Skip to main content

Advertisement

SpringerLink
Log in

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

  • Review
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1A, B
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • 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 96:5107–5110

    Article  CAS  PubMed  Google Scholar 

  • Albertson RC, Streelman JT, Kocher TD (2003) Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes. Proc Natl Acad Sci USA 100:5252–5257

    Article  CAS  PubMed  Google Scholar 

  • 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 100:14074–14079

    Article  CAS  PubMed  Google Scholar 

  • 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 266:119–130

    Article  Google Scholar 

  • 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 18:459–522

    Google Scholar 

  • Baric S, Salzburger W, Sturmbauer C (2003) Phylogeography and evolution of the Tanganyikan cichlid genus Tropheus based upon mitochondrial DNA sequences. J Mol Evol 56:54–68

    Article  CAS  PubMed  Google Scholar 

  • Barlow GW (2000) The cichlid fishes: Nature’s grand experiment in evolution. Perseus, Cambridge, Mass.

    Google Scholar 

  • Barluenga M, Meyer A (2004) The Midas cichlid species complex: incipient sympatric speciation in Nicaraguan crater lake cichlid fishes. Mol Ecol 13

    Google Scholar 

  • Beadle L (1974) The Inland waters of tropical Africa. Longman, London

  • 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 11:273–282

    Article  CAS  PubMed  Google Scholar 

  • Boulenger G (1898) Catalogue of the fresh-water fishes of Africa in the British Museum (Natural History). British Museum for Natural History, London

  • Brooks JL (1950) Speciation in ancient lakes. Q Rev Biol 25:30–176

    Article  Google Scholar 

  • Cohen AS, Soreghan M, Scholz CA (1993) Estimating the age of formation of lakes: an example from Lake Tanganyika, East African Rift system. Geology 21:511–514

    Article  CAS  Google Scholar 

  • 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 7:107–132

    Article  Google Scholar 

  • Coulter GW (1991) Lake Tanganyika and its life. Oxford University Press, Oxford

  • Danley PD, Kocher TD (2001) Speciation in rapidly diverging systems: lessons from Lake Malawi. Mol Ecol 10:1075–1086

    Article  CAS  PubMed  Google Scholar 

  • Danley PD, Markert JA, Arnegard ME, Kocher TD (2000) Divergence with gene flow in the rock-dwelling cichlids of Lake Malawi. Evolution 54:1725–1737

    CAS  PubMed  Google Scholar 

  • Delvaux D (1995) Age of Lake Malawi (Nyasa) and water level fluctuations. Mus R Afr Centr Tervuren (Belg.) Dept Geol Min Rapp Ann 1995–1996:99–108

  • Deutsch JC (1997) Colour diversification in Malawi cichlids: evidence for adaptation, reinforcement or sexual selection? Biol J Linn Soc 62:1–14

    Article  Google Scholar 

  • Dieckmann U, Doebeli M (1999) On the origin of species by sympatric speciation. Nature 400:354–357

    Article  CAS  PubMed  Google Scholar 

  • Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New York

  • 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 231–250

  • Echelle AA, Kornfield I (1984) Evolution of fish species flocks. University of Maine at Orono Press, Orono, Me.

  • Farias IP, Orti G, Meyer A (2000) Total evidence: molecules, morphology, and the phylogenetics of cichlid fishes. J Exp Zool 288:76–92

    Article  CAS  PubMed  Google Scholar 

  • 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 53:89–103

    CAS  PubMed  Google Scholar 

  • Fryer G (1997) Biological implications of a suggested Late Pleistocene desiccation of Lake Victoria. Hydrobiologia 354:177–182

    Article  Google Scholar 

  • 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 268:1147–1152

    Article  CAS  PubMed  Google Scholar 

  • Fryer G (2004) Speciation rates in lakes and the enigma of Lake Victoria. Hydrobiologia 515

  • Fryer G, Iles TD (1972) The cichlid fishes of the Great Lakes of Africa: their biology and evolution. Oliver and Boyd, Edinburgh

    Google Scholar 

  • Gavrilets S, Waxman D (2002) Sympatric speciation by sexual conflict. Proc Natl Acad Sci USA 99:10533–10538

    Article  CAS  PubMed  Google Scholar 

  • 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 31:93–102

    Google Scholar 

  • Goodwin NB, Balshine-Earn S, Reynolds JD (1998) Evolutionary transitions in parental care in cichlid fish. Proc R Soc Lond B Biol Sci 265:2265–2272

