Journal of Molecular Evolution

, Volume 60, Issue 3, pp 297–314 | Cite as

Ancient Divergence in Bathypelagic Lake Tanganyika Deepwater Cichlids: Mitochondrial Phylogeny of the Tribe Bathybatini

  • Stephan Koblmüller
  • Nina Duftner
  • Cyprian Katongo
  • Harris Phiri
  • Christian SturmbauerEmail author


The cichlid species flock of Lake Tanganyika represents a polyphyletic assemblage of eight ancestral lineages, which colonized the emerging lake independently. Our study is focused on one of these lineages, the Bathybatini, a tribe of specialized piscivorous cichlids of the deep pelagic zone. By analyzing three mtDNA gene segments of all eight species of the tribe and two species of the closely related Trematocarini, we propose on the basis of a linearized tree analysis that the Bathybatini comprise two distinct lineages, the genera Hemibates and Bathybates, that seeded the primary lacustrine Tanganyika radiation independently. The genus Hemibates is likely to represent a distinct lineage that emerged simultaneously with the tribe Trematocarini and the genus Bathybates and should be therefore treated as a distinct tribe. Within the genus Bathybates, B. minor clearly represents the most ancestral split and is likely to have diverged from the remaining species in the course of the “primary lacustrine Tanganyika radiation” during which also the radiations of the Lamprologini and the H-lineage took place. The remaining “large” Bathybates species also diversified almost simultaneously and in step with the diversification of other Tanganyikan lineages—the Limnochromini and Cyprichromini—with B. graueri occupying the most ancestral branch, suggesting that these were induced by the same environmental changes. The lack of geographic color morphs suggests that competition and resource partitioning, rather than allopatric speciation, promoted speciation within the genus Bathybates.


Adaptive radiation mtDNA sequences Control region Cytochrome b NADH dehydrogenase subunit 2 Resource partitioning 



We thank L. Makasa, R. Sinyinza, and the team at the Mpulungu Station of the Department of Fisheries, Ministry of Agriculture, and Cooperatives, Republic of Zambia, for their assistance during sample collection. We are grateful to J. Snoeks (Africa Museum Tervuren) for identification of “problematic” specimens and to E. Verheyen (Royal Belgian Museum of Natural Sciences) for providing additional tissue samples. We are further indebted to K. Sefc, whose constructive comments helped to improve this paper. S.K., N.D., and C.S. were supported by the Austrian Science Foundation (Grant P15239). S.K. received a DOC fellowship and N.D. a DOC-FFORTE (Women in Research and Technology) fellowship, both provided by the Austrian Academy of Sciences. S.K. and N.D. were further supported by the University of Graz. C.K. got support from the OEAD and the University of Zambia.


