Abstract
Intra-specific morphological variation in the cichlid Tropheus duboisi from 10 localities over its entire known distribution area along the central eastern and northern shore of Lake Tanganyika was investigated. This revealed significant differences between various populations that are geographically isolated. These morphological observations only partially correspond to the results of a haplotype network, based on mtDNA. In addition, a difference in the timing of the onset of the adult colour pattern was discovered for one isolated population. The occurrence of morphological intra-specific differentiation is discussed with respect to the basal position of T. duboisi within Tropheus as well as to the presumed morphological stasis of the genus.
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References
Akaike, H., 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716–723.
Baric, S., W. Salzburger & C. Sturmbauer, 2003. Phylogeography and evolution of the Tanganyika cichlid genus Tropheus based upon mitochondrial DNA sequences. Journal of Molecular Evolution 56: 54–68.
Bernatchez, L. & R. G. Danzmann, 1993. Congruence in control region sequence and restriction-site variation in mitochondrial DNA of brook charr (Salvelinus fontinalis Mitchill). Molecular Biology and Evolution 10: 1002–1014.
Brichard, P., 1989. Pierre Brichard’s Book of Cichlids and All the Other Fishes of Lake Tanganyika. T.F.H. Publications, Neptune City. 544 pp.
Centre Regional de Recherche en Hydrobiologie Appliquée (CRRHA), 1996. Rapport Final: 78 pp. with 13 annexes.
Clement, M., D. Posada & K. A. Crandall, 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1660.
Cohen, A. S., M. J. Soreghan & C. A. Scholz, 1993. Estimating the age of formation of lakes: an example from Lake Tanganyika, East African Rift system. Geology 21: 511–514.
Duftner, N., K. M. Sefc, S. Koblmüller, B. Nevado, E. Verheyen, H. Phiri & C. Sturmbauer, 2006. Distinct population structure in a phenotypically homogeneous rock-dwelling cichlid fish from Lake Tanganyika. Molecular Ecology 15: 2381–2396.
Egger, B., S. Koblmüller, C. Sturmbauer & K. M. Sefc, 2007. Nuclear and mitochondrial data reveal different evolutionary processes in the Lake Tanganyika cichlid genus Tropheus. BMC Evolutionary Biology 7: 137.
Felsenstein, J., 2005. PHYLIP (Phylogeny Inference Package) Version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington. http://evolution.genetics.washington.edu/phylip.html.
Gelman, A. & D. B. Rubin, 1992. Inference from iterative simulation using multiple sequences. Statistical Science 7: 457–472.
Glez-Peña, D., D. Gómez-Blanco, M. Reboiro-Jato, F. Fdez-Riverola & D. Posada, 2010. ALTER: program-oriented format conversion of DNA and protein alignments. Nucleic Acids Research 38(Suppl. 2): W14–W18.
Guindon, S. & O. Gascuel, 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696–704.
Hammer, Ø., D. A. Harper & P. D. Ryan, 2001. PAST: paleontological statistics software package for education and data analysis. Paleontologia Electronica 4: 9 pp.
Hanssens, M. & J. Snoeks, 2003. A new species and geographical variation in the Telmatochromis temporalis complex (Teleostei, Cichlidae) from Lake Tanganyika. Journal of Fish Biology 63: 596–616.
Hanssens, M., J. Snoeks & E. Verheyen, 1999. A morphometric revision of the genus Ophthalmotilapia (Teleostei, Cichlidae) from Lake Tanganyika (East Africa). Zoological Journal of the Linnean Society 125: 487–512.
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.
Hebert, P. D. N., M. Y. Stoeckle, T. S. Zemlak & C. M. Francis, 2004. Identification of birds through DNA barcodes. PLOS Biology 2: 1657–1663.
Herler, J., M. Kerschbaumer, P. Mitteroecker, L. Postl & C. Sturmbauer, 2010. Sexual dimorphism and population divergence in the Lake Tanganyika cichlid fish genus Tropheus. Frontiers in Zoology 7: 4.
Herrmann, H.-J., 1999. Tropheus: Verbreitung, Arten, Haltung. Karl-Heinz Dähne Verlag, Ettlingen. 112 pp.