    Article  Google Scholar 

  • Greenwood PH (1973) Morphology, endemism and speciation in African cichlid fishes. Verh Dtsch Zool Ges 66:115–124

    Google Scholar 

  • Greenwood PH (1979) Towards a phyletic classification of the ‘genus’ Haplochromis (Pisces, Cichlidae) and related taxa. Bull Br Mus Nat Hist Zool 35:265–322

    Google Scholar 

  • Greenwood PH (1980) Towards a phyletic classification of the ‘genus’ Haplochromis (Pisces, Cichlidae) and related taxa. Part 2. Bull Br Mus Nat Hist Zool 39:1–99

    Google Scholar 

  • 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 13–20

  • 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 141–155

  • Harvey PH, Rambaut A (2000) Comparative analyses for adaptive radiations. Philos Trans R Soc Lond B Biol Sci 355:1599–1605

    Article  CAS  PubMed  Google Scholar 

  • 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, 909–919

    Google Scholar 

  • Higashi M, Takimoto G, Yamamura N (1999) Sympatric speciation by sexual selection. Nature 402:523–526

    Article  CAS  PubMed  Google Scholar 

  • 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 113–135

  • 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 273:1091–1093

    CAS  PubMed  Google Scholar 

  • 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 19:865–883

    CAS  PubMed  Google Scholar 

  • 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 7:1605–1610

    Article  Google Scholar 

  • 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 58:79–96

    Article  PubMed  Google Scholar 

  • Kocher TD (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nature Rev Genet 5:288-298

    Google Scholar 

  • 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 2:158–165

    Article  CAS  PubMed  Google Scholar 

  • 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 4:420–432

    Article  CAS  PubMed  Google Scholar 

  • 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 http://www.hcgs.unh.edu/cichlid/

  • Kondrashov AS, Kondrashov FA (1999) Interactions among quantitative traits in the course of sympatric speciation. Nature 400:351–354

    Article  CAS  PubMed  Google Scholar 

  • Konings A (1990) Cichlids and all other fishes of Lake Malawi. THF, Neptune, N.J.

  • Kornfield I, Smith PF (2000) African cichlid fishes: model systems for evolutionary biology. Annu Rev Ecol Syst 31:163–196

    Article  Google Scholar 

  • Kosswig C (1947) Selective mating as a factor speciation in cichlid fish of East African lakes. Nature 159:604

    Google Scholar 

  • Kosswig C (1963) Ways of speciation in cichlids. Copeia 1963:238–244

    Google Scholar 

  • 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 8:1–28

    Google Scholar 

  • Liem KF (1973) Evolutionary strategies and morphological innovations: cichlid pharyngeal jaws. Syst Zool 22:425–441

    Google Scholar 

  • Liem KF (1980) Adaptive significance of intra- and interspecific differences in the feeding repertoires of cichlid fishes. Am Zool 20:295–314

    Google Scholar 

  • 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 8:1013–1026

    Article  Google Scholar 

  • Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York

  • Mayr E (1947) Ecological factors in speciation. Evolution 1:263–288

    Google Scholar 

  • Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge, Mass.

  • 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 3–12

  • Mayr E (2001) What evolution is. Basic books, New York

  • Mayr E, Brock WJ (2002) Classifications and other ordering systems. J Zool Syst Evol Res 40:169–194

    Article  Google Scholar 

  • Meyer A (1989) Costs and benefits of morphological specialization: feeding performance in the trophically polymorphic Neotropical cichlid fish, Cichlasoma citrinellum. Oecologia 80:431–136

    Google Scholar 

  • Meyer A (1990a) Ecological and evolutionary aspects of the trophic polymorphism in Cichlasoma citrinellum (Pisces: Cichlidae). Biol J Linn Soc 39:279–299

    Google Scholar 

  • Meyer A (1990b) Morphometrics and allometry of the trophically polymorphic cichlid fish, Cichlasoma citrinellum: alternative adaptations and ontogenetic changes in shape. J Zool 221:237–260

    Google Scholar 

  • Meyer A (1993) Phylogenetic relationships and evolutionary processes in East African cichlids. Trends Ecol Evol 8:279–284

    Article  Google Scholar 

  • Meyer A, Kocher TD, Basasibwaki P, Wilson AC (1990) Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347:550–553