  1. Akashi, H 1994Synonymous codon usage in Drosophila melanogaster. Natural selection and translational accuracyGenetics136927935PubMedGoogle Scholar
  2. Anderson, S, Bruijn, MHL, Coulson, AR, Eperon, IC, Sanger, F, Young, IG 1982Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genomeJ Mol Biol156683717PubMedGoogle Scholar
  3. Baric, S, Salzburger, W, Sturmbauer, C 2003Phylogeography and evolution of the Tanganyika cichlid genus Tropheus based upon mitochondrial DNA sequencesJ Mol Evol565468PubMedGoogle Scholar
  4. Brandstötler 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 press. Google Scholar
  5. Brown, WM 1985The mitochondrial genome of animalsMacIntyre, RJ eds. Molecular evolutionary geneticsPlenum PressNew York95130Google Scholar
  6. Cane, MA, Molnar, P 2001Closing of the Indonesian seaway as a precursor to East African aridification around 3–4 million years agoNature411157162PubMedGoogle Scholar
  7. Cohen, AS, Soreghan, MJ, Scholz, CA 1993Estimating the age of formation of lakes: an example from Lake Tanganyika, East African rift systemGeology21511514CrossRefGoogle Scholar
  8. Cohen, AS, Lezzar, KE, Tiercelin, JJ, Soreghan, MJ 1997New palaeogeographic and lake-level reconstructions of Lake Tanganyika: Implications for tectonic, climatic and biological evolution in a rift lakeBasin Res9107132Google Scholar
  9. Comeron, JM, Aguadé, M 1996Synonymous substitutions in the Xdh gene of Drosophila: Heterogeneous distribution along the coding regionGenetics14410531062PubMedGoogle Scholar
  10. Comeron, JM, Kreitman, M 1998The correlation between synonymous and nonsynonymous substitutions in Drosophila: Mutation, selection or relaxed constraints?Genetics150767775PubMedGoogle Scholar
  11. Coulter, GW 1991Lake Tanganyika and its lifeOxford University PressLondon, New YorkGoogle Scholar
  12. Coulter, GW 1994Speciation and fluctuating environments with reference to ancient East African lakesMartens, KGodderies, BCoulter, GW eds. Speciation in ancient lakes (Advances in Limnology 44)E. Schweizerbart’sche Verlagbuchhandlung (Näpele U. Obermüller)Stuttgart127137Google Scholar
  13. Duftner, N, Koblmüller, S, Sturmbauer, C 2005Evolutionary relationships of the Limnochromini, a tribe of benthic deepwater cichlid fish endemic to Lake Tanganyika, East AfricaJ Mol Evol60277289Google Scholar
  14. Farias, IP, Ortí, G, Sampaio, I, Schneider, H, Meyer, A 2001The cytochrome b gene as a phylogenetic marker: The limits of resolution for analyzing relationships among cichlid fishesJ Mol Evol5389103PubMedGoogle Scholar
  15. Felsenstein, J 1985Confidence limits on phylogenies: an approach using the bootstrapEvolution39783791Google Scholar
  16. Graur, D 1985Amino acid composition and the evolutionary rates of protein-coding genesJ Mol Evol225363PubMedGoogle Scholar
  17. Hoelzel, AR, Hancock, JM, Dover, GA 1991Evolution of the cetacean mitochondrial D-loop regionMol Biol Evol8475593PubMedGoogle Scholar
  18. Huelsenbeck, JP, Crandall, KA 1997Phylogeny estimation and hypothesis testing using maximum likelihoodAnnu Rev Ecol Syst28437466Google Scholar
  19. Huelsenbeck, JP, Ronquist, F 2001MrBayes: Bayesian inference of phylogenetic treesBioinformatics17754755CrossRefPubMedGoogle Scholar
  20. Kimura, M 1981Estimation of evolutionary distances between homologous nucleotide sequencesProc Natl Acad Sci USA78454458PubMedGoogle Scholar
  21. Klett, V, Meyer, A 2002What, if anything, is a tilapia? Mitochondrial ND2 phylogeny of Tilapiines and the evolution of parental care systems in the African cichlid fishesMol Biol Evol19865883PubMedGoogle Scholar
  22. Kluge, AG, Farris, JS 1969Quantitative phyletics and the evolution of AnuransSyst Zool18132Google Scholar
  23. 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
  24. 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
  25. Kocher, TD, Conroy, JA, McKaye, KR, Stauffer, JR 1993Similar morphologies of cichlid fishes in Lakes Tanganyika and Malawi are due to convergenceMol Phylogenet Evol4420432Google Scholar
  26. Kocher, TD, Conroy, JA, McKaye, KR, Stauffer, JR, Lockwood, SF 1995Evolution of NADH dehydrogenase in East African cichlid fishMol Phylogenet Evol4420432PubMedGoogle Scholar
  27. Konings, A 1998Tanganyika cichlids in their natural habitatCichlid PressEl Paso, TXGoogle Scholar
  28. Kumazawa, Y, Yamaguchi, M, Nishida, M 1999Mitochondrial molecular clocks and the origin of euteleostean biodiversity: Familial radiation of perciforms may have predated the Cretaceous/Tertiary boundaryAto, M eds. The biology of biodiversitySpringer VerlagTokyo3552Google Scholar
