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High cryptic diversity and persistent lineage segregation in endemic Romecytheridea (Crustacea, Ostracoda) from the ancient Lake Tanganyika (East Africa)

  • SPECIATION IN ANCIENT LAKES 6
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Abstract

Ostracods form a substantial part of the endemic fauna of ancient lakes. Here, we have investigated the phylogenetic and phylogeographic patterns and genetic diversities of species of the endemic genus Romecytheridea from the Southern and Central part of Lake Tanganyika. We found that ostracod populations from four different localities are genetically highly differentiated from each other when analyzing the mitochondrial 16S region, while they are almost identical with genetic markers from the nuclear genome (D1-D2 from the large ribosomal subunit (LSU) and ITS). The criteria of the K/θ method for the evolutionary species concepts are fulfilled when analyzing 16S DNA sequence data, indicating that these populations are in fact different (cryptic) species with allopatric distribution. We discuss various hypotheses on how this high diversity could have originated. The complete lineage segregation can partly be explained by geographic isolation during periods of low lake level stands. But, other factors must have contributed to genetic isolation and speciation, as the two closest populations (Chimba and Katoto) from shallow parts of the Southern basin of Tanganyika are also geographically fully segregated.

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References

  • Altschul, S. F., W. Gish, W. Miller, E. W. Myers & D. J. Lipman, 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403–410.

    Article  PubMed  CAS  Google Scholar 

  • Anseeuw, D., B. Nevado, P. Busselen, J. Snoeks & E. Verheyen, 2012. Extensive introgression among ancestral mtDNA lineages: phylogenetic relationships of the Utaka within the Lake Malawi Cichlid Flock. International Journal of Evolutionary Biology, in press. doi:10.1155/2012/865603.

  • Birky, C. W. Jr., 2013. Species detection and identification in sexual organisms using population genetic theory and DNA sequences. PLoS ONE 8: e52544. doi:10.1371/journal.pone.0052544.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Birky, C. W., J. Adams, M. Gemmel & J. Perry, 2010. Using population genetic theory and DNA sequences for species identification in asexual organisms. PLoS ONE 5: e10609.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bode, S. N. S., D. K. Lamatsch, M. J. F. Martins, O. Schmit, J. Vandekerkhove, F. Mezquita, T. Namiotko, G. Rossetti, I. Schön, R. K. Butlin & K. Martens, 2010. Exceptional cryptic diversity and multiple origins of parthenogenesis in a freshwater ostracod. Molecular Phylogenetics and Evolution 5: 542–552.

    Article  Google Scholar 

  • Bromham, L., D. Penny, A. Rambaut & M. D. Hendy, 2000. The power of relative rate tests depends on the data. Journal of Molecular Evolution 50: 296–301.

    PubMed  CAS  Google Scholar 

  • Brown, K. J., L. Rüber, R. Bills & J. J. Day, 2010. Mastacemblid eels support Lake Tanganyika as an evolutionary hotspot of diversification. BMC Evolutionary Biology 10: 188.

    Article  PubMed  PubMed Central  Google Scholar 

  • Clement, M., D. Posada & K. Crandall, 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1660.

    Article  PubMed  CAS  Google Scholar 

  • Cohen, A. S., 2012. Scientific drilling and biological evolution in ancient lakes: lessons learned and recommendations for the future. Hydrobiologia 682: 3–25.

    Article  CAS  Google Scholar 

  • Cohen, A. S., M. J. Soreghan & C. A. Scholz, 1993. Estimating the age of ancient lakes: an example from Lake Tanganyika, East African rift system. Geology 21: 511–514.

    Article  CAS  Google Scholar 

  • Cohen, A. S., K. E. Lezzar, J. J. Tiercelin & M. Soreghan, 1997. New palaeographic and lake-level reconstructions of Lake Tanganyika: implications for tectonic, climatic and biological evolution in a rift lake. Basin Research 9: 107–132.