    Article  CAS  PubMed  Google Scholar 

  • 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 44:409–425

    Google Scholar 

  • Meyer A, Knowles LL, Verheyen E (1996a) Widespread geographical distribution of mitochondrial haplotypes in rock-dwelling cichlid fishes from Lake Tanganyika. Mol Ecol 5:341–350

    Article  CAS  Google Scholar 

  • 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 303–323

  • Moran P, Kornfield I (1993) Retention of an ancestral polymorphism in the Mbuna species flock (Teleostei: Cichlidae) of Lake Malawi. Mol Biol Evol 10:1015–1029

    CAS  Google Scholar 

  • Moran P, Kornfield I, Reinhal PN (1994) Molecular systematics and radiation of the haplochromine cichlids (Teleostei: Perciformes) of Lake Malawi. Copeia 2:274–288

    Google Scholar 

  • 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 95:14238–14243

    Article  CAS  PubMed  Google Scholar 

  • 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 267:1049–1061

    Article  CAS  PubMed  Google Scholar 

  • 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 344:77–82

    CAS  PubMed  Google Scholar 

  • Nicholson SE (1999) Historical and modern fluctuations of Lakes Tanganyika and Rukwa and their relationships to rainfall variability. Climatic Change 41:53–71

    Article  Google Scholar 

  • Nishida M (1991) Lake Tanganyika as an evolutionary reservoir of old lineages of East African cichlid fishes: inferences from allozyme data. Experientia 47:974–979

    Google Scholar 

  • 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 264:1803–1812

    Article  Google Scholar 

  • 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 7:991–1001

    Article  Google Scholar 

  • 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 240:519–553

    Google Scholar 

  • 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, Brussels

    Google Scholar 

  • Pybus OG, Harvey PH (2000) Testing macro-evolutionary models using incomplete molecular phylogenies. Proc R Soc Lond B Biol Sci 267:2267–2272

    Article  CAS  PubMed  Google Scholar 

  • 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 189–224

  • Rensch B (1933) Zoologsiche Systematik und Artbildungsproblem. Verh Dtsch Zool Ges 1933:19–83

    Google Scholar 

  • Rico C, Turner GF (2002) Extreme microallopatric divergence in a cichlid species from Lake Malawi. Mol Ecol 11:1585–1590

    Article  CAS  PubMed  Google Scholar 

  • 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 16:37–46

    Article  CAS  Google Scholar 

  • Rossiter A (1995) The cichlid fish assemblages of Lake Tanganyika: ecology, behavior and evolution of its species flocks. Adv Ecol Res 26:157–252

    Google Scholar 

  • 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 225–240

  • 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 96:10230–10235

    Article  PubMed  Google Scholar 

  • 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 10:1207–1225

    Article  PubMed  Google Scholar 

  • 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 185–202

  • 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 51:113–135

    Article  PubMed  Google Scholar 

  • Salzburger W, Baric S, Sturmbauer C (2002b) Speciation via introgressive hybridization in East African cichlids? Mol Ecol 11:619–625

    Article  CAS  Google Scholar 

  • Salzburger W, Verheyen E, Snoeks J, Meyer A (2004) Response to technical comment. Science (in press)

  • Schliewen UK, Tautz D, Paabo S (1994) Sympatric speciation suggested by monophyly of crater lake cichlids. Nature 368:629–632

    Article  CAS  PubMed  Google Scholar 

  • 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 10:1471–1488

    Article  CAS  PubMed  Google Scholar 

  • Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, New York

  • Scholz CA, Rosendahl BR (1988) Low lake stands in Lakes Malawi and Tanganyika, East Africa, delineated with multifold seismic data. Science 240:1645–1648

    Google Scholar 

  • Seehausen O (1996) Lake Victoria rock cichlids: taxonomy, ecology, and distribution. Verdujin Cichlids, Zevenhuizen, The Netherlands

    Google Scholar 

  • 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 269:491–470

    Article  PubMed  Google Scholar 

  • Seehausen O, Alphen JJM van (1999) Can sympatric speciation by disruptive sexual selection explain rapid evolution of cichlids diversity in Lake Victoria? Ecol Lett 2:262–271

    Article  Google Scholar 

  • Seehausen O, Alphen JJM van, Witte F (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277:1808–1811

    Article  CAS  Google Scholar 

  • 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 2:367–378

    Article  Google Scholar 

  • 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 270:129–137

    Article  PubMed  Google Scholar 

  • 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 267:2273–2280

    Article  CAS  Google Scholar 

  • 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 12:2497–2504

    Article  PubMed  Google Scholar 

  • 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 355–372

  • Sparks JS (2004) Molecular phylogeny and biogeography of the Malagasy and South Asian cichlids (Teleostei: Perciformes: Cichlidae). Mol Phylogenet Evol 30:599–614

