, Volume 91, Issue 6, pp 277–290 | Cite as

The species flocks of East African cichlid fishes: recent advances in molecular phylogenetics and population genetics

  • Walter Salzburger
  • Axel Meyer


With more than 3,000 species, the fish family Cichlidae is one of the most species-rich families of vertebrates. Cichlids occur in southern and central America, Africa, Madagascar, and India. The hotspot of their biodiversity is East Africa, where they form adaptive radiations composed of hundreds of endemic species in several lakes of various sizes and ages. The unparalleled species richness of East African cichlids has been something of a conundrum for evolutionary biologists and ecologists, since it has been in doubt whether these hundreds of species arose by allopatric speciation or whether it is necessary to invoke somewhat less traditional models of speciation, such as micro-allopatric, peripatric, or even sympatric speciation or evolution through sexual selection mediated by female choice. Ernst Mayr’s analyses of these evolutionary uniquely diverse species assemblages have contributed to a more direct approach to this problem and have led to a deeper understanding of the patterns and processes that caused the formation of these huge groups of species. We review here recent molecular data on population differentiation and phylogenetics, which have helped to unravel, to some extent, the patterns and processes that led to the formation and ecological maintenance of cichlid species flocks. It is becoming apparent that sexually selected traits do play an important role in speciation in micro-allopatric or even sympatric settings. Species richness seems to be roughly correlated with the surface area, but not the age, of the lakes. We observe that the oldest lineages of a species flock of cichlids are often less species-rich and live in the open water or deepwater habitats. While the species flocks of the Lake Malawai and the Lake Victoria areas were shown to be monophyletic, the cichlid assemblage of Lake Tanganyika seems to consist of several independent species flocks. Cichlids emerge as an evolutionary model system in which many fundamental questions in evolution and ecology can be tested successfully, yet for other fish species flocks the relative importance of alternative mechanisms of speciation is likely to differ from that in cichlid fish.


Sexual Selection Cichlid Fish Allopatric Speciation Cichlid Species Ancient Lineage 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We wish to dedicate this article to Ernst Mayr, in great admiration and friendship and with our best wishes for his 100th birthday. We are grateful to M. Barluenga and the reviewers for valuable comments. We would also like to acknowledge the financial support of the Deutsche Forschungsgemeinschaft, the Landesstiftung Baden-Württemberg, and the Center for Junior Research Fellows at the University of Konstanz.


  1. Albertson RC, Markert JA, Danley PD, Kocher TD (1999) Phylogeny of a rapidly evolving clade: the cichlid fishes of Lake Malawi, East Africa. Proc Natl Acad Sci USA 96:5107–5110CrossRefPubMedGoogle Scholar
  2. Albertson RC, Streelman JT, Kocher TD (2003) Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes. Proc Natl Acad Sci USA 100:5252–5257CrossRefPubMedGoogle Scholar
  3. Allender CJ, Seehausen O, Knight ME, Turner GF, Maclean N (2003) Divergent selection during speciation of Lake Malawi cichlid fishes inferred from parallel radiations in nuptial coloration. Proc Natl Acad Sci USA 100:14074–14079CrossRefPubMedGoogle Scholar
