Skip to main content

Advertisement

SpringerLink
Log in

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

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  • J Adachi M Hasegawa (1996) ArticleTitleModel of amino acid substitution in proteins encoded by mitochondrial DNA J Mol Evol 42 459–468 Occurrence Handle1:CAS:528:DyaK28XivFKnurw%3D Occurrence Handle8642615

    CAS  PubMed  Google Scholar 

  • S Baric W Salzburger C Sturmbauer (2003) ArticleTitlePhylogeography and evolution of the Tanganyikan cichlid genus Tropheus based upon mitochondrial DNA sequences J Mol Evol 56 54–68 Occurrence Handle1:CAS:528:DC%2BD3sXpvFyjsw%3D%3D Occurrence Handle12569423

    CAS  PubMed  Google Scholar 

  • 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 press

  • MA Cane P Molnar (2001) ArticleTitleClosing of the Indonesian seaway as a precursor to east African aridification around 3–4 million years ago Nature 411 157–162 Occurrence Handle1:CAS:528:DC%2BD3MXjslGltLc%3D Occurrence Handle11346785

    CAS  PubMed  Google Scholar 

  • AS Cohen MJ Soreghan (1993) ArticleTitleEstimating the age of ancient lakes: An example from Lake Tanganyika, East African rift system Geology 21 511–514 Occurrence Handle10.1130/0091-7613(1993)021<0511:ETAOFO>2.3.CO;2 Occurrence Handle1:CAS:528:DyaK2cXht1SmtA%3D%3D

    Article  CAS  Google Scholar 

  • AS Cohen KE Lezzar JJ Tiercelin M Soreghan (1997) ArticleTitleNew palaeographic and lake-level reconstructions of Lake Tanganyika: Implications for tectonic, climatic and biological evolution in a rift lake Basin Res 9 107–132

    Google Scholar 

  • GW Coulter (1991) Lake Tanganyika and its life Oxford University Press Oxford

    Google Scholar 

  • PD Danley TD Kocher (2001) ArticleTitleSpeciation in rapidly diverging systems: Lessons from Lake Malawi Mol Ecol 10 1075–1086 Occurrence Handle1:STN:280:DC%2BD3M3ptlyquw%3D%3D Occurrence Handle11380867

    CAS  PubMed  Google Scholar 

  • D Delvaux (1995) ArticleTitleAge of Lake Malawi (Nyasa) and water level fluctuations Mus R Afr Centr Tervuren (Belg) Dept Geol Min Rapp Ann 1995–1996 99–108

    Google Scholar 

  • G Fryer TD Iles (1972) The cichlid fishes of the great lakes of Africa THF Neptune, NJ

    Google Scholar 

  • N Goldman JP Anderson AG Rodrigo (2000) ArticleTitleLikelihood-based tests of topologies in phylogenetics Syst Biol 49 IssueID4 652–670 Occurrence Handle1:STN:280:DC%2BD38zntVOjtw%3D%3D Occurrence Handle12116432

    CAS  PubMed  Google Scholar 

  • JP Huelsenbeck KA Crandall (1997) ArticleTitlePhylogeny estimation and hypothesis testing using maximum likelihood Annu Rev Ecol Syst 28 437–466

    Google Scholar 

  • JP Huelsenbeck F Ronquist (2001) ArticleTitleMrBayes: Bayesian inference of phylogenetic trees Biometrics 17 754–755 Occurrence Handle1:STN:280:DC%2BD3MvotV2isw%3D%3D

    CAS  Google Scholar 

  • H Kishino M Hasegawa (1989) ArticleTitleEvaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea J Mol Evol 29 170–179 Occurrence Handle1:CAS:528:DyaL1MXkvFCnsbc%3D Occurrence Handle2509717

    CAS  PubMed  Google Scholar 

  • V Klett A Meyer (2002) ArticleTitleWhat, if anything, is a Tilapia? Mitochondrial NADH2 phylogeny of Tilapiines and the evolution of parental care systems in the African cichlid fishes Mol Biol Evol 19 IssueID6 865–883 Occurrence Handle1:CAS:528:DC%2BD38Xks1Ojtb0%3D Occurrence Handle12032243

    CAS  PubMed  Google Scholar 

  • AG Kluge JS Farris (1969) ArticleTitleQuantitative phyletics and the evolution of anurans Syst Zool 18 1–32