    Article  CAS  PubMed  Google Scholar 

  • Stauffer JR, Bowers NJ (1996) Evidence of hybridization between Cynotilapia afra and Pseudotropheus zebra (Teleostei: Cichlidae) following an intralacustrine translocation in Lake Malawi. Copeia 1996:203–208

    Google Scholar 

  • Stiassny MLJ, Meyer A (1999) Cichlids of the Rift Lakes. Sci Am 280(2):64–69

    Google Scholar 

  • Streelman JT, Danley PD (2003) The stages of vertebrate evolutionary radiation. Trends Ecol Evol 18:126–131

    Article  Google Scholar 

  • 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 15:798–808

    CAS  PubMed  Google Scholar 

  • Streelman JT, Albertson RC, Kocher TD (2003a) Genome mapping of the orange blotch colour pattern in cichlid fishes. Mol Ecol 12:2465–2471

    Article  CAS  PubMed  Google Scholar 

  • Streelman JT, Webb JF, Albertson RC, Kocher TD (2003b) The cusp of evolution and development: a model of cichlid tooth shape diversity. Evol Dev 5:600–608

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sturmbauer C, Meyer A (1992) Genetic divergence, speciation and morphological stasis in a lineage of African cichlid fishes. Nature 358:578–581

    Article  CAS  PubMed  Google Scholar 

  • 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 11:691–703

    CAS  PubMed  Google Scholar 

  • 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 93–107

  • 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 18:144–154

    CAS  PubMed  Google Scholar 

  • 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 500:51–64

    Article  Google Scholar 

  • Takahashi K, Okada N (2002) Mosaic structure and retropositional dynamics during evolution of subfamilies of short interspersed elements in African cichlids. Mol Biol Evol 19:1303–1312

    CAS  PubMed  Google Scholar 

  • 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 15:391–407

    CAS  PubMed  Google Scholar 

  • 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 53:496–507

    Article  CAS  PubMed  Google Scholar 

  • 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 18:2057–2066

    CAS  PubMed  Google Scholar 

  • 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 59:593–604

    Article  Google Scholar 

  • 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 268:803–808

    Article  CAS  Google Scholar 

  • Turner GF, Burrows MT (1995) A model of sympatric speciation by sexual selection. Proc R Soc Lond B Biol Sci 260:287–292

    Google Scholar 

  • Turner GF, Seehausen O, Knight ME, Allender CJ, Robinson RL (2001) How many species of cichlid fishes are there in African lakes? Mol Ecol 10:793–806

    Article  CAS  PubMed  Google Scholar 

  • 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 351:797–805

    CAS  PubMed  Google Scholar 

  • Verheyen E, Salzburger W, Snoeks J, Meyer A (2003) Origin of the superflock of cichlid fishes from Lake Victoria, East Africa. Science 300:325–329

    Article  CAS  PubMed  Google Scholar 

  • 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 267:2133–2141

    Article  CAS  PubMed  Google Scholar 

  • Woltereck R (1931) Wie entsteht eine endemische Rasse oder Art? Biol Zentralbl 51:231–253

    Google Scholar 

  • Worthington EB (1937) On the evolution of fish in the Great Lakes of Africa. Int Rev Ges Hydrol Hydrogr 35:304–317

    Google Scholar 

  • Worthington EB (1940) Geographical differentiation in fresh waters with special reference to fish. In: Huxley J (ed) The new systematics. Clarendon, Oxford, pp 287–302

  • 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 263:1589–1598

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Lehrstuhl für Zoologie und Evolutionsbiologie, Fachbereich Biologie, Universität Konstanz, 78457, Konstanz, Germany

    Walter Salzburger & Axel Meyer

Authors
  1. Walter Salzburger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Axel Meyer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Axel Meyer.

Additional information

Dedicated to Prof. Ernst Mayr

Rights and permissions

Reprints and permissions

About this article

Cite this article

Salzburger, W., Meyer, A. The species flocks of East African cichlid fishes: recent advances in molecular phylogenetics and population genetics. Naturwissenschaften 91, 277–290 (2004). https://doi.org/10.1007/s00114-004-0528-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-004-0528-6

Keywords

Search

Navigation