Abstract
One of the most surprising outcomes of recent molecular studies on cichlid fishes of the three Great East African Lakes Victoria, Malawi and Tanganyika, was the stunning rapidity of speciation and cladogenesis at early stages of adaptive radiation. Despite their rapid pace, speciation events were so far intuitively assumed to proceed in a bifurcating and tree-like fashion, even if they could not be resolved by gene phylogenies due to a lack of resolution. On the basis of phylogenetic analyses of the Tropheini, a lineage of endemic rock-dwelling cichlid fishes from Lake Tanganyika, we suggest a pathway of explosive speciation that accounts for a non-bifurcating manner of cladogenesis. This pattern is likely to be the result of the contemporaneous origin of a multitude of founder populations in geographically isolated rock habitats among which gene flow was interrupted simultaneously by a major change of the lake habitat in the form of a rapid rise of the lake level. As a consequence, all new species arising from that vicariance event must exhibit almost equal genetic distances to each other, within the scope of genetic diversity of the founder population(s), even if the actual processes of subsequent speciation and eco-morphological diversification followed independent routes. Our phylogeny also suggests a high frequency of parallel evolution of equivalent trophic specialization in the Tropheini. This phenomenon seems to be an inherent feature of this pathway of speciation, due to the action of similar selective forces on the same set of species colonizing isolated habitats of the same type. Explosive speciation via synchronization of genetic divergence triggered by rapid environmental changes seems to be particularly likely to occur at advanced stages of adaptive radiation, when species are already adapted to particular habitats and have a reduced ability for dispersal.
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References
Baric, S. & C. Sturmbauer, 1999. Ecological parallelism and cryptic species in the genus Ophiothrix derived from mitochondrial DNA sequences. Mol. Phylogen. Evol. 11: 157–162.
Baric, S., W. Salzburger & C. Sturmbauer, 2003. Phylogeography and evolution of the Tanganyikan cichlid genus Tropheus based upon mitochondrial DNA sequences. J. Mol. Evol. 56: 54–68.
Boulenger, G., 1898, Report on the collection of Fishes made by Mr J. E. S. Moore in Tanganyika during his Expedition 1895–1896. Trans. Zool. Soc. Lond. 15: 1–30.
Brichard, P., 1978. Un cas d'isolement de substrats rocheux au milieu de fonds de sable dans le nord du lac Tanganyka. Rev. Zool. africaine 92: 518–524.
Brooks, J. L., 1950. Speciation in ancient lakes. Quarternal Rev. Biol. 25: 30–60, 131–176.
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.
Cohen, A. S., K.-E. Lezzar, J.-J. Tiercelin & M. Soreghan, 1997. New palaeogeographic and lake-level reconstructions of Lake Tanganyika: implications for tectonic, climatic and biological evolution in a rift lake. Basin Res. 9: 107–132.
Coulter, G. W., 1994. Speciation and fluctuating environments, with reference to ancient East African lakes. In Martens, K., B. Goddeeris & G. Coulter (eds), Advances in Limnology, Vol. 44, Speciation in ancient lakes. Schweizerbart'sche Verlagsbuchhandlung, Stuttgart: 127–337.
Coulter, G. W., B. R. Allanson, M. N. Bruton, P. H. Greenwood, R. C. Hart, P. B. N. Jackson & A. J. Ribbink, 1986. Unique qualities and special problems of the African great lakes. Environ. Biol. Fish. 17: 161–183.
Danley, P. D. & T. D. Kocher, Speciation in rapidly diverging systems: lessons from lake Malawi. Mol. Ecol. 10: 1075–1086.
Fryer, G. & T. D. Iles, 1972. The Cichlid Fishes of the Great Lakes of Afrika: Their Biology and Evolution, TFH Publications, Neptune City. 641 pp.
Galis, F. & J. A. J. Metz, 1998. Why are there so many cichlid species? Trends Ecol. Evol. 13: 2–3.
Genner, M. J., G. F. Turner & S. J. Hawkins, 1999. Foraging of rocky habitat cichlid fishes in Lake Malawi: coexistence through niche partitioning? Oecologia 121: 283–292.
Gould, S. J., 1990. Wonderful Life. Hutchinson Radius, London.
Greenwood, P. H., 1984. African cichlid fishes and evolutionary theories. In Echelle, A. A. & I. Kornfield (eds), Evolution of Fish Species Flocks. University of Maine at Orono Press, Orono: 141–154.