  4. Arnegard ME, Markert JA, Danley PD, Stauffer JR, Ambali AJ, Kocher TD (1999) Population structure and colour variation of the cichlid fish Labeotropheus fuelleborni Ahl along a recently formed archipelago of rocky habitat patches in southern Lake Malawi. Proc R Soc Lond B Biol Sci 266:119–130CrossRefGoogle Scholar
  5. Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Evol Syst 18:459–522Google Scholar
  6. Baric S, Salzburger W, Sturmbauer C (2003) Phylogeography and evolution of the Tanganyikan cichlid genus Tropheus based upon mitochondrial DNA sequences. J Mol Evol 56:54–68CrossRefPubMedGoogle Scholar
  7. Barlow GW (2000) The cichlid fishes: Nature’s grand experiment in evolution. Perseus, Cambridge, Mass.Google Scholar
  8. Barluenga M, Meyer A (2004) The Midas cichlid species complex: incipient sympatric speciation in Nicaraguan crater lake cichlid fishes. Mol Ecol 13Google Scholar
  9. Beadle L (1974) The Inland waters of tropical Africa. Longman, LondonGoogle Scholar
  10. Booton GC, Kaufman L, Chandler M, Oguto-Ohwayo R, Duan W, Fuerst PA (1999) Evolution of the ribosomal RNA internal transcribed spacer one (ITS-1) in cichlid fishes of the Lake Victoria region. Mol Phylogenet Evol 11:273–282CrossRefPubMedGoogle Scholar
  11. Boulenger G (1898) Catalogue of the fresh-water fishes of Africa in the British Museum (Natural History). British Museum for Natural History, LondonGoogle Scholar
  12. Brooks JL (1950) Speciation in ancient lakes. Q Rev Biol 25:30–176CrossRefGoogle Scholar
  13. Cohen AS, Soreghan M, Scholz CA (1993) Estimating the age of formation of lakes: an example from Lake Tanganyika, East African Rift system. Geology 21:511–514CrossRefGoogle Scholar
  14. Cohen AS, Lezzar KE, Tiercelin JJ, Soreghan M (1997) New paleogeographic and lake-level reconstructions of Lake Tanganyika: implications for tectonic, climatic and biological evolution in a rift lake. Basin Res 7:107–132CrossRefGoogle Scholar
  15. Coulter GW (1991) Lake Tanganyika and its life. Oxford University Press, OxfordGoogle Scholar
  16. Danley PD, Kocher TD (2001) Speciation in rapidly diverging systems: lessons from Lake Malawi. Mol Ecol 10:1075–1086CrossRefPubMedGoogle Scholar
  17. Danley PD, Markert JA, Arnegard ME, Kocher TD (2000) Divergence with gene flow in the rock-dwelling cichlids of Lake Malawi. Evolution 54:1725–1737PubMedGoogle Scholar
  18. Delvaux D (1995) Age of Lake Malawi (Nyasa) and water level fluctuations. Mus R Afr Centr Tervuren (Belg.) Dept Geol Min Rapp Ann 1995–1996:99–108Google Scholar
  19. Deutsch JC (1997) Colour diversification in Malawi cichlids: evidence for adaptation, reinforcement or sexual selection? Biol J Linn Soc 62:1–14CrossRefGoogle Scholar
  20. Dieckmann U, Doebeli M (1999) On the origin of species by sympatric speciation. Nature 400:354–357CrossRefPubMedGoogle Scholar
  21. Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New YorkGoogle Scholar
  22. Dominey WJ (1984) Effects of sexual selection and life history on speciation: species flocks in African cichlids and Hawaiian Drosophila. In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. University of Maine at Orono Press, Orono, Me., pp 231–250Google Scholar
  23. Echelle AA, Kornfield I (1984) Evolution of fish species flocks. University of Maine at Orono Press, Orono, Me.Google Scholar
  24. Farias IP, Orti G, Meyer A (2000) Total evidence: molecules, morphology, and the phylogenetics of cichlid fishes. J Exp Zool 288:76–92CrossRefPubMedGoogle Scholar