Heule, C. & W. Salzbuger, 2011. The ontogenetic development of egg-spots in the haplochromine cichlid fish Astatotilapia burtoni. Journal of Fish Biology 78: 1588–1593.
Huelsenbeck, J. P. & F. Ronquist, 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.
Ivanova, N. V., J. R. de Waard & P. D. N. Hebert, 2006. An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes 6: 998–1002.
Jolicoeur, P., 1963. The multivariate generalisation of the allometry equation. Biometrics 19: 497–499.
Kerschbaumer, M. & C. Sturmbaumer, 2011. The utility of geometric morphometrics to eludicate pathways of cichlid fish evolution. International Journal of Evolutionary Biology. Article ID 290245, 8 pp.
Kerschbaumer, M., L. Postl, M. Koch, T. Wiedl & C. Sturmbauer, 2011. Morphological distinctness despite large-scale phenotypic plasticity—analysis of wild and pond-bred juveniles of allopatric populations of Tropheus moorii. Naturwissenschaften 2: 125–134.
Kimura, M., 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111–120.
Kimura, M., 1981. Estimation of evolutionary distances between homologous nucleotide sequences. Proceedings of the National Academy of Sciences of the United States of America 78: 454–458.
Klingenberg, C. P., 2011. MorphoJ: an integrated software package for geometric morphometrics. Molecular ecology Resources 11: 353–357.
Koblmüller, S., K. M. Sefc & C. Sturmbauer, 2008. The Lake Tanganyika cichlid species assemblage: recent advances in molecular phylogenetics. Hydrobiologia 615: 5–20.
Koblmüller, S., B. Egger, C. Sturmbauer & K. M. Sefc, 2010. Rapid radiation, ancient incomplete lineage sorting and ancient hybridization in the endemic Lake Tanganyika cichlid tribe tropheini. Molecular Phylogenetics and Evolution 55: 318–334.
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.
Kohda, M. & Y. Yanagisawa, 1992. Vertical distributions of two herbivorous cichlid fishes of the genus Tropheus in Lake Tanganyika, Africa. Ecology of Freshwater Fish 1: 99–103.
Kohda, M., Y. Yanagisawa, T. Sato, K. Nakaya, Y. Niimura, K. Matsumoto & H. Ochi, 1996. Geographical colour variation in cichlid fishes at the southern end of Lake Tanganyika. Environmental Biology of Fishes 45: 237–248.
Konings, A., 1998. Tanganyika Cichlids in Their Natural Habitat. Cichlid Press, El Paso. 272 pp.
Konings, A., 2013. Tropheus in Their Natural Habitat. Cichlid press, El Paso. 160 pp.
Ladigez, W., 1959. Beiträge zur Kenntnis der Cichliden des Tanganjika-Sees I. Internationale Revue der gesamten Hydrobiologie 44: 431–438.
Liem, K. F., 1980. Adaptive significance of intra- and interspecific differences in the feeding repertoire of cichlid fishes. American Zoologist 20: 295–314.
Liem, K. F. & A. P. Summers, 2000. Integration of versatile functional design, population ecology, ontogeny and phylogeny. Netherlands Journal of Zoology 50: 245–259.
Maderbacher, M., C. Bauer, J. Herler, L. Postl, L. Makasa & C. Sturmbauer, 2008. Assessment of traditional versus geometric morphometrics for discriminating populations of the Tropheus moorii species complex (Teleostei: Cichlidae), a Lake Tanganyika model for allopatric speciation. Journal of Zoological Systematics and Evolutionary Research 46: 153–161.
Maréchal, C. & M. Poll, 1991. Tropheus. In Daget, J., J.-P. Gosse, G. G. Teugels & D. F. E. Thys van den Audenaerde (eds), Check-list of the Freshwater Fishes of Africa (CLOFFA), Vol. 4. ISNB, Brussels: 521–525.
Marlier, G., 1959. Observations sur la biologie littorale du Lac Tanganyika. Revue de Zoologie et de Botanique Africaines 59: 164–183.