    Article  Google Scholar 

  • Cohen, A. S., J. R. Stone, K. R. M. Beuning, L. E. Park, P. N. Reinthal, D. Dettman, C. A. Scholz, T. C. Johnson, J. W. King, M. R. Talbot, E. T. Brown & S. J. Ivory, 2007. Ecological consequences of early Late Pleistocene megadroughts in tropical Africa. Proceedings of the National Academy of Sciences, USA 104: 16422–16427.

    Article  CAS  Google Scholar 

  • Ducasse, O. & P. Carbonel, 1993. Tanganyikacythere nov.gen. (Cytherideinae, Ostracoda) du Lac Tanganyika: systématique des valves, donées écologiques. Geobios 26: 427–447.

    Article  Google Scholar 

  • Edgar, R. C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Excoffier, L. & H. E. L. Lischer, 2010. Arlequin version 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.

    Article  PubMed  Google Scholar 

  • Genner, M. J. & G. F. Turner, 2011. Ancient hybridization and phenotypic novelty within Lake Malawi’s Cichlid Fish Radiation. Molecular Biology and Evolution. doi:10.1093/molbev/msr183.

    PubMed  Google Scholar 

  • Gouy, M., S. Guindon & O. Gascuel, 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27: 221–224.

    Article  PubMed  CAS  Google Scholar 

  • Guindon, S. & O. Gascuel, 2003. PhyML – a simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696–704.

    Article  PubMed  Google Scholar 

  • Hardin, G., 1960. The competitive exclusion principle. Science 131: 1292–1297.

    Article  PubMed  CAS  Google Scholar 

  • Hebert, P. D. N. & T. R. Gregory, 2005. The promise of DNA barcoding for taxonomy. Systematic Biololgy 54: 852–859.

    Article  Google Scholar 

  • Hedrick, P. W., 2007. Sex: differences in mutation, recombination, selection, gene flow, and genetic drift. Evolution 61: 2750–2771.

    Article  PubMed  Google Scholar 

  • Hillis, D. M. & M. T. Dixon, 1991. Ribosomal DNA: molecular evolution and phylogenetic inference. Quarterly Review of Biology 66: 411–453.

    Article  PubMed  CAS  Google Scholar 

  • Koblmüller, S., N. Duftner, K. M. Sefc, M. Aibara, M. Stipacek, M. Blanc, B. Egger & C. Sturmbauer, 2007. Reticulate phylogeny of gastropod-shell-breeding cichlids from Lake Tanganyika – the result of repeated introgressive hybridization. BMC Evolutionary Biology 7: 7. doi:10.1186/1471-2148-7-7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Koblmüller, S., W. Salzburger, B. Obermüller, E. Eigner, C. Sturmbauer & K. M. Sefc, 2011. Separated by sand, fused by dropping water: habitat barriers and fluctuating water levels steer the evolution of rock-dwelling cichlid populations in Lake Tanganyika. Molecular Ecology 20: 2272–2290.

    Article  PubMed  Google Scholar 

  • Koenders, A., K. Martens, S. Halse & I. Schön, 2012. Cryptic species of the Eucypris virens species complex (Ostracoda, Crustacea) have invaded Western Australia. Biological Invasions 14: 2187–2201.

    Article  Google Scholar 

  • Lezzar K.-E., J.-J. Tiercelin, M. de Batist, A. S. Cohen, T. Bandora, P. van Rensbergen, C. le Turdu, W. Mifundu & J. Klerkx, 1996. New seismic stratigraphy and Late Tertiary history of the north Tanganyika basin, East African rift system, deduced from multichannel and high-resolution reflection seismic data and piston core evidence. Basin Research 8: 1–28.

    Google Scholar 

  • Marijnissen, S. A. E., E. Michel, S. R. Daniels, D. Erpenbeck, S. B. J. Menken & F. R. Schram, 2006. Molecular evidence for recent divergence of Lake Tanganyika endemic crabs (Decapoda: Platythelphusidae). Molecular Phylogenetics and Evolution 40: 628–634.