  25. Farias IP, Orti G, Sampaio I, Schneider H, Meyer A (2001) The cytochrome b gene as a phylogenetic marker: the limits of resolution for analyzing relationships among cichlid fishes. J Mol Evol 53:89–103PubMedGoogle Scholar
  26. Fryer G (1997) Biological implications of a suggested Late Pleistocene desiccation of Lake Victoria. Hydrobiologia 354:177–182CrossRefGoogle Scholar
  27. Fryer G (2001) On the age and origin of the species flock of haplochromine cichlid fishes of Lake Victoria. Proc R Soc Lond B Biol Sci 268:1147–1152CrossRefPubMedGoogle Scholar
  28. Fryer G (2004) Speciation rates in lakes and the enigma of Lake Victoria. Hydrobiologia 515Google Scholar
  29. Fryer G, Iles TD (1972) The cichlid fishes of the Great Lakes of Africa: their biology and evolution. Oliver and Boyd, EdinburghGoogle Scholar
  30. Gavrilets S, Waxman D (2002) Sympatric speciation by sexual conflict. Proc Natl Acad Sci USA 99:10533–10538CrossRefPubMedGoogle Scholar
  31. Genner MJ, Seehausen O, Cleary DFR, Knight ME, Michel E, Turner GF (2004) How does the taxonomic status of allopatric populations influence species richness within African cichlid fish assemblages? J Biogeogr 31:93–102Google Scholar
  32. Goodwin NB, Balshine-Earn S, Reynolds JD (1998) Evolutionary transitions in parental care in cichlid fish. Proc R Soc Lond B Biol Sci 265:2265–2272CrossRefGoogle Scholar
  33. Greenwood PH (1973) Morphology, endemism and speciation in African cichlid fishes. Verh Dtsch Zool Ges 66:115–124Google Scholar
  34. Greenwood PH (1979) Towards a phyletic classification of the ‘genus’ Haplochromis (Pisces, Cichlidae) and related taxa. Bull Br Mus Nat Hist Zool 35:265–322Google Scholar
  35. Greenwood PH (1980) Towards a phyletic classification of the ‘genus’ Haplochromis (Pisces, Cichlidae) and related taxa. Part 2. Bull Br Mus Nat Hist Zool 39:1–99Google Scholar
  36. Greenwood PH (1984a) What is a species flock. In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. University of Maine at Orono Press, Orono, Me., pp 13–20Google Scholar
  37. Greenwood PH (1984b) African cichlids and evolutionary theories. In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. University of Maine at Orono Press, Orono, Me., pp 141–155Google Scholar
  38. Harvey PH, Rambaut A (2000) Comparative analyses for adaptive radiations. Philos Trans R Soc Lond B Biol Sci 355:1599–1605CrossRefPubMedGoogle Scholar
  39. Hey J, Won Y-J, Sivasundar A, Nielsen R, Markert JA (2004) Using nuclear haplotypes with microsatellites to study gene flow between recently separated cichlid species. Mol Ecol 13, 909–919Google Scholar
  40. Higashi M, Takimoto G, Yamamura N (1999) Sympatric speciation by sexual selection. Nature 402:523–526CrossRefPubMedGoogle Scholar
  41. Johnson TC, Ng’ang’a P (1990) Reflections on a rift lake. In: Katz BJ (ed) Lacustrine basin exploration: case studies and modern analogs. American Association of Petroleum Geologists Memoir, pp 113–135Google Scholar
  42. Johnson TC, Scholz CA, Talbot MR, Kelts K, Ricketts RD, Ngobi G, Beuning K, Ssemmanda II, McGill JW (1996) Late Pleistocene desiccation of Lake Victoria and rapid evolution of cichlid fishes. Science 273:1091–1093PubMedGoogle Scholar
  43. Klett V, Meyer A (2002) What, if anything, is a tilapia? Mitochondrial ND2 phylogeny of tilapiines and the evolution of parental care systems in the African cichlid fishes. Mol Biol Evol 19:865–883PubMedGoogle Scholar
  44. Knight ME, Turner GF, Rico C, Oppen MJ van, Hewitt GM (1998) Microsatellite paternity analysis on captive Lake Malawi cichlids supports reproductive isolation by direct mate choice. Mol Ecol 7:1605–1610CrossRefGoogle Scholar
