Journal of Molecular Evolution

, Volume 60, Issue 3, pp 277–289 | Cite as

Evolutionary Relationships of the Limnochromini, a Tribe of Benthic Deepwater Cichlid Fish Endemic to Lake Tanganyika, East Africa

  • Nina Duftner
  • Stephan Koblmüller
  • Christian Sturmbauer


Lake Tanganyika harbors an enormous diversity of cichlid fish that stem from eight distinct ancestral lineages, which colonized the lake after its formation 9 to 12 million years ago. Six of twelve currently described tribes are assigned to the “H-lineage,” an assemblage of exclusively mouthbrood-ing cichlids, all of which evolved during a short period of time during the course of the primary radiation of lacustrine species. Our study focuses on the deepwater tribe Limnochromini, comprising bi-parental mouthbrooders, and is based on phylogenetic analysis of two mitochondrial gene segments. We confirm the polyphyletic origin of the Limnochromini as they are defined to date, in that Gnathochromis pfefferi is placed among the Tropheini, whereas the genus Benthochromis is presented as an independent lineage. The remaining nine species were unambiguously resolved as monophyletic and should be redefined as the tribe Limnochromini. Concerning generic assignments, the genus Greenwoodochromis appeared as monophyletic, Limnochromis as paraphyletic, and the genera Reganochromis and Baileychromis as monophyletic sister genera. The linearized tree analysis and the comparison of average sequence divergences to that of the remaining tribes of the H-lineage revealed a relatively recent but simultaneous proliferation of the Limnochromini, suggesting that the same environmental changes triggered the radiation of particular deepwater, benthic, pelagic, and littoral lineages. By using a preliminary calibration of a molecular clock based on gamma-corrected amino acid distances of the NADH2 gene, the diversification of the Limnochromini could tentatively be dated to 2.9–3.5 MYA, coinciding with a period of aridification in East Africa between 2.5 and 3 MYA. The lack of geographic color morphs and the structural uniformity and resource scarcity of deepwater habitats suggest that competition and resource partitioning leading to differential trophic specialization promoted speciation within the Limnochromini, rather than an allopatric model.


Adaptive radiation Control region NADH dehydrogenase subunit 2 Explosive speciation Niche partitioning Molecular clock 



We thank C. Kapasa, P. Ngalande, H. Phiri, L. Makasa, R. Sinyinza, D. Sinyinza, and the team at the Mpulungu Station of the Ministry of Agriculture, Food and Fisheries, Republic of Zambia, as well as L. Mumba, G. Mutenda, and C. Katongo, of the University of Zambia in Lusaka for their cooperation during fieldwork. We are grateful to J. Snoeks, of the Royal Africa Museum in Tervuren (Belgium), for species identification. Thanks go to M. Nishida, Y. Terai, and N. Okada, who provided an important fish sample. We thank K. Sefc, S. Weiss, and three anonymous reviewers for critical reading of early versions of the manuscript. N.D., S.K., and C.S. were supported by the Austrian Science Foundation (Grant P15239). N.D. and S.K. were further supported by the University of Graz. N.D. received a DOC-FFORTE (Women in Research and Technology) fellowship and S.K. a DOC fellowship, both provided by the Austrian Academy of Sciences.


