Evolution of the tribe Tropheini from Lake Tanganyika: Synchronized explosive speciation producing multiple evolutionary parallelism

Hydrobiologia

Volumn 500, Issue , 2003, Pages 51-64

  Sturmbauer, Christian ^a   Hainz, Ursula ^b   Baric, Sanja ^c   Verheyen, Erik ^d   Salzburger, Walter ^e  

^a UNIVERSITY OF GRAZ   (Austria)

^b ST ANNA CHILDREN S HOSPITAL   (Austria)

^c Res Ctr Agric Forest Laimburg   (Italy)

^d ROYAL BELGIAN INSTITUTE OF NATURAL SCIENCES   (Belgium)

^e UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Adaptive radiation; Lake Tanganyika cichlid fishes; mtDNA sequences; Tropheini; Trophic specialization

Indexed keywords

BIODIVERSITY; ECOLOGY; FISHERIES; GENETIC ENGINEERING; MARINE BIOLOGY; ROCKS;

FOUNDER POPULATIONS; PHYLOGENETIC ANALYSES;

LAKES;

ADAPTIVE RADIATION; CICHLID; EVOLUTION; PHYLOGENY; SPECIATION (BIOLOGY);

AFRICA; EAST AFRICAN LAKES; LAKE TANGANYIKA; SUB-SAHARAN AFRICA;

CICHLIDAE; PISCES; VICTORIA;

EID: 0345331012     PISSN: 00188158     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1024680201436     Document Type: Article

References (77)

1. 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.
2. 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.
3. 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.
4. 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.
5. Brooks, J. L., 1950. Speciation in ancient lakes. Quarternal Rev. Biol. 25: 30-60, 131-176.
6. 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.
7. 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.
8. 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.
9. 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.
10. Danley, P. D. & T. D. Kocher, Speciation in rapidly diverging systems: lessons from lake Malawi. Mol. Ecol. 10: 1075-1086.
11. 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.
12. Galis, F. & J. A. J. Metz, 1998. Why are there so many cichlid species? Trends Ecol. Evol. 13: 2-3.
13. 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.
14. Gould, S. J., 1990. Wonderful Life. Hutchinson Radius, London.
15. 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.
16. Hanel, R. & C. Sturmbauer, 2000. Multiple recurrent evolution of trophic types in northeastern Atlantic sea breams (Sparidae, Percoidei). J. Mol. Evol. 50: 276-283.
17. Hasegawa, M., H. Kishino & T. Jano, 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22: 160-174.
18. 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.
19. 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.
20. 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.
21. 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.
22. 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.
23. 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.
24. 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.
25. 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.
26. Kornfield, I. & P. F. Smith, 2000. African Cichlid Fishes: Model Systems for Evolutionary Biology. Ann. Rev. Ecol. Syst. 31: 163-196.
27. Kosswig, C., 1947. Selective mating as a factor for speciation in cichlid fish of East African lakes. Nature 159: 604.
28. 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.
29. 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.
30. Liem, K. F., 1973. Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws. Syst. Zool. 22: 425-441.
31. Maddison, W. P., 1989. Reconstructing character evolution on polytomous cladograms. Cladistics 5: 365-377.
32. 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.
33. McKaye, K. R. & A. C. Marsh, 1983. Food switching by two specialised algae-scraping cichlid fishes in Lake Malawi, Africa. Oecologia 56: 245-248.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. Posada, D. & K. A. Crandall, 1998. Modeltest: testing the model of DNA stubstitution. Bioinformatics 14: 817-818.
44. Rensch, B., 1933. Zoologische Systematik und Artbildungsproblem. Verhandlungen der Deutschen Zoologischen Geselschaft 1933: 19-83.
45. 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.
46. Rossiter, A., 1995. The cichlid fish assemblages of Lake Tanganyika: ecology, behaviour and evolution of its species flocks. Adv. Ecol. Res. 26: 187-252.
47. 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.
48. 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.
49. Saitou, N. & M. Nei, 1987. The Neighbor-joining method: A new method for reconstructing Phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
50. Salzburger, W., S. Baric & C. Sturmbauer, 2002a. Speciation via introgressive hybridization in East African cichlids? Mol. Ecol. 11: 619-625.
51. 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.
52. Schliewen, U. K., D. Tautz & S. Pääbo, 1994. Sympatric speciation suggested by monophyly of crater lake cichlids. Nature 368: 629-632.
53. Schluter, D. & J. D. McPhail, 1992. Ecological character displacement and speciation in sticklebacks. Am. Nat. 140: 85-108.
54. Scholz, C. A. & B. Rosendahl, 1988. Low lake stands in Lakes Malawi and Tanganyika, delineated with multifold seismic data. Science 240: 1645-1648.
55. Seehausen, O., J. J. M. van Alphen & F. Witte, 1997. Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 227: 1808-1811.
56. Shimodaira, H. & M. Hasegawa, 1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16: 1114-1116.
57. 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.
58. Strimmer, K. & A. von Haeseler, 1996. Quartet Puzzling: A Quartet Maximum-Likelihood Method for Reconstructing Tree Topologies. Mol. Biol. Evol. 7: 964-969.
59. 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.
60. 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.
61. 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.
62. Sturmbauer C. & A. Meyer, 1992. Genetic divergence, speciation and morphological stasis in a lineage of African cichlid fishes. Nature 358: 578-581.
63. 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.
64. 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.
65. 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.
66. 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.
67. 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.
68. Swofford, D. L., 2000. PAUP*: Phylogenetic Analysis Using Prasimony (and other methods), beta version 4.0. Sinauer, Sunderland, MA.
69. 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.
70. Takezaki, N., A. Rzhetsky & M. Nei, 1995. Phylogenetic Test of the Molecular Clock and Linearized Trees. Mol. Biol. Evol. 12: 823-833.
71. 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.
72. 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.
73. 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.
74. 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.
75. 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.
76. 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.
77. 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.