Hanel, R. & C. Sturmbauer, 2000. Multiple recurrent evolution of trophic types in northeastern Atlantic sea breams (Sparidae, Percoidei). J. Mol. Evol. 50: 276–283.
Hasegawa, M., H. Kishino & T. Jano, 1985. Dating of the humanape splitting by a molecular clock of mitochondrial DNA. J.Mol. Evol. 22: 160–174.
Hori, M., 1991. Feeding relationships among cichlid fishes in Lake Tanganyika: effects of intra-and interspecific variations of feeding behavior on their coexistence. Ecol. Int. Bull. 19: 89–101.
Jackman, T. D, A. Larson, K. de Queiroz & J. B. Losos, 1999. Phylogenetic relationships and tempo of early diversification in Anolis lizrads. Syst. Biol. 48: 254–285.
Johnson, T. C., C. A. Scholz, M. R. Talbot, K. Kelts, R. D. Ricketts, G. Ngobi, K. Beuning, I. Ssemmanda & J.W. McGill, 1996. Late pleistoceine dessiccation of Lake Victoria and rapid evolution of cichlid fishes. Science 273: 1091–1093.
Jukes, T. H. & C. R. Cantor, 1969. Evolution of protein molecules. In Munro, H. N. (ed.), Mammalian Protein Metabolism. Academic Press, New York: 21–132.
Kimura, M., 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111–120.
Kocher, T. D., W. K. Thomas, A. Meyer, S. V. Edwards, S. Pääbo, F. X. Villablanca & A. C. Wilson, 1989. Dynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primers. Proc. nat. Acad. Sci., U.S.A. 86: 6196–6200.
Kocher, T. D., J. A. Conroy, K. R. McKaye, & J. R. Stauffer, 1993. Similar morphologies of cichlid fishes in Lakes Tanganyika and Malawi are due to convergence. Mol. Phylogen. Evol. 2: 158–165.
Kocher, T. D., J. A. Conroy, K. R. McKaye, J. R. Stauffer & S. F. Lockwood, 1995. Evolution of NADH Dehydrogenase Subunit 2 in East African cichlid fishes. Mol. Phylogen. Evol. 4: 420–432.
Kornfield, I. & P. F. Smith, 2000. African Cichlid Fishes: Model Systems for Evolutionary Biology. Ann. Rev. Ecol. Syst. 31: 163–196.
Kosswig, C., 1947. Selective mating as a factor for speciation in cichlid fish of East African lakes. Nature 159: 604.
Lee, W. J., J. Konroy, W. H. Howell & T. D. Kocher, 1995. Structure and evolution of teleost mitochondrial control regions. J. Mol. Biol. 40: 1–13.
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-piston core evidence. Basin Res. 8: 1–28.
Liem, K. F., 1973. Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws. Syst. Zool. 22: 425–441.
Maddison, W. P., 1989. Reconstructing character evolution on polytomous cladograms. Cladistics 5: 365–377.
Mayr, E., 1984. Evolution of fish species flocks: a commentary. In Echelle, A. A. & I. Kornfield (eds), Evolution of Fish Species Flocks. University of Maine at Orono Press, Orono: 3–11.
McKaye, K. R. & A. C. Marsh, 1983. Food switching by two specialised algae-scraping cichlid fishes in Lake Malawi, Africa. Oecologia 56: 245–248.
Moran, P. & I. Kornfield, 1993. Retention of an ancestral polymorphism in the mbuna species flock (Pisces: Cichlidae) of Lake Malawi. Mol. Biol. Evol. 10: 1015–1029.
Meyer, A., T. D. Kocher, P. Basasibwaki & A. C. Wilson, 1990. Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347: 550–553.
Nagl, S., H. Tichy, W. E. Mayer, N. Takahata & J. Klein, 1998. Persistence of neutral polymorphisms in Lake Victoria cichlid fish. Proc. nat. Acad. Sci., U.S.A. 95: 14238–14243.
Nagl, S., H. Tichy, W. E. Mayer, N. Takezaki, N. Takahata & J. Klein, 2000. The origin and age of haplochromine fishes in Lake Victoria, East Africa. Proc. R. Soc. Lond. B 267: 1–12.
Nishida, M., 1997. Phylogenetic relationships and evolution of Lake Tanganyika cichlids: a molecular perspective. In Kawanabe, H., M. Hori & M. Nagoshi (eds), Fish Communities in Lake Tanganyika. Kyoto University Press: 1–24.