  45. Koblmüller S, Salzburger W, Sturmbauer C (2004) Evolutionary 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 58:79–96CrossRefPubMedGoogle Scholar
  46. Kocher TD (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nature Rev Genet 5:288-298Google Scholar
  47. Kocher TD, Conroy JA, McKaye KR, Stauffer JR (1993) Similar morphologies of cichlid fish in lakes Tanganyika and Malawi are due to convergence. Mol Phylogenet Evol 2:158–165CrossRefPubMedGoogle Scholar
  48. Kocher TD, Conroy JA, McKaye KR, Stauffer JR, Lockwood SF (1995) Evolution of NADH dehydrogenase subunit 2 in East African cichlid fish. Mol Phylogenet Evol 4:420–432CrossRefPubMedGoogle Scholar
  49. Kocher TD, Fernald R, Hofmann H, Meyer A, Okada N, Penman DJ, Seehausen O (2004) Genome sequence of a cichlid fish: the Nile tilapia (Oreochromis niloticus). Proposal submitted to the JGI Community Sequencing Program by the Cichlid Genome Consortium: see
  50. Kondrashov AS, Kondrashov FA (1999) Interactions among quantitative traits in the course of sympatric speciation. Nature 400:351–354CrossRefPubMedGoogle Scholar
  51. Konings A (1990) Cichlids and all other fishes of Lake Malawi. THF, Neptune, N.J.Google Scholar
  52. Kornfield I, Smith PF (2000) African cichlid fishes: model systems for evolutionary biology. Annu Rev Ecol Syst 31:163–196CrossRefGoogle Scholar
  53. Kosswig C (1947) Selective mating as a factor speciation in cichlid fish of East African lakes. Nature 159:604Google Scholar
  54. Kosswig C (1963) Ways of speciation in cichlids. Copeia 1963:238–244Google Scholar
  55. Lezzar KE, Tiercelin JJ, De Batist M, Cohen AS, Bandora T, Van Regensbergen P, Le Turdu C, Mifundu W, Klerkx J (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 Res 8:1–28Google Scholar
  56. Liem KF (1973) Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws. Syst Zool 22:425–441Google Scholar
  57. Liem KF (1980) Adaptive significance of intra- and interspecific differences in the feeding repertoires of cichlid fishes. Am Zool 20:295–314Google Scholar
  58. Markert JA, Arnegard ME, Danley PD, Kocher TD (1999) Biogeography and population genetics of the Lake Malawi cichlid Melanochromis auratus: habitat transience, philopatry and speciation. Mol Ecol 8:1013–1026CrossRefGoogle Scholar
  59. Mayr E (1942) Systematics and the origin of species. Columbia University Press, New YorkGoogle Scholar
  60. Mayr E (1947) Ecological factors in speciation. Evolution 1:263–288Google Scholar
  61. Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge, Mass.Google Scholar
  62. Mayr E (1984) Evolution of fish species flocks: a commentary. In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. University of Maine at Orono Press, Orono, Me., pp 3–12Google Scholar
  63. Mayr E (2001) What evolution is. Basic books, New YorkGoogle Scholar
  64. Mayr E, Brock WJ (2002) Classifications and other ordering systems. J Zool Syst Evol Res 40:169–194CrossRefGoogle Scholar
  65. Meyer A (1989) Costs and benefits of morphological specialization: feeding performance in the trophically polymorphic Neotropical cichlid fish, Cichlasoma citrinellum. Oecologia 80:431–136Google Scholar
  66. Meyer A (1990a) Ecological and evolutionary aspects of the trophic polymorphism in Cichlasoma citrinellum (Pisces: Cichlidae). Biol J Linn Soc 39:279–299Google Scholar
  67. Meyer A (1990b) Morphometrics and allometry of the trophically polymorphic cichlid fish, Cichlasoma citrinellum: alternative adaptations and ontogenetic changes in shape. J Zool 221:237–260Google Scholar