  1. Adachi, J, Hasegawa, M 1996Model of amino acid substitution in proteins encoded by mitochondrial DNAJ Mol Evol42459468PubMedGoogle Scholar
  2. Baric, S, Salzburger, W, Sturmbauer, C 2003Phylogeography and evolution of the Tanganyikan cichlid genus Tropheus based upon mitochondrial DNA sequencesJ Mol Evol565468PubMedGoogle Scholar
  3. Brandstätler A, Salzburger W, Sturmbauer C (2005) Mitochondrial phylogeny of the Cyprichromini, a lineage of open-water cichlid fishes endemic to Lake Tanganyika, East Africa. Mol Phylogenet Evol. In pressGoogle Scholar
  4. Cane, MA, Molnar, P 2001Closing of the Indonesian seaway as a precursor to east African aridification around 3–4 million years agoNature411157162PubMedGoogle Scholar
  5. Cohen, AS, Soreghan, MJ 1993Estimating the age of ancient lakes: An example from Lake Tanganyika, East African rift systemGeology21511514CrossRefGoogle Scholar
  6. Cohen, AS, Lezzar, KE, Tiercelin, JJ, Soreghan, M 1997New palaeographic and lake-level reconstructions of Lake Tanganyika: Implications for tectonic, climatic and biological evolution in a rift lakeBasin Res9107132Google Scholar
  7. Coulter, GW 1991Lake Tanganyika and its lifeOxford University PressOxfordGoogle Scholar
  8. Danley, PD, Kocher, TD 2001Speciation in rapidly diverging systems: Lessons from Lake MalawiMol Ecol1010751086PubMedGoogle Scholar
  9. Delvaux, D 1995Age of Lake Malawi (Nyasa) and water level fluctuationsMus R Afr Centr Tervuren (Belg) Dept Geol Min Rapp Ann1995–199699108Google Scholar
  10. Fryer, G, Iles, TD 1972The cichlid fishes of the great lakes of AfricaTHFNeptune, NJGoogle Scholar
  11. Goldman, N, Anderson, JP, Rodrigo, AG 2000Likelihood-based tests of topologies in phylogeneticsSyst Biol49652670PubMedGoogle Scholar
  12. Huelsenbeck, JP, Crandall, KA 1997Phylogeny estimation and hypothesis testing using maximum likelihoodAnnu Rev Ecol Syst28437466Google Scholar
  13. Huelsenbeck, JP, Ronquist, F 2001MrBayes: Bayesian inference of phylogenetic treesBiometrics17754755Google Scholar
  14. Kishino, H, Hasegawa, M 1989Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in HominoideaJ Mol Evol29170179PubMedGoogle Scholar
  15. Klett, V, Meyer, A 2002What, if anything, is a Tilapia? Mitochondrial NADH2 phylogeny of Tilapiines and the evolution of parental care systems in the African cichlid fishesMol Biol Evol19865883PubMedGoogle Scholar
  16. Kluge, AG, Farris, JS 1969Quantitative phyletics and the evolution of anuransSyst Zool18132Google Scholar
  17. Koblmüller, S, Salzburger, W, Sturmbauer, C 2004Evolutionary relationships in the sand-dwelling cichlid lineage of Lake Tanganyika suggest multiple colonization of rocky habitats and convergent origin of biparental mouthbroodingJ Mol Evol587996PubMedGoogle Scholar
  18. Koblmüller, S, Duftner, N, Katongo, C, Phiri, H, Sturmbauer, C 2005Ancient divergence in bathypelagic Lake Tanganyika deep water cichlids: Mitochondrial phylogeny of the tribe BathybatiniJ Mol Evol60297314Google Scholar
  19. Kocher, TD, Thomas, WK, Meyer, A, Edwards, SV, Pääbo, S, Villablanca, FX, Wilson, AC 1989Dynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primersProc Natl Acad Sci USA8661966200PubMedGoogle Scholar
  20. Kocher, TD, Conroy, JA, McKaye, KR, Stauffer, JR, Lockwood, SF 1995Evolution of NADH dehydrogenase in East African cichlid fishMol Phylogenet Evol4420PubMedGoogle Scholar
  21. Konings, A 1998Tanganyika cichlids in their natural habitatCichlid PressEl Paso, TXGoogle Scholar
  22. Kornfield, I, Smith, PF 2000African cichlid fishes: Model systems for evolutionary biologyAnnu Rev Ecol Syst31163196Google Scholar