    Google Scholar 

  • S Koblmüller W Salzburger C Sturmbauer (2004) ArticleTitleEvolutionary relationships in the sand-dwelling cichlid lineage of Lake Tanganyika suggest multiple colonization of rocky habitats and convergent origin of biparental mouthbrooding J Mol Evol 58 79–96 Occurrence Handle14743316

    PubMed  Google Scholar 

  • S Koblmüller N Duftner C Katongo H Phiri C Sturmbauer (2005) ArticleTitleAncient divergence in bathypelagic Lake Tanganyika deep water cichlids: Mitochondrial phylogeny of the tribe Bathybatini J Mol Evol 60 297–314

    Google Scholar 

  • TD Kocher WK Thomas A Meyer SV Edwards S Pääbo FX Villablanca AC Wilson (1989) ArticleTitleDynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primers Proc Natl Acad Sci USA 86 6196–6200 Occurrence Handle1:CAS:528:DyaL1MXlvV2ksbw%3D Occurrence Handle2762322

    CAS  PubMed  Google Scholar 

  • TD Kocher JA Conroy KR McKaye JR Stauffer SF Lockwood (1995) ArticleTitleEvolution of NADH dehydrogenase in East African cichlid fish Mol Phylogenet Evol 4 IssueID4 420 Occurrence Handle1:CAS:528:DyaK28XhtF2isLY%3D Occurrence Handle8747298

    CAS  PubMed  Google Scholar 

  • A Konings (1998) Tanganyika cichlids in their natural habitat Cichlid Press El Paso, TX

    Google Scholar 

  • I Kornfield PF Smith (2000) ArticleTitleAfrican cichlid fishes: Model systems for evolutionary biology Annu Rev Ecol Syst 31 163–196

    Google Scholar 

  • Y Kumazawa M Nishida (2000) ArticleTitleMolecular phylogeny of osteoglossoids: A new model for Gondwanian origin and plate tectonic transportation of the Asian arowana Mol Biol Evol 17 IssueID12 1869–1878 Occurrence Handle1:CAS:528:DC%2BD3cXptVWrsbo%3D Occurrence Handle11110903

    CAS  PubMed  Google Scholar 

  • KE Lezzar JJ Tiercelin M De Batist AS Cohen T Bandora P van Rensbergen C Le Turdu W Mifundu J Klerkx (1996) ArticleTitleNew 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 evidence Basin Res 8 1–28

    Google Scholar 

  • E Lippitsch (1998) ArticleTitlePhylogenetic study of cichlid fishes in Lake Tanganyika: A lepidological approach J Fish Biol 53 752–766

    Google Scholar 

  • A Meyer JM Morrisey M Schartl (1994) ArticleTitleRecurrent origin of sexually selected trait in Xiphophorus fishes inferred from a molecular phylogeny Nature 368 539–541 Occurrence Handle1:STN:280:ByuC1cjoslE%3D Occurrence Handle8139686

    CAS  PubMed  Google Scholar 

  • A Meyer CM Montero A Spreinat (1996) Molecular phylogenetic inferences about the evolutionary history of East African cichlid fish radiations T Johnson E Odada (Eds) IDEAL (Internal Decade of East African Lakes). The limnology, climatology and palaeoclimatoloy of the East African lakes Gordon and Breach Scientific London 303–323

    Google Scholar 

  • P Moran I Kornfield PN Reinthal (1994) ArticleTitleMolecular systematics and radiation of the haplochromine cichlids (Teleostei: Perciformes) of Lake Malawi Copeia 2 274–288

    Google Scholar 

  • M Nishida (1991) ArticleTitleLake Tanganyika as an evolutionary reservoir of old lineages of East African fishes: Inferences from allozyme data Experientia 47 974–979

    Google Scholar 

  • M Nishida (1997) Phylogenetic relationships and evolution of Tanganyika cichlids: A molecular perspective H Kwanabe M Hori M Nagoshi (Eds) Fish communities in Lake Tanganyika Kyoto University Press Kyoto, Japan 3–23

    Google Scholar 

  • M Poll (1986) ArticleTitleClassification des Cichlidae du lac Tanganyika: Tribus, Genre et Espéces Mem Classe Sci Acad Roy Belg 5 5–163

    Google Scholar 

  • D Posada KA Crandall (1998) ArticleTitleModeltest: Testing the model of DNA substitution Bioinformatics 14 IssueID9 817–818 Occurrence Handle10.1093/bioinformatics/14.9.817 Occurrence Handle1:CAS:528:DyaK1MXktlCltw%3D%3D Occurrence Handle9918953