Muschinck, M., A. Indermauer & W. Salzburger, 2012. Convergent evolution within an adaptive radiation of cichlid fishes. Current Biology 22: 1–7.
Nelissen, M. H. J., 1978a. Contribution to the ethology of Tropheus duboisi Marlier (Pisces, Cichlidae). Acta Zoologica et Pathologica Antverpiensia 70: 133–139.
Nelissen, M. H. J., 1978b. Contribution to the ethology of Tropheus brichardi Nelissen en Thys, 1975 (Pisces, Cichlidae). Acta Zoologica et Pathologica Antverpiensia 70: 141–147.
Nelissen, M. H. J., 1979. A taxonomic revision of the genera Simochromis, Pseudosimochromis and Tropheus (Pisces, Cichlidae). Annals of the Royal Museum for Central Africa, Serie 8, Zoological Sciences.
Ntakimazi, G., 1995. La role des ecotones terre/eau dans la diversité biologique et les resources du Lac Tanganyika. Raport UNESCO/MAB/DANIDA 510/BDI/40.
Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.
R Development Core Team, 2008. R: A Language and Environment for Statistical Computing. R foundation for Statistical Computing, Vienna, Austria.
Raeymaekers, J. A. M., P. I. Hablützel, A. F. Grégoir, J. Bamps, A. K. Roose, M. P. M. Vanhove, M. Van Steenberge, A. Pariselle, T. Huyse, J. Snoeks & F. A. M. Volckaert, 2013. Contrasting parasite communities among allopatric colour morphs of the Lake Tanganyika cichlid Tropheus: potential for parasite-driven speciation? BMC Evolutionary Biology 13: 41.
Risch, S. & J. Snoeks, 2008. Geographic variation in Neolamprologus niger (Poll, 1956) (Perciformes, Cichlidae) from Lake Tanganyika (Africa). Zootaxa 1857: 21–32.
Rohlf, J. F., 1999. tpsDig, version 2.10. Department of Ecology and Evolution, State University of New York at Stony Brook.
Ronquist, F. & J. P. Huelsenbeck, 2003. MrBayes3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.
Schupke, P., 2003. African Cichlids II. Tanganyika I. Tropheus. Aqualog Verlag A.C.S. GmbH., Rodgau. 190 pp.
Sefc, K. M., S. Baric, W. Salzburger & C. Sturmbauer, 2007. Species-specific population structure in rock-specialized sympatric cichlid species in Lake Tanganyika, East Africa. Journal of Molecular Evolution 64: 33–49.
Silvestro, D. & I. Michalak, 2012. raxmlGUI: a graphical front-end for RAxML. Organisms Diversity & Evolution 12(4): 335–337.
Snoeks, J., 2000. How well known is the ichthyodiversity of the large East African lakes? Advances in Ecological Research 31: 17–38.
Snoeks, J., 2004. The Cichlid Diversity of Lake Malawi/Nyasa/Niassa: Identification, Distribution and Taxonomy. Cichlid Press, El Paso. 360 pp.
Snoeks, J., L. Rüber & E. Verheyen, 1994. The Tanganyika problem: comments on the taxonomy and distribution patterns of its cichlid fauna. Archiv für Hydrobiologie, Beihefte Ergebnisse der Limnologie 44: 355–372.
Spreitzer, M. L., S. Mautner, L. Makasa & C. Sturmbauer, 2012. Genetic and morphological differentiation in the rock-dwelling and specialized shrimp-feeding cichlid fish species Altolamprologus compressiceps from Lake Tanganyika, East Africa. Hydrobiologia 682: 143–154.
Staeck, W., 1975. Noch einmal: Tropheus duboisi Marlier, 1959. Deutsche Cichliden-Gesellschaft-Informationen 6: 40–42.
Stamatakis, A., 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.
Stolz, H., 1974. Bericht über Besonderheiten. Deutsche Cichliden-Gesellschaft-Informationen 5: 154–157.
Sturmbauer, C. & A. Meyer, 1992. Genetic divergence, speciation and morphological stasis in a lineage of African cichlid fishes. Nature 358: 578–581.