  68. Meyer A (1993) Phylogenetic relationships and evolutionary processes in East African cichlids. Trends Ecol Evol 8:279–284CrossRefGoogle Scholar
  69. Meyer A, Kocher TD, Basasibwaki P, Wilson AC (1990) Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347:550–553CrossRefPubMedGoogle Scholar
  70. Meyer A, Montero C, Spreinat A (1994) Evolutionary history of the cichlid fish species flocks of the East African great lakes inferred from molecular phylogenetic data. Adv Limnol 44:409–425Google Scholar
  71. Meyer A, Knowles LL, Verheyen E (1996a) Widespread geographical distribution of mitochondrial haplotypes in rock-dwelling cichlid fishes from Lake Tanganyika. Mol Ecol 5:341–350CrossRefGoogle Scholar
  72. Meyer A, Montero CM, Spreinat A (1996b) Molecular phylogenetic inferences about the evolutionary history of the East African cichlid fish radiations. In: Johnson TC, Odada EO (eds) Limnology, climatology and paleoclimatology of the East African lakes. Gordon and Breach Scientific, Toronto, pp 303–323Google Scholar
  73. Moran P, Kornfield I (1993) Retention of an ancestral polymorphism in the Mbuna species flock (Teleostei: Cichlidae) of Lake Malawi. Mol Biol Evol 10:1015–1029Google Scholar
  74. Moran P, Kornfield I, Reinhal PN (1994) Molecular systematics and radiation of the haplochromine cichlids (Teleostei: Perciformes) of Lake Malawi. Copeia 2:274–288Google Scholar
  75. Nagl S, Tichy H, Mayer WE, Takahata N, Klein J (1998) Persistence of neutral polymorphisms in Lake Victoria cichlid fish. Proc Natl Acad Sci USA 95:14238–14243CrossRefPubMedGoogle Scholar
  76. Nagl S, Tichy H, Mayer WE, Takezaki N, Takahata N, Klein J (2000) The origin and age of haplochromine fishes in Lake Victoria, East Africa. Proc R Soc Lond B Biol Sci 267:1049–1061CrossRefPubMedGoogle Scholar
  77. Nee S, Holmes EC, May RM, Harvey PH (1994) Extinction rates can be estimated from molecular phylogenies. Philos Trans R Soc Lond B Biol Sci 344:77–82PubMedGoogle Scholar
  78. Nicholson SE (1999) Historical and modern fluctuations of Lakes Tanganyika and Rukwa and their relationships to rainfall variability. Climatic Change 41:53–71CrossRefGoogle Scholar
  79. Nishida M (1991) Lake Tanganyika as an evolutionary reservoir of old lineages of East African cichlid fishes: inferences from allozyme data. Experientia 47:974–979Google Scholar
  80. Oppen MJ van, Turner GF, Rico C, Deutsch JC, Ibrahim KM, Robinson RL, Hewitt GM (1997) Unusually fine-scale genetic structuring found in rapidly speciating Malawi cichlid fishes. Proc R Soc Lond B Biol Sci 264:1803–1812CrossRefGoogle Scholar
  81. Oppen MJ van, Turner GF, Rico C, Robinson RL, Deutsch JC, Genner MJ, Hewitt GM (1998) Assortative mating among rock-dwelling cichlid fishes supports high estimates of species richness from Lake Malawi. Mol Ecol 7:991–1001CrossRefGoogle Scholar
  82. Owen RB, Crossley R, Johnson TC, Tweddle D, Kornfield I, Davison S, Eccles DH, Engstrom DE (1990) Major low levels of Lake Malawi and implications for evolution rates in cichlid fishes. Proc R Soc Lond B Biol Sci 240:519–553Google Scholar
  83. Poll M (1986) Classification des Cichlidae du lac Tanganika: tribus, genres et espèces. Memoires de la classe des sciences. T. XLV. Fascicule 2 edn. Académie Royale de Belgique, BrusselsGoogle Scholar
  84. Pybus OG, Harvey PH (2000) Testing macro-evolutionary models using incomplete molecular phylogenies. Proc R Soc Lond B Biol Sci 267:2267–2272CrossRefPubMedGoogle Scholar