O'hUigin, C., Y. Satta, N. Takahata & J. Klein, 2002. Contribution of homoplasy and of ancient polymorphism to the evolution of genes in anthropoid primates. Mol. Biol. Evol. 19: 1501–1513.
Owen, R. B., R. Crossley, T. C. Johnson, D. Tweddle, I. Kornfield, S. Davison, D. H. Eccles & D. E. Endstrom, 1990. Major low levels of Lake Malawi and their implications for speciation rates in cichlid fishes. Proc. R. Soc. Lond. B 240: 519–553.
Parker, A. & I. Kornfield, 1997. Evolution of the mitochondrial DNA control region in the mbuna (Cichlidae) species flock of Lake Malawi, East Africa. J. Mol. Evol. 45: 70–83.
Poll, M., 1986. Classification des cichlidae du lac Tanganika. Tribus, Genres et Espèces (Bruxelles, Belgium). Mémoires de la Classe des Sciences Académie Royal de Belgique 45: 1–63.
Posada, D. & K. A. Crandall, 1998. Modeltest: testing the model of DNA stubstitution. Bioinformatics 14: 817–818.
Rensch, B., 1933. Zoologische Systematik und Artbildungsproblem. Verhandlungen der Deutschen Zoologischen Geselschaft 1933: 19–83.
Ribbink, A. J., 1994. Alternative perspectives on some controversial aspects of cichlid fish speciation. In Martens, K., B. Goddeeris & G. Coulter (eds), Advances in Limnology Vol. 44, Speciation in Ancient Lakes. Schweizerbart'sche Verlagsbuchhandlung, Stuttgart: 101–125.
Rossiter, A., 1995. The cichlid fish assemblages of Lake Tanganyika: ecology, behaviour and evolution of its species flocks. Adv. Ecol. Res. 26: 187–252.
Rüber, L., E. Verheyen, C. Sturmbauer & A. Meyer, 1998. Lake level fluctuations and speciation in a rock-dwelling cichlid tribe endemic to Lake Tanganyika. In Grant, P. & B. Clarke (eds), Evolution on Islands. Oxford University Press, Oxford: 225–240.
Rüber, L., E. Verheyen & A. Meyer, 1999. Replicated evolution of trophic specializations in an endemic cichlid lineage from Lake Tanganyika. Proc. nat. Acad. Sci. U.S.A. 96: 10230–10235.
Saitou, N. & M. Nei, 1987. The Neighbor-joining method: A new method for reconstructing Phylogenetic trees. Mol. Biol. Evol. 4: 406–425.
Salzburger, W., S. Baric & C. Sturmbauer, 2002a. Speciation via introgressive hybridization in East African cichlids? Mol. Ecol. 11: 619–625.
Salzburger, W., A. Meyer, S. Baric, E. Verheyen & C. Sturmbauer, 2002b. Phylogeny of the Lake Tanganyika cichlid species flock and its relationships to the Central and East African haplochromine cichlis fish faunas. Syst. Biol. 51: 113–135.
Schliewen, U. K., D. Tautz & S. Pääbo, 1994. Sympatric speciation suggested by monophyly of crater lake cichlids. Nature 368: 629–632.
Schluter, D. & J. D. McPhail, 1992. Ecological character displacement and speciation in sticklebacks. Am. Nat. 140: 85–108.
Scholz, C. A. & B. Rosendahl, 1988. Low lake stands in Lakes Malawi and Tanganyika, delineated with multifold seismic data. Science 240: 1645–1648.
Seehausen, O., J. J. M. van Alphen & F. Witte, 1997. Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 227: 1808–1811.
Shimodaira, H. & M. Hasegawa, 1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16: 1114–1116.
Snoeks, J., L. Rüber & E. Verheyen, 1994. The Tanganyika problem: comments on the taxonomy and distribution patterns of its cichlid fauna. In Martens, K., B. Goddeeris & G. Coulter (eds), Advances in Limnology Vol. 44, Speciation in Ancient Lakes.Schweizerbart'sche Verlagsbuchhandlung, Stuttgart: 335–372.
Strimmer, K. & A. von Haeseler, 1996. Quartet Puzzling: A Quartet Maximum-Likelihood Method for Reconstructing Tree Topologies. Mol. Biol. Evol. 7: 964–969.
Strimmer, K. & A. von Haeseler, 1997. Likelihood mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proc. nat. Acad. Sci. U.S.A. 94: 6815–6819.