  29. Kuwamura, T 1997The evolution of parental care and mating systems among Tanganyikan cichlidsKawanabe, HMore, MNagoshi, M eds. Fish communities in Lake TanganyikaKyoto University PressKyoto, Japan5986Google Scholar
  30. Lee, WJ, Conroy, J, Howell, WH, Kocher, TD 1995Structure and evolution of the teleost mitochondrial control regionsJ Mol Evol415466PubMedGoogle Scholar
  31. Lezzar, KE, Tiercelin, JJ, Batist, M, Cohen, AS, Bandora, R, Rensbergen, C, Le Turdu, C, Mifundu, W, Klerkx, J 1996New seismic stratigraphy and Late Tertiary history of the North Tanganyika basin, East African rift system deduced from multichannel and high-piston core evidenceBasin Res8128Google Scholar
  32. Lippitsch, E 1998Phylogenetic study of cichlid fishes in Lake Tanganyika: a lepidological approachJ Fish Biol53752766Google Scholar
  33. Meyer, A 1993Phylogenetic relationships and evolutionary processes in East African cichlid fishesTrends Ecol Evol8279284Google Scholar
  34. Nakai, K, Kawanabe, H, Gashagaza, MM 1994Ecological studies on the littoral cichlid communities of Lake Tanganyika: The coexistence of many endemic speciesMartens, KGodderies, BCoulter, GW eds. Speciation in ancient lakes (Advances in Limnology 44)E. Schweizerbart’sche Verlagbuchhandlung (Näpele U. Obermüller)Stuttgart373389Google Scholar
  35. Nishida, M 1991Lake Tanganyika as an evolutionary reservoir of old lineages of East African fishes: Inferences from allozyme dataExperientia47974979Google Scholar
  36. Nishida, M 1997Phylogenetic relationships and evolution of Tanganyikan cichlids: a molecular perspectiveKawanabe, HHori, MNagoshi, M eds. Fish communities in Lake TanganyikaKyoto University PressKyoto, Japan123Google Scholar
  37. Poll, M 1956Poissons Cichlidae. Résult. scient. Explor. hydrobiolbelge Lac Tanganika (1946–1947)III1629Google Scholar
  38. Poll, M 1986Classification des cichlidae du lac Tanganika. Tribus, genres et espècesAcad R Belg Mem Cl Sci451163Google Scholar
  39. Posada, D, Crandall, K 1998MODEL TEST: Testing the model of DNA substitutionBioinformatics14817818CrossRefPubMedGoogle Scholar
  40. Rossiter, A 1995The cichlid fish assemblages of Lake Tanganyika: Ecology, behaviour and evolution of its species flocksAdv Ecol Res26187252Google Scholar
  41. Rozas, J, Sánchesz-DelBarrio, JC, Messeguer, X, Rozas, R 2003DnaSP, DNA polymorphism analyses by coalescent and other methodsBioinformatics1924962497CrossRefPubMedGoogle Scholar
  42. 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
  43. Saccone, C, Attimonelli, M, Sbisá, E 1991Structural elements highly preserved during the evolution of the D-loop-containing region in vertebrate mitochondrial DNAJ Mol Evol26205211Google Scholar
  44. Salzburger, W, Meyer, A, Baric, S, Verheyen, E, Sturmbauer, C 2002Phylogeny of the Lake Tanganyika cichlid species flock and its relationships to Central and East African haplochromine cichlid fish faunasSyst Biol51113135PubMedGoogle Scholar
  45. Schmidt, HA, Strimmer, K, Vingron, M, Haeseler, A 2002TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computingBioinformatics18502504PubMedGoogle Scholar
  46. Scholz, CA, Rosendahl, B 1988Low lake stands in Lakes Malawi and Tanganyika, delineated with multifold seismic dataScience24016451648Google Scholar
  47. Scholz, CA, King, JW, Ellis, GS, Swart, PK, Stager, JC, Colman, SM 2003Palaeolimnology of Lake Tanganyika, East Africa, over the past 100 kyrJ Palaeolimn30139150Google Scholar
  48. Sharp, PM, Li, WH 1987The rate of synonymous substitution in enterobacterial genes is inversely related to codon usage biasMol Biol Evol4222230PubMedGoogle Scholar
  49. Snoeks, J 2000How well known is the ichthyodiversity of the large East African lakes?Adv Ecol Res311738Google Scholar
  50. Stiassny, MLJ 1981Phylogenetic versus convergent relationship between piscivorous cichlid fishes from Lakes Malawi and TanganyikaBull Br Mus Nat Hist Zool4067101Google Scholar
  51. Stiassny, MLJ 1991Phylogenetic intrarelationships of the family Cichlidae: An overviewKeenleyside, MHA eds. Cichlid fishes. Behaviour, ecology and evolutionChapman & HallLondon135Google Scholar
  52. Stiassny, MLJ 1997A phylogenetic overview of the lamprologine cichlids of Africa (Teleostei: Cichlidae): A morphological perspectiveS Afr J Sc93512523Google Scholar
  53. Strimmer, K, Haeseler, A 1996Quartet puzzling: A quartet maximum-likelihood method for reconstructing tree topologiesMol Biol Evol13964969Google Scholar