Sturmbauer, C., U. Hainz, S. Baric, E. Verheyen & W. Salzburger, 2003. Evolution of the tribe tropheini from Lake Tanganyika: synchronised explosive speciation producing multiple evolutionary parallelism. Hydrobiologia 500: 51–64.
Sturmbauer, C., S. Koblmüller, K. M. Sefc & N. Duftner, 2005. Phylogeographic history of the genus Tropheus, a lineage of rock-dwelling cichlid fishes endemic to Lake Tanganyika. Hydrobiologica 542: 335–366.
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.
Tavaré, S., 1986. Some probabilistic and statistical problems in the analysis of DNA sequences. In Miura, R. M. (ed.), Some Mathematical Questions in Biology—DNA Sequence Analysis. American Mathematical Society, Providence: 57–86.
Theis, A., W. Salzburger & B. Egger, 2012. The function of anal fin egg-spots in the cichlid fish Astatotilapia burtoni. PLoS ONE 7(1): e29878.
Tiercelin, J.-J., C. Pflumio, M. Castrec, J. Boulège, P. Gente, J. Rolet, C. Coussement, K. O. Stetter, R. Huber, S. Buku & W. Mifundo, 1993. Hydrothermal vents in Lake Tanganyika, East African Rift system. Geology 21: 499–502.
Van Steenberge, M., M. P. M. Vanhove, D. Muzumani Risasi, T. Mulimbwa N’sibula, F. Muterezi Bukinga, A. Pariselle, C. Gillardin, E. Vreven, J. A. M. Raeymaekers, T. Huyse, F. A. M. Volckaert, V. Nshombo Muderhwa & J. Snoeks, 2011. A recent inventory of the fishes of the north-western and central western coast of Lake Tanganyika (Democratic Republic Congo). Acta Ichthyologica et Piscatoria 41: 201–214.
Verheyen, E., L. Rüber, J. Snoeks & A. Meyer, 1996. Mitochondrial phylogeography of rock-dwelling cichlid fishes reveals evolutionary influence of historical lake level fluctuations of Lake Tanganyika, Africa. Philosophical Transactions of the Royal Society B, Biological Sciences 351: 797–805.
Wake, D. B., G. Roth & M. H. Wake, 1983. On the problem of stasis in organismal evolution. Journal of Theoretical Biology 101: 211–224.
Ward, R. D., T. S. Zemlak, B. H. Innes, P. R. Last & P. D. N. Hebert, 2005. DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society B, Biological Sciences 360: 1847–1857.
Yanagisawa, Y., 1993. Long-term territory maintenance by female Tropheus duboisi (Cichlidae) involving foraging during the mouth-brooding period. Ecology of Freshwater Fish 2: 1–7.
Acknowledgments
We would like to thank C. Gillardin, J.A.M. Raeymaekers, D. Muzumani Risasi, T. Mulimbwa N’sibula, F. Muterezi Bukinga, V. Nshombo Muderhwa, J. Mbirize Ndalozibwa, A. Avenant-Oldewage, A. Pariselle and S. Risch for assistance during sampling, S. Loix for assistance in the lab, F. Van den Broeck for software support and T. Musschoot for creating the map. We would also like to thank M. Parrent, M. Schreyen (Fishes of Burundi), G. Ntakimazi (Université du Burundi), Ad Konings and H. Büscher (University of Basel) for their help in preparing this manuscript. MVS is a PhD fellow of the Research Foundation—Flanders (FWO—Vlaanderen). Fieldwork was partly funded by a travel grant from the King Leopold III Fund for Nature Conservation and Exploration.
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Guest editors: S. Koblmüller, R. C. Albertson, M. J. Genner, K. M. Sefc & T. Takahashi / Advances in Cichlid Research: Behavior, Ecology and Evolutionary Biology
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Van Steenberge, M., Vanhove, M.P.M., Breman, F.C. et al. Complex geographical variation patterns in Tropheus duboisi Marlier, 1959 (Perciformes, Cichlidae) from Lake Tanganyika. Hydrobiologia 748, 39–60 (2015). https://doi.org/10.1007/s10750-013-1692-5
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DOI: https://doi.org/10.1007/s10750-013-1692-5