    Article  CAS  PubMed  Google Scholar 

  • A Rossiter (1995) ArticleTitleThe cichlid fish assemblage of Lake Tanganyika: Ecology, behaviour, and evolution of its species flocks Adv Ecol Res 26 10230–10235

    Google Scholar 

  • L Rüber E Verheyen C Sturmbauer A Meyer (1998) Lake level fluctuations and speciation in rock-dwelling cichlid fish in Lake Tanganyika, East Africa P Grant (Eds) Evolution on Islands Oxford University Press Oxford 225–240

    Google Scholar 

  • L Rüber A Meyer C Sturmbauer E Verheyen (2001) ArticleTitlePopulation structure in two sympatric species of the Lake Tanganyika cichlid tribe Eretmodini: Evidence for introgression Mol Ecol 10 1207–1225 Occurrence Handle11380878

    PubMed  Google Scholar 

  • W Salzburger A Meyer S Baric E Verheyen C Sturmbauer (2002) ArticleTitlePhylogeny of the Lake Tanganyika cichlid species flock and its relationship to the Central and East African haplochromine cichlid fish faunas Syst Biol 51 IssueID1 1–23

    Google Scholar 

  • HA Schmidt K Strimmer M Vingron A Haeseler Particlevon (2002) ArticleTitleTREE-PUZZLE: Maximum likelihood phylogenetic analysis using quartets and parallel computing Bioinformatics 18 502–504 Occurrence Handle1:CAS:528:DC%2BD38XivFKrsL0%3D Occurrence Handle11934758

    CAS  PubMed  Google Scholar 

  • CA Scholz BR Rosendahl (1988) ArticleTitleLow lake stands in Lakes Malawi and Tanganyika, East Africa, delineated with multifold seismic data Science 240 1645–1648

    Google Scholar 

  • CA Scholz JW King GS Ellis PK Swart JC Stager SM Colman (2003) ArticleTitlePaleolimnology of Lake Tanganyika, East Africa, over the past 100 kyr J Paleolim 30 139–150

    Google Scholar 

  • K Strimmer A Haeseler Particlevon (1997) ArticleTitleLikelihood-mapping: A simple method to visualize phylogenetic content of a sequence alignment Proc Natl Acad Sci USA 94 6815–6819 Occurrence Handle10.1073/pnas.94.13.6815 Occurrence Handle1:CAS:528:DyaK2sXktF2ruro%3D Occurrence Handle9192648

    Article  CAS  PubMed  Google Scholar 

  • C Sturmbauer (1998) ArticleTitleExplosive speciation in cichlid fishes of the African Great Lakes: A dynamic model of adaptive radiation J Fish Biol 53 IssueIDSuppl A 18–36

    Google Scholar 

  • C Sturmbauer A Meyer (1992) ArticleTitleGenetic divergence, speciation and morphological stasis in a lineage of African cichlid fishes Nature 358 IssueID13 578–581 Occurrence Handle1:STN:280:By2A28rotFw%3D Occurrence Handle1501712

    CAS  PubMed  Google Scholar 

  • C Sturmbauer A Meyer (1993) ArticleTitleMitochondrial phylogeny of the endemic mouthbrooding lineages of cichlid fishes from Lake Tanganyika in Eastern Africa Mol Biol 10 IssueID4 751–768 Occurrence Handle1:CAS:528:DyaK3sXlvF2qtb0%3D

    CAS  Google Scholar 

  • C Sturmbauer E Verheyen L Rüber A Meyer (1997) Phylogeographic patterns in populations of cichlid fishes from rocky habitats in Lake Tanganyika TD Kocher C Stepien (Eds) Molecular phylogeny of fishes Academic Press New York 97–111

    Google Scholar 

  • C Sturmbauer S Baric W Salzburger L Rüber E Verheyen (2001) ArticleTitleLake level fluctuations synchronize genetic divergence of cichlid fishes in African lakes Mol Biol Evol 18 144–154 Occurrence Handle1:CAS:528:DC%2BD3MXotVOmsQ%3D%3D Occurrence Handle11158373

    CAS  PubMed  Google Scholar 

  • C Sturmbauer U Hainz S Baric E Verheyen W Salzburger (2003) ArticleTitleEvolution of the tribe Tropheini from Lake Tanganyika: Synchronized explosive speciation producing multiple evolutionary parallelism Hydrobiologia 500 51–64