    Article  PubMed  CAS  Google Scholar 

  • Martens, K., 1994. Ostracod speciation in ancient lakes: a review. In: Martens, K., B. Goddeeris & G. Coulter (eds), Speciation in Ancient Lakes, Advances in Limnology, Vol. 44: 203–222.

  • Martens, K., 1997. Speciation in ancient lakes. Trends in Ecology and Evolution 12: 177–182.

    Article  PubMed  CAS  Google Scholar 

  • Martens, K., I. Schön, C. Meisch & D. J. Horne, 2008. Global diversity of ostracods (Ostracoda, Crustacea) in freshwater. Hydrobiologia 595: 185–193.

    Article  Google Scholar 

  • Martens, K., S. Halse & I. Schön, 2012. Nine new species of Bennelongia DeDeckker & McKenzie, 1981 (Crustacea, Ostracoda) from Western Australia, with the description of one new subfamily. Europan Journal of Taxonomy 8: 1–56.

    Google Scholar 

  • Mims, M. C., C. D. Hulsey, B. M. Fitzpatrick & J. T. Streelman, 2010. Geography disentangles introgression from ancestral polymorphism in Lake Malawi cichlids. Molecular Ecology 19: 940–951. doi:10.1111/j.1365-294X.2010.04529.x.

    Article  PubMed  Google Scholar 

  • Nevado, B., S. Koblmüller, C. Sturmbauer, J. Snoeks, J. Usano-Alemany & E. Verheyen, 2009. Complete mitochondrial DNA replacement in a Lake Tanganyika cichlid fish. Molecular Ecology 18: 4240–4255.

    Article  PubMed  CAS  Google Scholar 

  • Nevado, B., T. Backeljau, M. Hanssens & E. Verheyen, 2011. Repeated unidirectional introgression of nuclear and mitochondrial DNA between four congeneric Tanganyikan cichlids. Molecular Biology and Evolution 28: 2253–2267.

    Article  PubMed  CAS  Google Scholar 

  • Palumbi, S., R. A. Martin, S. Romano, W. O. McMillan, L. Stice & G. Grabowski, 1991. The simple fool’s Guide to PCR, Version 2. Department of Zoology and Kewalo Marine Laboratory, University of Hawaii, Honolulu.

  • Pfenninger, M. & K. Schwenk, 2007. Cryptic animal species are homogeneously distributed along taxa and biogeographic regions. BMC Evolutionary Biology 7: 121.

    Article  PubMed  PubMed Central  Google Scholar 

  • Posada, D., 2008. jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.

    Article  PubMed  CAS  Google Scholar 

  • Quenouille, B., N. Hubert, E. Bermingham & S. Planes, 2011. Speciation in tropical seas: allopatry followed by range change. Molecular Phylogenetics and Evolution 58: 546–552.

    Article  PubMed  Google Scholar 

  • Rome, D. R., 1962. Ostracodes. Exploration Hydrobiologique duc Lac Tanganyika (1946-1947). Résultats Scientifiques 3(8): 1–304.

    Google Scholar 

  • Ronquist, F., M. Teslenko, P. van der Mark, D. Ayres, A. Darling, S. Höhna, B. Larget, L. Liu, M. A. Suchard & J. P. Huelsenbeck, 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, in press. doi:10.1093/sysbio/sys029.

  • Rüber, L., E. Verheyen & A. Meyer, 1999. Replicated evolution of trophic specializations in an endemic cichlid fish lineage from Lake Tanganyika. Proceedings of the National Academy of Sciences USA 96: 10230–10235.

    Article  Google Scholar 

  • Rüber, L., A. Meyer, C. Sturmbauer & E. Verheyen, 2001. Population structure in two sympatric species of the Lake Tanganyika cichlid tribe Eretmodini: evidence for introgression. Molecular Ecology 10: 1207–1225.

    Article  PubMed  Google Scholar 

  • Salzburger, W., A. Meyer, S. Baric, E. Verheyen & C. Sturmbauer, 2002. Phylogeny of the Lake Tanganyika cichlid species flock and its relationship to the central and East African haplochromine cichlid fish faunas. Systematic Biology 51: 113–135.