  23. Kumazawa, Y, Nishida, M 2000Molecular phylogeny of osteoglossoids: A new model for Gondwanian origin and plate tectonic transportation of the Asian arowanaMol Biol Evol1718691878PubMedGoogle Scholar
  24. Lezzar, KE, Tiercelin, JJ, De Batist, M, Cohen, AS, Bandora, T, van Rensbergen, P, Le Turdu, C, Mifundu, W, Klerkx, J 1996New seismic stratigraphy and late Tertiary history of the north Tanganyikan basin, East African Rift system, deduced from multichannel and high-resolution reflection seismic data and piston core evidenceBasin Res8128Google Scholar
  25. Lippitsch, E 1998Phylogenetic study of cichlid fishes in Lake Tanganyika: A lepidological approachJ Fish Biol53752766Google Scholar
  26. Meyer, A, Morrisey, JM, Schartl, M 1994Recurrent origin of sexually selected trait in Xiphophorus fishes inferred from a molecular phylogenyNature368539541PubMedGoogle Scholar
  27. Meyer, A, Montero, CM, Spreinat, A 1996Molecular phylogenetic inferences about the evolutionary history of East African cichlid fish radiationsJohnson, TOdada, E eds. IDEAL (Internal Decade of East African Lakes). The limnology, climatology and palaeoclimatoloy of the East African lakesGordon and Breach ScientificLondon303323Google Scholar
  28. Moran, P, Kornfield, I, Reinthal, PN 1994Molecular systematics and radiation of the haplochromine cichlids (Teleostei: Perciformes) of Lake MalawiCopeia2274288Google Scholar
  29. Nishida, M 1991Lake Tanganyika as an evolutionary reservoir of old lineages of East African fishes: Inferences from allozyme dataExperientia47974979Google Scholar
  30. Nishida, M 1997Phylogenetic relationships and evolution of Tanganyika cichlids: A molecular perspectiveKwanabe, HHori, MNagoshi, M eds. Fish communities in Lake TanganyikaKyoto University PressKyoto, Japan323Google Scholar
  31. Poll, M 1986Classification des Cichlidae du lac Tanganyika: Tribus, Genre et EspécesMem Classe Sci Acad Roy Belg55163Google Scholar
  32. Posada, D, Crandall, KA 1998Modeltest: Testing the model of DNA substitutionBioinformatics14817818CrossRefPubMedGoogle Scholar
  33. Rossiter, A 1995The cichlid fish assemblage of Lake Tanganyika: Ecology, behaviour, and evolution of its species flocksAdv Ecol Res261023010235Google Scholar
  34. Rüber, L, Verheyen, E, Sturmbauer, C, Meyer, A 1998Lake level fluctuations and speciation in rock-dwelling cichlid fish in Lake Tanganyika, East AfricaGrant, P eds. Evolution on IslandsOxford University PressOxford225240Google Scholar
  35. Rüber, L, Meyer, A, Sturmbauer, C, Verheyen, E 2001Population structure in two sympatric species of the Lake Tanganyika cichlid tribe Eretmodini: Evidence for introgressionMol Ecol1012071225PubMedGoogle Scholar
  36. Salzburger, W, Meyer, A, Baric, S, Verheyen, E, Sturmbauer, C 2002Phylogeny of the Lake Tanganyika cichlid species flock and its relationship to the Central and East African haplochromine cichlid fish faunasSyst Biol51123Google Scholar
  37. Schmidt, HA, Strimmer, K, Vingron, M, Haeseler, A 2002TREE-PUZZLE: Maximum likelihood phylogenetic analysis using quartets and parallel computingBioinformatics18502504PubMedGoogle Scholar
  38. Scholz, CA, Rosendahl, BR 1988Low lake stands in Lakes Malawi and Tanganyika, East Africa, delineated with multifold seismic dataScience24016451648Google Scholar
  39. Scholz, CA, King, JW, Ellis, GS, Swart, PK, Stager, JC, Colman, SM 2003Paleolimnology of Lake Tanganyika, East Africa, over the past 100 kyrJ Paleolim30139150Google Scholar
  40. Strimmer, K, Haeseler, A 1997Likelihood-mapping: A simple method to visualize phylogenetic content of a sequence alignmentProc Natl Acad Sci USA9468156819CrossRefPubMedGoogle Scholar