    Google Scholar 

  • DL Swofford (2000) PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4.0 Sinauer Associates Sunderland, MA

    Google Scholar 

  • T Takahashi (2003) ArticleTitleSystematics of Tanganyikan cichlid fishes (Teleostei: Perciformes) Ichthyl Res 50 361–382

    Google Scholar 

  • K Takahashi Y Terai M Nishida N Okada (1998) ArticleTitleA 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 Tanganyika Mol Biol Evol 15 391–407 Occurrence Handle1:CAS:528:DyaK1cXitlKiurc%3D Occurrence Handle9549090

    CAS  PubMed  Google Scholar 

  • K Takahashi Y Terai M Nishida N Okada (2001) ArticleTitlePhylogenetic relationships and ancient incomplete lineages sorting among cichlid fishes in Lake Tanganyika as revealed by analysis of insertion of retroposons Mol Biol Evol 18 IssueID11 2057–2066 Occurrence Handle1:CAS:528:DC%2BD3MXotVSlsbs%3D Occurrence Handle11606702

    CAS  PubMed  Google Scholar 

  • N Takezaki A Rzhetsky M Nei (1995) ArticleTitlePhylogenetic test of the molecular clock and linearized trees Mol Biol Evol 12 IssueID5 823–833 Occurrence Handle1:CAS:528:DyaK2MXns1yqsbg%3D Occurrence Handle7476128

    CAS  PubMed  Google Scholar 

  • K Tamura M Nei (1993) ArticleTitleEstimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees Mol Biol Evol 10 IssueID3 512–526 Occurrence Handle1:CAS:528:DyaK3sXks1CksL4%3D Occurrence Handle8336541

    CAS  PubMed  Google Scholar 

  • JD Thompson DG Higgins TJ Gibson (1994) ArticleTitleCLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties, and weight matrix choice Nucleic Acids Res 22 4673–4680

    Google Scholar 

  • JJ Tiercelin A Mondeguer (1991) The geology of the Tanganyika trough K Martens B Goddeeris G Coulter (Eds) Lake Tanganyika and its life Oxford University Press Oxford 7–48

    Google Scholar 

  • GF Turner O Seehausen KE Knight CJ Allender RL Robinson (2001) ArticleTitleHow many species of cichlid fishes are there in African lakes? Mol Ecol 10 793–806 Occurrence Handle1:STN:280:DC%2BD3M3htVWhsg%3D%3D Occurrence Handle11298988

    CAS  PubMed  Google Scholar 

  • E Verheyen L Rüber J Snoeks A Meyer (1996) ArticleTitleMitochondrial phylogeography of rock-dwelling cichlid fishes reveals evolutionary influence of historical lake level fluctuations of Lake Tanganyika Phil Trans R Soc B 351 797–805 Occurrence Handle1:CAS:528:DyaK28XltF2lsb4%3D

    CAS  Google Scholar 

  • E Verheyen W Salzburger J Snoeks A Meyer (2003) ArticleTitleOrigin of the superflock of cichlid fishes from Lake Victoria, East Africa Science 300 325–329 Occurrence Handle10.1126/science.1080699 Occurrence Handle1:CAS:528:DC%2BD3sXislyqtLg%3D Occurrence Handle12649486

    Article  CAS  PubMed  Google Scholar 

  • Z Yang (1994) ArticleTitleEstimating the pattern of nucleotide substitution J Mol Evol 39 306–314 Occurrence Handle1:CAS:528:DyaK2cXmt1eit7c%3D Occurrence Handle7932792

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Department of Zoology, Karl-Franzens-University of Graz, Universitätsplatz 2, A-8010, Graz, Austria

    Nina Duftner, Stephan Koblmüller & Christian Sturmbauer

Authors
  1. Nina Duftner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephan Koblmüller
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christian Sturmbauer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christian Sturmbauer.

Additional information

Reviewing Editor: Dr. Axel Meyer

Rights and permissions

Reprints and permissions

About this article

Cite this article

Duftner, N., Koblmüller, S. & Sturmbauer, C. Evolutionary Relationships of the Limnochromini, a Tribe of Benthic Deepwater Cichlid Fish Endemic to Lake Tanganyika, East Africa. J Mol Evol 60, 277–289 (2005). https://doi.org/10.1007/s00239-004-0017-8

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-004-0017-8

Keywords

Search

Navigation