fishes from Lake Jipe and Nyumba ya Mungu reservoir, we expanded our analysis to all four Oreochromis species currently inhabiting the Upper Pangani River system to determine the closest relative of O. hunteri, and hence the possible source population of the ancestral species that colonised Lake Chala. Our results indicate no interbreeding occurs between O. hunteri and O. cf. korogwe, and suggest O. jipe to be the closest living relative of O. hunteri. The introduced O. cf. korogwe is a phenotypically uniform but genetically variable population, the identity of which remains unknown. The high haplotype diversity of O. hunteri is consistent with fossil evidence indicating that its ancestor colonised Lake Chala at least 25,000 years ago.

Keywords

Introgression Colonisation Crater lake Cichlids Geometric morphometrics 

Notes

Acknowledgements

This study was carried out under Memorandum of Understanding A14/TT/0923 between Ghent University and the National Museums of Kenya (NMK), and institutional affiliation of DV with NMK. We thank Caxton Oluseno and the fishermen of lakes Chala and Jipe for assistance in acquiring fish specimens for this study, and the staff of the NERC Biomolecular Analysis Facility and the Nosil lab, both at the University of Sheffield, for support. We further thank three anonymous reviewers for their suggestions to improve this manuscript. This research was sponsored by the Ghent University Special Research Fund through Collaborative Research Activity ‘DeepCHALLA’, including PhD support to JD. MM received support from the Swiss National Science Foundation, the University of Sheffield, and the International Continental Scientific Drilling Program. The Euler HPC cluster at ETH Zürich was used for phylogenetic analyses. We thank Michael Matschiner for advice on the program Fitchi. The mitochondrial CR and ND2 sequences produced by this study are accessible through GenBank, and vouchers of all sequenced fish specimens will be archived at NMK.

Supplementary material

10750_2018_3570_MOESM1_ESM.docx (28 kb)
Supplementary material 1 (DOCX 27 kb)