  41. Sturmbauer, C 1998Explosive speciation in cichlid fishes of the African Great Lakes: A dynamic model of adaptive radiationJ Fish Biol531836Google Scholar
  42. Sturmbauer, C, Meyer, A 1992Genetic divergence, speciation and morphological stasis in a lineage of African cichlid fishesNature358578581PubMedGoogle Scholar
  43. Sturmbauer, C, Meyer, A 1993Mitochondrial phylogeny of the endemic mouthbrooding lineages of cichlid fishes from Lake Tanganyika in Eastern AfricaMol Biol10751768Google Scholar
  44. Sturmbauer, C, Verheyen, E, Rüber, L, Meyer, A 1997Phylogeographic patterns in populations of cichlid fishes from rocky habitats in Lake TanganyikaKocher, TDStepien, C eds. Molecular phylogeny of fishesAcademic PressNew York97111Google Scholar
  45. Sturmbauer, C, Baric, S, Salzburger, W, Rüber, L, Verheyen, E 2001Lake level fluctuations synchronize genetic divergence of cichlid fishes in African lakesMol Biol Evol18144154PubMedGoogle Scholar
  46. Sturmbauer, C, Hainz, U, Baric, S, Verheyen, E, Salzburger, W 2003Evolution of the tribe Tropheini from Lake Tanganyika: Synchronized explosive speciation producing multiple evolutionary parallelismHydrobiologia5005164Google Scholar
  47. Swofford, DL 2000PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4.0Sinauer AssociatesSunderland, MAGoogle Scholar
  48. Takahashi, T 2003Systematics of Tanganyikan cichlid fishes (Teleostei: Perciformes)Ichthyl Res50361382Google Scholar
  49. Takahashi, K, Terai, Y, Nishida, M, Okada, N 1998A novel family of short interspersed repetitive elements (SINEs) from cichlids: The patterns of insertion of SINEs at orthologous loci support the proposed monophyly of four major groups of cichlid fishes in Lake TanganyikaMol Biol Evol15391407PubMedGoogle Scholar
  50. Takahashi, K, Terai, Y, Nishida, M, Okada, N 2001Phylogenetic relationships and ancient incomplete lineages sorting among cichlid fishes in Lake Tanganyika as revealed by analysis of insertion of retroposonsMol Biol Evol1820572066PubMedGoogle Scholar
  51. Takezaki, N, Rzhetsky, A, Nei, M 1995Phylogenetic test of the molecular clock and linearized treesMol Biol Evol12823833PubMedGoogle Scholar
  52. Tamura, K, Nei, M 1993Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzeesMol Biol Evol10512526PubMedGoogle Scholar
  53. Thompson, JD, Higgins, DG, Gibson, TJ 1994CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties, and weight matrix choiceNucleic Acids Res2246734680Google Scholar
  54. Tiercelin, JJ, Mondeguer, A 1991The geology of the Tanganyika troughMartens, KGoddeeris, BCoulter, G eds. Lake Tanganyika and its lifeOxford University PressOxford748Google Scholar
  55. Turner, GF, Seehausen, O, Knight, KE, Allender, CJ, Robinson, RL 2001How many species of cichlid fishes are there in African lakes? Mol Ecol 10793806PubMedGoogle Scholar
  56. Verheyen, E, Rüber, L, Snoeks, J, Meyer, A 1996Mitochondrial phylogeography of rock-dwelling cichlid fishes reveals evolutionary influence of historical lake level fluctuations of Lake TanganyikaPhil Trans R Soc B351797805Google Scholar
  57. Verheyen, E, Salzburger, W, Snoeks, J, Meyer, A 2003Origin of the superflock of cichlid fishes from Lake Victoria, East AfricaScience300325329CrossRefPubMedGoogle Scholar
  58. Yang, Z 1994Estimating the pattern of nucleotide substitutionJ Mol Evol39306314PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • Nina Duftner
    • 1
  • Stephan Koblmüller
    • 1
  • Christian Sturmbauer
    • 1
  1. 1.Department of ZoologyKarl-Franzens-University of GrazGrazAustria

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