    Article  PubMed  Google Scholar 

  • Schmidt, H. A., K. Strimmer, M. Vingron & A. von Haeseler, 2002. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502–504.

    Article  PubMed  CAS  Google Scholar 

  • Schön, I. & K. Martens, 2003. No slave to sex. Proceedings of the Royal Society of London Series B 270: 827–833.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schön, I. & K. Martens, 2012. Molecular analyses of ostracod flocks from Lake Baikal and Lake Tanganyika. Hydrobiologia 682: 91–110.

    Article  Google Scholar 

  • Schön, I., R. K. Butlin, H. I. Griffiths & K. Martens, 1998. Slow molecular evolution in an ancient asexual ostracod. Proceedings of the Royal Society of London Series B 265: 235–242.

    Article  Google Scholar 

  • Schön, I., K. Martens, K. Van Doninck & R. K. Butlin, 2003. Evolution in the slow lane: molecular rates of evolution in sexual and asexual ostracods (Crustacea: Ostracoda). Biological Journal of the Linnean Society 79: 93–100.

    Article  Google Scholar 

  • Schön, I., K. Martens & S. Halse, 2010. Genetic diversity in Australian ancient asexual Vestalenula (Ostracoda, Darwinulidae) – little variability down-under. Hydrobiologia 641: 59–70.

    Article  Google Scholar 

  • Schön, I., R. Pinto, S. Halse, A. Smith, K. Martens & C. W. Birky Jr., 2012. Cryptic diversity in putative ancient asexual darwinulids (Crustacea: Ostracoda). PLoS ONE 7: e39844.

  • Schwarzer, J., E. E. Swartz, E. Vreven, J. Snoeks, F. P. D. Cotterill & U. K. Schliewen, 2012. Repeated trans watershed hybridization among haplochromine chichlids (Cichlidae) was triggered by Neogene landscape evolution. Proceedings of the Royal Academy of Science, Series B. doi:10.1098/rspb.2012.1667.

    Google Scholar 

  • Sonnenberg, R., A. W. Nolte & D. Tautz, 2007. An evaluation of LSU rDNA D1-D2 sequences for their use in species identification. Frontiers in Zoology 4: 6.

    Article  PubMed  PubMed Central  Google Scholar 

  • Sturmbauer, C., S. Baric, W. Salzburger, L. Rüber & E. Verheyen, 2001. Lake level fluctuations synchronize genetic divergences of cichlid fishes in African lakes. Molecular Biology and Evolution 18: 144–154.

    Article  PubMed  CAS  Google Scholar 

  • Sturmbauer, C., U. Hainz, T. S. Baric, E. Verheyen & W. Salzburger, 2003. Evolution of the tribe Tropheini from Lake Tanganyika: Synchronized explosive speciation producing multiple evolutionary parallelism. Hydrobiologia 500: 541–564.

    Article  Google Scholar 

  • Tamura, K. & M. Nei, 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512–526.

    PubMed  CAS  Google Scholar 

  • Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei & S. Kumar, 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28:2731–2739.

    Google Scholar 

  • Tiercelin, J.-J. & A. Mondeuger, 1991. The geology of the Tanganyikan trough. In Coulter, G. W. (ed.), Lake Tanganyika and Its Life. Oxford University Press, London: 7–48.

    Google Scholar 

  • Trontelj, P. & C. Fiser, 2009. Cryptic species diversity should not be trivialised. Systematic Biodiversity 7: 1–3.

    Article  Google Scholar 

  • White, T. J., T. Bruns, S. Lee & J. Taylor, 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis, M. A., D. G. Gelfand, J. J. Sninsky & T. J. White (eds), PCR Protocols: A Guide to Methods and Applications. Academic Press, London: 315–322.