  85. Reinthal PN, Meyer A (1997) Molecular phylogenetic tests of speciation models in Lake Malawi cichlid fishes. In: Givinish TJ, Sytsma KJ (eds) Evolution and adaptive radiations. Cambridge University Press, Cambridge, pp 189–224Google Scholar
  86. Rensch B (1933) Zoologsiche Systematik und Artbildungsproblem. Verh Dtsch Zool Ges 1933:19–83Google Scholar
  87. Rico C, Turner GF (2002) Extreme microallopatric divergence in a cichlid species from Lake Malawi. Mol Ecol 11:1585–1590CrossRefPubMedGoogle Scholar
  88. Rico C, Bouteillon P, Oppen MJ van, Knight ME, Hewitt GM, Turner GF (2003) No evidence for parallel sympatric speciation in cichlid species of the genus Pseudotropheus from north-western Lake Malawi. J Evol Biol 16:37–46CrossRefGoogle Scholar
  89. Rossiter A (1995) The cichlid fish assemblages of Lake Tanganyika: ecology, behavior and evolution of its species flocks. Adv Ecol Res 26:157–252Google Scholar
  90. Rüber L, Verheyen E, Sturmbauer C, Meyer A (1998) Lake level fluctuations and speciation in rock-dwelling cichlid fish in Lake Tanganyika, East Africa. In: Grant PR (ed) Evolution on islands. Oxford University Press, New York, pp 225–240Google Scholar
  91. Rüber L, Verheyen E, Meyer A (1999) Replicated evolution of trophic specializations in an endemic cichlid fish lineage from Lake Tanganyika. Proc Natl Acad Sci USA 96:10230–10235CrossRefPubMedGoogle Scholar
  92. Rüber L, Meyer A, Sturmbauer C, Verheyen E (2001) Population structure in two sympatric species of the Lake Tanganyika cichlid tribe Eretmodini: evidence for introgression. Mol Ecol 10:1207–1225CrossRefPubMedGoogle Scholar
  93. Sage RD, Loiselle PV, Basasibwaki P, Wilson AC (1984) Molecular versus morphological change among cichlid fishes of Lake Victoria. In: Echelle AA, Kornfield I (eds) Evolution of fish species flocks. University of Maine at Orono Press, Orono, Me., pp 185–202Google Scholar
  94. Salzburger W, Meyer A, Baric S, Verheyen E, Sturmbauer C (2002a) Phylogeny of the Lake Tanganyika cichlid species flock and its relationship to the Central and East African haplochromine cichlid fish faunas. Syst Biol 51:113–135CrossRefPubMedGoogle Scholar
  95. Salzburger W, Baric S, Sturmbauer C (2002b) Speciation via introgressive hybridization in East African cichlids? Mol Ecol 11:619–625CrossRefGoogle Scholar
  96. Salzburger W, Verheyen E, Snoeks J, Meyer A (2004) Response to technical comment. Science (in press)Google Scholar
  97. Schliewen UK, Tautz D, Paabo S (1994) Sympatric speciation suggested by monophyly of crater lake cichlids. Nature 368:629–632CrossRefPubMedGoogle Scholar
  98. Schliewen U, Rassmann K, Markmann M, Markert J, Kocher T, Tautz D (2001) Genetic and ecological divergence of a monophyletic cichlid species pair under fully sympatric conditions in Lake Ejagham, Cameroon. Mol Ecol 10:1471–1488CrossRefPubMedGoogle Scholar
  99. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, New YorkGoogle Scholar
  100. Scholz CA, Rosendahl BR (1988) Low lake stands in Lakes Malawi and Tanganyika, East Africa, delineated with multifold seismic data. Science 240:1645–1648Google Scholar
  101. Seehausen O (1996) Lake Victoria rock cichlids: taxonomy, ecology, and distribution. Verdujin Cichlids, Zevenhuizen, The NetherlandsGoogle Scholar
  102. Seehausen O (2002) Patterns in fish radiation are compatible with Pleistocene desiccation of Lake Victoria and 14,600-year history for its cichlid species flock. Proc R Soc Lond B Biol Sci 269:491–470CrossRefPubMedGoogle Scholar
  103. Seehausen O, Alphen JJM van (1999) Can sympatric speciation by disruptive sexual selection explain rapid evolution of cichlids diversity in Lake Victoria? Ecol Lett 2:262–271CrossRefGoogle Scholar