Sturmbauer, C., 1998. Explosive Speciation in cichlid fishes of the African Great Lakes: a dynamic model of adaptive radiation. J. Fish Biol. 53, Suppl. A: 18–36.
Sturmbauer, C., W. Mark & R. Dallinger, 1992. Ecophysiology of Aufwuchs eating cichlids in Lake Tanganyika: niche separation by trophic specialization. Environ. Biol. Fish. 35: 283–290.
Sturmbauer C. & A. Meyer, 1992. Genetic divergence, speciation and morphological stasis in a lineage of African cichlid fishes. Nature 358: 578–581.
Sturmbauer, C. & A. Meyer, 1993. Mitochondrial phylogeny of the endemic mouthbrooding lineages of cichlid fishes of Lake Tanganyika, East Afrika. Mol. Biol. Evol. 10: 751–768.
Sturmbauer, C., E. Verheyen & A. Meyer, 1994. Mitochondrial phylogeny of the Lamprologini, the major substrate spawning lineage of cichlid fishes from Lake Tanganyika in eastern Afrika. Mol. Biol. Evol. 11: 691–703.
Sturmbauer, C. & R. Dallinger, 1995. Diurnal variation of spacing and foraging behaviour in Tropheus moorii (Cichlidae) in Lake Tanganyika. Neth. J. Zool. 45: 386–401.
Sturmbauer, C., E. Verheyen, L. Rüber & A. Meyer, 1997. Phylogeographic patterns in populations of cichlid fishes from rocky habitats in Lake Tanganyika. In Kocher, T. D. & C. Stepien (eds), Molecular Phylogeny of Fishes. Academic Press, San Diego: 97–111.
Sturmbauer, C., S. Baric, W. Salzburger, L. Rüber & E. Verheyen, 2001. Lake Level Fluctuations Synchronize Genetic Divergence of Cichlid Fishes in African Lakes. Mol. Biol. Evol. 18: 144–154.
Swofford, D. L., 2000. PAUP✻: Phylogenetic Analysis Using Prasimony (and other methods), beta version 4.0. Sinauer, Sunderland, MA.
Takahashi, K., Y. Terai, M. Nishida & N. Okada, 2001. Phylogenetic relationships and ancient incomplete lineage sorting among cichlid fishes in Lake Tanganyika as revealed by analysis of the insertion of retroposons. Mol. Biol. Evol. 18: 2057–2066.
Takezaki, N., A. Rzhetsky & M. Nei, 1995. Phylogenetic Test of the Molecular Clock and Linearized Trees. Mol. Biol. Evol. 12: 823–833.
Taylor, E. B. & J. D. McPahil, 2000. Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus. Proc. R. Soc. Lond. B 7: 2375–2384.
Thompson, J. D., D. G. Higgins & T. J. Gibson, 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment trough sequence weighting, position-specific gap penalties and weight matrix choice. Nucelic Acids Res. 22: 4673–4680.
Tiercelin, J.-J. & A. Mondeguer, 1991. The geology of the Tanganyika trough. In Coulter, G. W. (ed.), Lake Tanganyika and its Life. Oxford University Press, Oxford: 7–48.
Turner, G. F., 1994. Speciation mechanisms in Lake Malawi cichlids: a critical review. In Martens, K., B. Goddeeris & G. Coulter (eds), Advances in Limnology Vol. 44, Speciation in Ancient Lakes. Schweizerbart'sche Verlagsbuchhandlung, Stuttgart: 139–160.
Verheyen, E., L. Rüber, J. Snoeks & A. Meyer, 1996. Mitochondrial phylogeny of rock-dwelling cichlid fishes reveals evolutionary influence of historical lake level fluctuations of Lake Tanganyika, Africa. Phil. Trans. R. Soc. Lond. B 351: 797–805.
Verheyen, E.,W. Salzburger, J. Snoeks & A. Meyer, 2003. Origin of the superflock of cichlid fishes from Lake Victoria, East Africa. Science 300: 325–329.
Yamaoka, K. A., 1983. A Revision of the Cichlid Fish Genus Petrochromis from Lake Tanganyika, with Description of a New Species. Jap. J. Ichthyol. 30: 129–141.
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Sturmbauer, C., Hainz, U., Baric, S. et al. Evolution of the tribe Tropheini from Lake Tanganyika: synchronized explosive speciation producing multiple evolutionary parallelism. Hydrobiologia 500, 51–64 (2003). https://doi.org/10.1023/A:1024680201436
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DOI: https://doi.org/10.1023/A:1024680201436