  54. Strimmer, K, Haeseler, A 1997Likelihood-mapping: A simple method to visualize phylogenetic content of a sequence alignmentProc Natl Acad Sci USA9468156819CrossRefPubMedGoogle Scholar
  55. Sturmbauer, C 1998Explosive speciation in cichlid fishes of the African Great Lakes: A dynamic model of adaptive radiationJ Fish Biol531836Google Scholar
  56. Sturmbauer, C, Meyer, A 1992Genetic divergence, speciation and morphological stasis in a lineage of African cichlid fishesNature358578581PubMedGoogle Scholar
  57. Sturmbauer, C, Meyer, A 1993Mitochondrial phylogeny of the endemic mouthbrooding lineages of cichlid fishes from Lake Tanganyika in Eastern AfricaMol Biol Evol10751768PubMedGoogle Scholar
  58. Sturmbauer, C, Verheyen, E, Meyer, A 1994Mitochondrial phylogeny of the Lamprologini, the major substrate spawning lineage of cichlid fishes from Lake Tanganyika in Eastern AfricaMol Biol Evol11691703PubMedGoogle Scholar
  59. Sturmbauer, C, Verheyen, E, Rüber, A, Meyer, L 1997Phylogeographic patterns in populations of cichlid fishes from rocky habitats in Lake TanganyikaKocher, TDStepien, C eds. Molecular phylogeny of fishesAcademic PressSan Diego91111Google Scholar
  60. 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
  61. 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
  62. Swofford, DL 2000PAUP*: Phylogenetic analysis using parsimony (and other methods), version 4.0b2aSinauerSunderland, MAGoogle Scholar
  63. Takahashi, T 2002Systematics of the tribe Trematocarini (Perciformes: Cichlidae) from Lake Tanganyika, AfricaIchthyol Res49253259Google Scholar
  64. Takahashi, K, Terai, Y, Nishida, M, Okada, N 1998A novel family of short interspersed elements (SINEs) from cichlids: The patterns of inserions of SINEs at orthologous loci support the proposed monophyly of four major groups of cichlid fishes in Lake TanganyikaMol Biol Evol15391407PubMedGoogle Scholar
  65. Takahashi, K, Terai, Y, Nishida, M, Okada, N 2001Phylogenetic relationships and ancient incomplete lineage sorting among cichlid fishes in Lake Tanganyika as revealed by analysis of the insertion of retroposonsMol Biol Evol1820572066PubMedGoogle Scholar
  66. Takahashi, T 2003aComparative osteology of the infraorbitals in cichlid fishes (Osteichthyes: Teleostei: Perciformes) from Lake TanganyikaSpecies Diversity8126Google Scholar
  67. Takahashi, T 2003bSystematics of Tanganyikan cichlid fishes (Teleostei: Perciformes)Ichthyol Res50367382Google Scholar
  68. Takezaki, N, Rzhetsky, A, Nei, M 1995Phylogenetic test of the molecular clock and linearized treesMol Biol Evol12823833PubMedGoogle Scholar
  69. 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
  70. Terai, Y, Takahashi, K, Nishida, M, Sato, T, Okada, N 2003Using SINEs to probe ancient explosive speciation: “Hidden” radiation of African cichlids? Mol Biol Evol20924930PubMedGoogle Scholar
  71. Thompson, JD, Gibson, TJ, Plewniak, F, Jeanmougin, F, Higgins, DG 1997The Clustal X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis toolsNucleic Acids Res2448764882CrossRefGoogle Scholar
  72. Tiercelin, JJ, Mondeguer, A 1991The geology of the Tanganyika troughMartens, KGoddeeris, BCoulter, G eds. Lake Tanganyika and its lifeOxford University PressOxford748Google Scholar
  73. Turner, GF, Seehausen, O, Knight, KE, Allender, CJ, Robinson, RL 2001How many species of cichlid fishes are there in African lakes?Mol Ecol10793806PubMedGoogle Scholar
  74. Verheyen, E, Rüber, L, Snoeks, J, Meyer, A 1996Mitochondrial phylogeny of rock-dwelling cichlid fishes reveals evolutionary influence of historical lake level fluctuations of Lake Tanganyika, AfricaPhil Trans R Soc Lond B351797805Google Scholar
  75. Walsh, PS, Metzger, DA, Higuchi, R 1991Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic materialBiotechniques10506513PubMedGoogle Scholar
  76. Wolfe, KH, Sharp, PM 1993Mammalian gene evolution: Nucleotide sequence divergence between mouse and ratJ Mol Evol37441456CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • Stephan Koblmüller
    • 1
  • Nina Duftner
    • 1
  • Cyprian Katongo
    • 1
    • 2
  • Harris Phiri
    • 3
  • Christian Sturmbauer
    • 1
    Email author
  1. 1.Department of ZoologyKarl-Franzens-University of GrazGrazAustria
  2. 2.Department of Biological SciencesUniversity of ZambiaLusakaZambia
  3. 3.Department of Research and Specialist Services, Fisheries Research DivisionMinistry of Agriculture, Food and FisheriesMpulunguZambia

Personalised recommendations