References

  1. Agnèse, J., B. Adépo-Gourène & L. Pouyaud, 1997. Natural hybridization in tilapias. In Agnèse, J. F. (ed.), Genetics and Aquaculture in Africa. ORSTOM, Paris: 95–103.Google Scholar
  2. Angienda, P. O., H. J. Lee, K. R. Elmer, R. Abila, E. N. Waindi & A. Meyer, 2011. 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. Conservation Genetics 12: 243–255.CrossRefGoogle Scholar
  3. Bailey, R. G., S. Churchfield, T. Petr & R. Pimm, 1978. The ecology of the fishes in Nyumba ya Mungu reservoir, Tanzania. Biological Journal of the Linnean Society 10: 109–137.CrossRefGoogle Scholar
  4. Barluenga, M. & A. Meyer, 2010. Phylogeography, colonization and population history of the Midas cichlid species complex (Amphilophus spp.) in the Nicaraguan crater lakes. BMC Evolutionary Biology 10: 326.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Barluenga, M., K. N. Stölting, W. Salzburger, M. Muschick & A. Meyer, 2006. Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439: 719–723.CrossRefPubMedGoogle Scholar
  6. Beveridge, M. C. & B. McAndrew, 2000. Tilapias: Biology and Exploitation. Springer Science & Business Media, Dordrecht.CrossRefGoogle Scholar
  7. Blaauw, M., B. van Geel, I. Kristen, B. Plessen, A. Lyaruu, D. R. Engstrom, J. van der Plicht & D. Verschuren, 2011. High-resolution 14C dating of a 25,000-year lake-sediment record from equatorial East Africa. Quaternary Science Reviews 30: 3043–3059.CrossRefGoogle Scholar
  8. Bouckaert, R., J. Heled, D. Kühnert, T. Vaughan, C. H. Wu, D. Xie, M. A. Suchard, A. Rambaut & A. J. Drummond, 2014. BEAST 2: a software platform for bayesian evolutionary analysis. PLoS Computational Biology 10: e1003537.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Crispo, E., J. S. Moore, J. A. Lee-Yaw, S. M. Gray & B. C. Haller, 2011. Broken barriers: human-induced changes to gene flow and introgression in animals. BioEssays 33: 508–518.CrossRefPubMedGoogle Scholar
  10. D’Amato, M. E., M. M. Esterhuyse, B. C. W. Van Der Waal, D. Brink & F. A. M. Volckaert, 2007. Hybridization and phylogeography of the Mozambique tilapia Oreochromis mossambicus in southern Africa evidenced by mitochondrial and microsatellite DNA genotyping. Conservation Genetics 8: 475–488.CrossRefGoogle Scholar
  11. Dadzie, S., R. D. Haller & E. Trewavas, 1988. A note on the fishes of Lake Jipe and Lake Chale on the Kenya–Tanzania border. Journal of East African Natural History 192: 46–51.Google Scholar
  12. Darriba, D., G. L. Taboada, R. Doallo & D. Posada, 2012. JModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Deines, A. M., I. Bbole, C. Katongo, J. L. Feder & D. M. Lodge, 2014. Hybridisation between native Oreochromis species and introduced Nile tilapia O. niloticus in the Kafue River, Zambia. African Journal of Aquatic Science 39: 23–34.CrossRefGoogle Scholar
  14. Denny, P., 1978. Nyumba ya Mungu reservoir, Tanzania, the general features. Biological Journal of the Linnean Society 10: 5–28.CrossRefGoogle Scholar
  15. Dieleman, J., B. Van Bocxlaer, C. Manntschke, D. W. Nyingi, D. Adriaens & D. Verschuren, 2015. Tracing functional adaptation in African cichlid fishes through morphometric analysis of fossil teeth: exploring the methods. Hydrobiologia 755: 73–88.CrossRefGoogle Scholar
  16. Drummond, A. J. & R. R. Bouckaert, 2015. Bayesian Evolutionary Analysis with BEAST 2. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  17. Drummond, A. J., A. Rambaut, B. Shapiro & O. G. Pybus, 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution 22: 1185–1192.CrossRefPubMedGoogle Scholar
  18. Eknath, A. E. & G. Hulata, 2009. Use and exchange of genetic resources of Nile tilapia (Oreochromis niloticus). Reviews in Aquaculture 1: 197–213.CrossRefGoogle Scholar
  19. Elmer, K. R., T. K. Lehtonen, S. Fan & A. Meyer, 2012. Crater lake colonization by neotropical cichlid fishes. Evolution 67: 281–288.CrossRefPubMedGoogle Scholar
  20. Excoffier, L., G. Laval & S. Schneider, 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47–50.Google Scholar