  104. Seehausen O, Alphen JJM van, Witte F (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277:1808–1811CrossRefGoogle Scholar
  105. Seehausen O, Alphen JJM van, Lande R (1999) Color polymorphism and sex ratio distortion in a cichlid fish as an incipient stage in sympatric speciation by sexual selection. Ecol Lett 2:367–378CrossRefGoogle Scholar
  106. Seehausen O, Koetsier E, Schneider MV, Chapman LJ, Chapman CA, Knight ME, Turner GF, Alphen JJM van, Bills R (2003) Nuclear markers reveal unexpected genetic variation and a Congolese–Nilotic origin of the Lake Victoria cichlid species flock. Proc R Soc Lond B Biol Sci 270:129–137CrossRefPubMedGoogle Scholar
  107. Shaw PW, Turner GF, Idid MR, Robinson RL, Carvalho GR (2000) Genetic population structure indicates sympatric speciation of Lake Malawi pelagic cichlids. Proc R Soc Lond B Biol Sci 267:2273–2280CrossRefGoogle Scholar
  108. Smith PF, Konings A, Kornfield I (2003) Hybrid origin of a cichlid population in Lake Malawi: implications for genetic variation and species diversity. Mol Ecol 12:2497–2504CrossRefPubMedGoogle Scholar
  109. Snoeks J, Rüber L, Verheyen E (1994) The Tanganyika problem: comments on the taxonomy and distribution patterns of its cichlid fauna. In: Martens K, Goddeeris G, Coulter GW (eds) Speciation in ancient lakes. Schweizerbart’sche Verlagsdruckerei, Stuttgart, pp 355–372Google Scholar
  110. Sparks JS (2004) Molecular phylogeny and biogeography of the Malagasy and South Asian cichlids (Teleostei: Perciformes: Cichlidae). Mol Phylogenet Evol 30:599–614CrossRefPubMedGoogle Scholar
  111. Stauffer JR, Bowers NJ (1996) Evidence of hybridization between Cynotilapia afra and Pseudotropheus zebra (Teleostei: Cichlidae) following an intralacustrine translocation in Lake Malawi. Copeia 1996:203–208Google Scholar
  112. Stiassny MLJ, Meyer A (1999) Cichlids of the Rift Lakes. Sci Am 280(2):64–69Google Scholar
  113. Streelman JT, Danley PD (2003) The stages of vertebrate evolutionary radiation. Trends Ecol Evol 18:126–131CrossRefGoogle Scholar
  114. Streelman JT, Zardoya R, Meyer A, Karl SA (1998) Multilocus phylogeny of cichlid fishes (Pisces: Perciformes): evolutionary comparison of microsatellite and single-copy nuclear loci. Mol Biol Evol 15:798–808PubMedGoogle Scholar
  115. Streelman JT, Albertson RC, Kocher TD (2003a) Genome mapping of the orange blotch colour pattern in cichlid fishes. Mol Ecol 12:2465–2471CrossRefPubMedGoogle Scholar
  116. Streelman JT, Webb JF, Albertson RC, Kocher TD (2003b) The cusp of evolution and development: a model of cichlid tooth shape diversity. Evol Dev 5:600–608CrossRefPubMedGoogle Scholar
  117. 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):18–36CrossRefGoogle Scholar
  118. Sturmbauer C, Meyer A (1992) Genetic divergence, speciation and morphological stasis in a lineage of African cichlid fishes. Nature 358:578–581CrossRefPubMedGoogle Scholar
  119. Sturmbauer C, Verheyen E, Meyer A (1994) Mitochondrial phylogeny of the Lamprologini, the major substrate spawning lineage of cichlid fishes from Lake Tanganyika in Eastern Africa. Mol Biol Evol 11:691–703PubMedGoogle Scholar
  120. Sturmbauer C, Rüber L, Verheyen E, Meyer A (1997) Phylogeographic patterns in populations of cichlid fishes from rocky habitats in Lake Tanganyika. In: Kocher TD, Stepien C (eds) Molecular systematics of fishes. Academic Press, New York, pp 93–107Google Scholar