    Chapter  Google Scholar 

  • Wilke, T., R. Schultheiß & C. Albrecht, 2009. As time goes by: a simple fool’s guide to molecular clock approaches in invertebrates. American Malacological Bulletin 27: 25–45.

    Article  Google Scholar 

  • Wilson, A. B., M. Glaubrecht & A. Meyer, 2004. Ancient lakes as evolutionary reservoirs: evidence from the thalassoid gastropods of Lake Tanganyika. Proceedings of the Royal Society London, Series B 271: 529–536.

    Article  Google Scholar 

  • Wouters, K. 1979. Kavalacythereis braconensis gen.n.spec.n., a remarkable new cytheracean genus and species from Lake Tanganyika (Zaire). Annales de la Societé zoologique de Belgique 108 (3/4): 179–187.

  • Wouters, K., 1988a. On Romecytheridea tenuisculpta (ROME). Stereo-Atlas of Ostracod Shells 15(2): 97–100.

    Google Scholar 

  • Wouters, K., 1988b. On Romecytheridea ampla WOUTERS sp.nov. Stereo-Atlas of Ostracod Shells, 15(2): 101-106.

  • Wouters, K. & K. Martens, 1992. Contribution to the knowledge of Tanganyikan cytheraceans, with the description of Mesocyprideis nom.nov. (Crustacea, Ostracoda). Bulletin van het Koninklijk Belgisch Instituut voor Natuurwetenschappen, Biologie 62: 159–166.

    Google Scholar 

  • Wouters, K. & K. Martens, 1994. Contribution to the knowledge of the Cyprideis species flock (Crustacea, Ostracoda) of Lake Tanganyika, with the description of three new species. Bulletin van het Koninklijk Belgisch Instituut voor Natuurwetenschappen, Biologie 64: 111–128.

    Google Scholar 

  • Wouters, K. & K. Martens, 1999. Four new species of the Cyprideis species flock (Crustacea: Ostracoda) of Lake Tanganyika (East Africa). Bulletin van het Koninklijk Belgisch Instituut voor Natuurwetenschappen, Biologie 69: 67–82.

    Google Scholar 

  • Wouters, K. & K. Martens, 2000. On the taxonomic position of the genera Archeocyprideis and Kavalacythereis of the Cyprideis species flock (Crustacea, Ostracoda) in Lake Tanganyika (East Africa), with the first description of the appendages. Bulletin van het Koninklijk Belgisch Instituut voor Natuurwetenschappen, Biologie 70: 207–216.

    Google Scholar 

  • Wouters, K. & K. Martens, 2001. On the Cyprideis species flock (Crustacea, Ostracoda) in Lake Tanganyika, with the description of four new species. Hydrobiologia 450: 111–127.

    Article  Google Scholar 

  • Wouters, K. & K. Martens, 2007. Three new species of the Cyprideis species flock (Crustacea, Ostracoda) of Lake Tanganyika (East Africa). Bulletin van het Koninklijk Belgisch Instituut voor Natuurwetenschappen, Biologie 77: 147–160.

    Google Scholar 

  • Wouters, K. & K. Martens, 2008. Three further new species of the Cyprideis species flock (Crustacea, Ostracoda) from Lake Tanganyika (East Africa). Bulletin van het Koninklijk Belgisch Instituut voor Natuurwetenschappen, Biologie 78: 29–43.

    Google Scholar 

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Acknowledgments

We acknowledge the ESF EUROCHORES programme Eurodiversity for funding the MOLARCH project (05_EDIV_FP237-MOLARCH).

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Correspondence to Isa Schön.

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Guest editors: T. von Rintelen, R. M. Marwoto, G. D. Haffner & F. Herder / Speciation in Ancient Lakes – Classic Concepts and New Approaches

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Schön, I., Poux, C., Verheyen, E. et al. High cryptic diversity and persistent lineage segregation in endemic Romecytheridea (Crustacea, Ostracoda) from the ancient Lake Tanganyika (East Africa). Hydrobiologia 739, 119–131 (2014). https://doi.org/10.1007/s10750-013-1581-y

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