  21. Firmat, C., P. Alibert, M. Losseau, J. F. Baroiller & U. K. Schliewen, 2013. Successive invasion-mediated interspecific hybridizations and population structure in the endangered cichlid Oreochromis mossambicus. PLoS ONE 8: e63880.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fryer, G. & T. D. Iles, 1972. The Cichlid Fishes of the Great Lakes of Africa, their Biology and Distribution. Oliver and Boyd, Edinburgh.Google Scholar
  23. Genner, M. J. & G. F. Turner, 2014. Timing of population expansions within the Lake Malawi haplochromine cichlid fish radiation. Hydrobiologia 748: 121–132.CrossRefGoogle Scholar
  24. Genner, M. J., M. E. Knight, M. P. Haesler & G. F. Turner, 2010. Establishment and expansion of Lake Malawi rock fish populations after a dramatic Late Pleistocene lake level rise. Molecular Ecology 19: 170–182.CrossRefPubMedGoogle Scholar
  25. Grant, W. S., 2015. Problems and cautions with sequence mismatch analysis and Bayesian skyline plots to infer historical demography. Journal of Heredity 106: 333–346.CrossRefPubMedGoogle Scholar
  26. Günther, A., 1889. On some fishes from the Kilima-Njaro district. Proceedings of the Scientific Meetings of the Zoological Society of London for the Year 1889: 70–72.Google Scholar
  27. Håkansson, N. T., 2008. The decentralized landscape: regional wealth and the expansion of production in northern Tanzania before the eve of colonialism. In Cliggett, L. & C. A. Pool (eds.), Economies and the Transformation of Landscape. AltaMira Press, Creek: 239–266.Google Scholar
  28. Hammer, Ø., D. A. T. Harper & P. D. Ryan, 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1): 1–9.Google Scholar
  29. Hasegawa, M., H. Kishino & T. A. Yano, 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22: 160–174.CrossRefPubMedGoogle Scholar
  30. Holzman, R. & C. D. Hulsey, 2017. Mechanical transgressive segregation and the rapid origin of trophic novelty. Scientific Reports 7: 40306.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Klett, V. & A. Meyer, 2002. What, if anything, is a Tilapia? Mitochondrial ND2 phylogeny of tilapiines and the evolution of parental care systems in the African cichlid fishes. Molecular Biology and Evolution 19: 865–883.CrossRefPubMedGoogle Scholar
  32. Kocher, T. D., J. A. Conroy, K. R. McKaye, J. R. Stauffer & S. F. Lockwood, 1995. Evolution of NADH dehydrogenase subunit 2 in east African cichlid fish. Molecular Phylogenetics and Evolution 4(4): 420–432.CrossRefPubMedGoogle Scholar
  33. Lee, W. J., J. Conroy, W. H. Howell & T. D. Kocher, 1995. Structure and evolution of teleost mitochondrial control regions. Journal of Molecular Evolution 41: 54–66.CrossRefPubMedGoogle Scholar
  34. Lowe, R. H., 1955. New species of Tilapia (Pisces, Cichlidae) from Lake Jipe and the Pangani River, East Africa. Bulletin of the British Museum (Natural History) Zoology 2(12): 349–368.Google Scholar
  35. Lowe-McConnell, R. H., 1987. Ecological Studies in Tropical Fish Communities. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  36. Martinsen, G. D., T. G. Whitham, R. J. Turek & P. Keim, 2001. Hybrid populations selectively filter gene introgression between species. Evolution 55: 1325–1335.CrossRefPubMedGoogle Scholar
  37. Matschiner, M., 2016. Fitchi: haplotype genealogy graphs based on the Fitch algorithm. Bioinformatics 32: 1250–1252.CrossRefPubMedGoogle Scholar
  38. Meier, J. I., D. A. Marques, S. Mwaiko, C. E. Wagner, L. Excoffier & O. Seehausen, 2017. Ancient hybridization fuels rapid cichlid fish adaptive radiations. Nature Communications 8: 14363.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Meyer, A., J. M. Morrissey & M. Schartl, 1994. Recurrent origin of a sexually selected trait in Xiphophorus fishes inferred from a molecular phylogeny. Nature 368: 539–542.CrossRefPubMedGoogle Scholar
  40. Moernaut, J., D. Verschuren, F. Charlet, I. Kristen, M. Fagot & M. De Batist, 2010. The seismic-stratigraphic record of lake-level fluctuations in Lake Challa: hydrological stability and change in equatorial East Africa over the last 140 kyr. Earth and Planetary Science Letters 290: 214–223.CrossRefGoogle Scholar
  41. Nagl, S., H. Tichy, W. E. Mayer, I. E. Samonte, B. J. McAndrew & J. Klein, 2001. Classification and phylogenetic relationships of African tilapiine fishes inferred from mitochondrial DNA sequences. Molecular phylogenetics and evolution 20: 361–374.CrossRefPubMedGoogle Scholar