  121. Sturmbauer C, Baric S, Salzburger W, Rüber L, Verheyen E (2001) Lake level fluctuations synchronize genetic divergences of cichlid fishes in African lakes. Mol Biol Evol 18:144–154PubMedGoogle Scholar
  122. Sturmbauer C, Hainz U, Baric S, Verheyen E, Salzburger W (2003) Evolution of the tribe Tropheini from Lake Tanganyika: synchronized explosive speciation producing multiple evolutionary parallelism. Hydrobiologia 500:51–64CrossRefGoogle Scholar
  123. Takahashi K, Okada N (2002) Mosaic structure and retropositional dynamics during evolution of subfamilies of short interspersed elements in African cichlids. Mol Biol Evol 19:1303–1312PubMedGoogle Scholar
  124. Takahashi K, Terai Y, Nishida M, Okada N (1998) A 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 15:391–407PubMedGoogle Scholar
  125. Takahashi K, Nishida M, Yuma M, Okada N (2001a) Retroposition of the AFC family of SINEs (short interspersed repetitive elements) before and during the adaptive radiation of cichlid fishes in Lake Malawi and related inferences about phylogeny. J Mol Evol 53:496–507CrossRefPubMedGoogle Scholar
  126. Takahashi K, Terai Y, Nishida M, Okada N (2001b) 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 18:2057–2066PubMedGoogle Scholar
  127. Taylor MI, Verheyen E (2001) Microsatellite data reveals weak population substructuring in Copadichromis sp. ‘virginalis kajose’, a demersal cichlid from Lake Malawi, Africa. J Fish Biol 59:593–604CrossRefGoogle Scholar
  128. Taylor MI, Ruber L, Verheyen E (2001) Microsatellites reveal high levels of population substructuring in the species-poor Eretmodine cichlid lineage from Lake Tanganyika. Proc R Soc Lond B Biol Sci 268:803–808CrossRefGoogle Scholar
  129. Turner GF, Burrows MT (1995) A model of sympatric speciation by sexual selection. Proc R Soc Lond B Biol Sci 260:287–292Google Scholar
  130. Turner GF, Seehausen O, Knight ME, Allender CJ, Robinson RL (2001) How many species of cichlid fishes are there in African lakes? Mol Ecol 10:793–806CrossRefPubMedGoogle Scholar
  131. Verheyen E, Ruber L, Snoeks J, Meyer A (1996) Mitochondrial phylogeography of rock-dwelling cichlid fishes reveals evolutionary influence of historical lake level fluctuations of Lake Tanganyika, Africa. Philos Trans R Soc Lond B Biol Sci 351:797–805PubMedGoogle Scholar
  132. Verheyen E, Salzburger W, Snoeks J, Meyer A (2003) Origin of the superflock of cichlid fishes from Lake Victoria, East Africa. Science 300:325–329CrossRefPubMedGoogle Scholar
  133. Wilson AB, Noack-Kunnmann K, Meyer A (2000) Incipient speciation in sympatric Nicaraguan crater lake cichlid fishes: sexual selection versus ecological diversification. Proc R Soc Lond B Biol Sci 267:2133–2141CrossRefPubMedGoogle Scholar
  134. Woltereck R (1931) Wie entsteht eine endemische Rasse oder Art? Biol Zentralbl 51:231–253Google Scholar
  135. Worthington EB (1937) On the evolution of fish in the Great Lakes of Africa. Int Rev Ges Hydrol Hydrogr 35:304–317Google Scholar
  136. Worthington EB (1940) Geographical differentiation in fresh waters with special reference to fish. In: Huxley J (ed) The new systematics. Clarendon, Oxford, pp 287–302Google Scholar
  137. Zardoya R, Vollmer DM, Craddock C, Streelman JT, Karl S, Meyer A (1996) Evolutionary conservation of microsatellite flanking regions and their use in resolving the phylogeny of cichlid fishes (Pisces: Perciformes). Proc R Soc Lond B Biol Sci 263:1589–1598PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Lehrstuhl für Zoologie und Evolutionsbiologie, Fachbereich BiologieUniversität KonstanzKonstanzGermany

Personalised recommendations