  42. Ndiwa, T. C., D. W. Nyingi & J. F. Agnese, 2014. An important natural genetic resource of Oreochromis niloticus (Linnaeus, 1758) threatened by aquaculture activities in Loboi Drainage, Kenya. PLoS ONE 9: e106972.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Nyingi, D. W. & J. F. Agnèse, 2007. Recent introgressive hybridization revealed by exclusive mtDNA transfer from Oreochromis leucostictus (Trewavas, 1933) to Oreochromis niloticus (Linnaeus, 1758) in Lake Baringo, Kenya. Journal of Fish Biology 70: 148–154.CrossRefGoogle Scholar
  44. Parnell, N. F., C. D. Hulsey & J. T. Streelman, 2012. The genetic basis of a complex functional system. Evolution 66: 3352–3366.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Pullin, R.S & R.H. Lowe-McConnell, 1982. The biology and culture of tilapias. Proceedings of the International Conference on the Biology and Culture of Tilapias, 2–5 September 1980 at the Study and Conference Center of the Rockefeller Foundation, Bellagio, (Vol. 7). WorldFish, 1982: 426–432.Google Scholar
  46. R Development Core Team, 2016. R: A Language and Environment for Statistical Computing. Foundation for Statistical Computing, Vienna.Google Scholar
  47. Rambaut, A., 2009. FigTree v1. 3.1: Tree Figure Drawing Tool. Website: http://tree.bio.ed.ac.uk/software/figtree.
  48. Rognon, X. & R. Guyomard, 2003. Large extent of mitochondrial DNA transfer from Oreochromis aureus to O. niloticus in West Africa. Molecular Ecology 12: 435–445.CrossRefPubMedGoogle Scholar
  49. Rohlf, F. J., 2010. TpsDig2: Thin Plate Spline Digitise (Version 2.16). Stony Brook University, New York.Google Scholar
  50. Salzburger, W., S. Baric & C. Sturmbauer, 2002. Speciation via introgressive hybridization in East African cichlids? Molecular Ecology 11: 619–625.CrossRefPubMedGoogle Scholar
  51. Seegers, L., L. De Vos & D. O. Okeyo, 2003. Annotated checklist of the freshwater fishes of Kenya (excluding the lacustrine haplochromines from Lake Victoria). Journal of East African Natural History 92: 11–47.CrossRefGoogle Scholar
  52. Sheets, H. D., 2008. IMP: Integrated Morphometrics Package. Department of Physics, Canisius College, Buffalo.Google Scholar
  53. Stamatakis, A., 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Stelkens, R. B. & O. Seehausen, 2009. Phenotypic divergence but not genetic distance predicts assortative mating among species of a cichlid fish radiation. Journal of Evolutionary Biology 22: 1679–1694.CrossRefPubMedGoogle Scholar
  55. Stelkens, R. B., K. A. Young & O. Seehausen, 2010. The accumulation of reproductive incompatibilities in African cichlid fish. Evolution 64: 617–633.CrossRefPubMedGoogle Scholar
  56. Trewavas, E., 1983. Tilapiine Fishes of the Genera Sarotherodon, Oreochromis and Danakilia. British Museum (Natural History), London.CrossRefGoogle Scholar
  57. Verschuren, D., J. S. Sinninghe Damsté, J. Moernaut, I. Kristen, M. Blaauw, M. Fagot & G. H. Haug, 2009. Half-precessional dynamics of monsoon rainfall near the East African Equator. Nature 462: 637–641.CrossRefPubMedGoogle Scholar
  58. Wirtz, P., 1999. Mother species-father species: unidirectional hybridization in animals with female choice. Animal Behaviour 58: 1–12.CrossRefPubMedGoogle Scholar
  59. Wolff, C., I. Kristen-Jenny, G. Schettler, B. Plessen, H. Meyer, P. Dulski, R. Naumann, A. Brauer, D. Verschuren & G. H. Haug, 2014. Modern seasonality in Lake Challa (Kenya/Tanzania) and its sedimentary documentation in recent lake sediments. Limnology and Oceanography 59: 1621–1636.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Limnology Unit, Department of BiologyGhent UniversityGhentBelgium
  2. 2.Department of Animal and Plant SciencesUniversity of SheffieldSheffieldUK
  3. 3.Aquatic Ecology & Evolution, Institute of Ecology and EvolutionUniversity of BernBernSwitzerland
  4. 4.Department of Fish Ecology & EvolutionEAWAG, Swiss Federal Institute for Aquatic Science and TechnologyKastanienbaumSwitzerland
  5. 5.Ichthyology Section, Zoology DepartmentNational Museums of KenyaNairobiKenya

Personalised recommendations