Major environmental changes can trigger dramatic evolutionary change. Lake Malawi contains an adaptive radiation of more than 800 haplochromine species that have evolved within the last 2–4 million years. Using mitochondrial DNA sequences, we reconstructed temporal changes in effective size of 46 populations from 28 species within the flock. All populations showed expansions within the last million years, but timescales differed substantially. Offshore pelagic species of the genera Diplotaxodon and Rhamphochromis underwent rapid population expansions on average 175,000 and 290,000 years ago, respectively. By contrast, shallow-water benthic-living species underwent rapid population expansions within the last 50,000 years. These results suggest that populations of pelagic taxa persisted through major Pleistocene megadroughts between 160,000 and 90,000 years ago when the lake was smaller, shallower, more saline and turbid. They also suggest that populations of inshore demersal taxa were smaller or absent during these low stands, only expanding when the lake rose towards present levels. Given many shallow-water and benthic-living haplochromine species in Lake Malawi exhibit extreme local endemism, we suggest that many have originated since the last major lake rise. Such new ecological opportunity may have been critical for the evolution of high cichlid species richness that now characterises littoral habitats.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Albertson, R. C., J. A. Markert, P. D. Danley & T. D. Kocher, 1999. Phylogeny of a rapidly evolving clade: the cichlid fishes of Lake Malawi, East Africa. Proceedings of the National Academy of Sciences USA 96: 5107–5110.
Allender, C. J., O. Seehausen, M. E. Knight, G. F. Turner & N. Maclean, 2003. Divergent selection during speciation of Lake Malawi cichlid fishes inferred from parallel radiations in nuptial coloration. Proceedings of the National Academy of Sciences USA 100: 14074–14079.
Anseeuw, D., G. E. Maes, P. Busselen, D. Knapen, J. Snoeks & E. Verheyen, 2008. Subtle population structure and male-biased dispersal in two Copadichromis species (Teleostei, Cichlidae) from Lake Malawi, East Africa. Hydrobiologia 615: 69–79.
Anseeuw, D., J. A. Raeymaekers, P. Busselen, E. Verheyen & J. Snoeks, 2011. Low genetic and morphometric intraspecific divergence in peripheral Copadichromis populations (Perciformes: Cichlidae) in the Lake Malawi basin. International Journal of Evolutionary Biology 2011: 835–946.
Bromage, T. G., F. Schrenk & F. W. Zonneveld, 1995. Paleoanthropology of the Malawi Rift: an early hominid mandible from the Chiwondo Beds, northern Malawi. Journal of Human Evolution 28: 71–108.
Cohen, A. S., J. R. Stone, K. R. Beuning, L. E. Park, P. N. Reinthal, D. Dettman, C. A. Scholz, T. C. Johnson, J. W. King, M. R. Talbot, E. T. Brown & S. J. Ivory, 2007. Ecological consequences of early Late-Pleistocene megadroughts in tropical Africa. Proceedings of the National Academy of Sciences USA 104: 16422–16427.
Danley P. D., M. Husemann, B. Ding, L. M. Dipietro, E. J. Beverly & D. J. Peppe, 2012. The impact of the geologic history and paleoclimate on the diversification of East African cichlids. International Journal of Evolutionary Biology 2012: Article ID 574851.
Delalande, M. L., P. Bergonzini, A Filly Branchu & D. Williamson, 2008. Hydroclimatic and geothermal controls on the salinity of Mbaka lakes (SW Tanzania): limnological and paleolimnological implications. Journal of Hydrology 359: 274–286.
Delvaux, D, 1995. Age of Lake Malawi (Nyasa) and water level fluctuations. Musée Royal de l’Afrique Centrale Tervuren (Belgium). Département de Géologie et Minéralogie. Rapport Annuel: 1993–1994, 99–108.
Drummond, A. J., A. Rambaut, B. Shapiro & O. G. Pybus, 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution 22: 1185–1192.
Ebinger, C. J., A. L. Deino, R. E. Drake & A. L. Tesha, 1989. Chronology of volcanism and rift basin propagation: Rungwe Volcanic Province, East Africa. Journal of Geophysical Research 94: 785–803.
Ebinger, C. J., A. L. Deino, A. L. Tesha, T. Becker & U. Ring, 1993. Tectonic controls on rift basin morphology: evolution of the Northern Malawi (Nyasa) rift. Journal of Geophysical Research 98(821–836): 1993.
Fryer, G., 1959. The trophic interrelationships and ecology of some littoral communities of Lake Nyasa with especial reference to the fishes, and a discussion of the evolution of a group of rock-frequenting Cichlidae. Proceedings of the Zoological Society of London 132: 153–281.
Genner, M. J. & G. F. Turner, 2005. The mbuna cichlids of Lake Malawi: a model for rapid speciation and adaptive radiation. Fish and Fisheries 6: 1–34.
Genner, M. J. & G. F. Turner, 2012. Ancient hybridization and phenotypic novelty in Lake Malawi’s cichlid fish radiation. Molecular Biology and Evolution 29: 195–206.
Genner, M. J., O. Seehausen, D. H. Lunt, D. A. Joyce, P. W. Shaw, G. R. Carvalho & G. F. Turner, 2007a. Age of cichlids: new dates for ancient lake fish radiations. Molecular Biology and Evolution 24: 1269–1282.
Genner, M. J., P. Nichols, G. R. Carvalho, R. L. Robinson, P. W. Shaw, A. Smith & G. F. Turner, 2007b. Evolution of a cichlid fish in a Lake Malawi satellite lake. Proceedings of the Royal Society of London B 274: 2249–2257.
Genner, M. J., P. Nichols, G. R. Carvalho, R. L. Robinson, P. W. Shaw & G. F. Turner, 2007c. Reproductive isolation among deep-water cichlid fishes of Lake Malawi differing in monochromatic male breeding dress. Molecular Ecology 16: 651–662.
Genner, M. J., P. Nichols, G. R. Carvalho, R. L. Robinson, P. W. Shaw & G. F. Turner, 2008. Genetic homogeneity of an exploited Lake Malawi cichlid fish. Freshwater Biology 53: 1823–1831.
Genner, M. J., P. Nichols, G. R. Carvalho, R. L. Robinson, P. W. Shaw & G. F. Turner, 2009. Population structure on breeding grounds of Lake Malawi’s twilight zone cichlid fishes. Journal of Biogeography 37: 258–269.
Genner, M. J., M. E. Knight, M. P. Haesler & G. F. Turner, 2010. Establishment and expansion of Lake Malawi rock fish populations after a dramatic Late Pleistocene lake level rise. Molecular Ecology 19: 170–182.
Heled, J. & A. J. Drummond, 2010. Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution 27: 570–580.
Ho, S. Y. & B. Shapiro, 2011. Skyline-plot methods for estimating demographic history from nucleotide sequences. Molecular Ecology Resources 11: 423–434.
Ho, S. Y., R. Lanfear, L. Bromham, M. J. Phillips, J. Soubrier, A. G. Rodrigo & A. Cooper, 2011. Time-dependent rates of molecular evolution. Molecular Ecology 20: 3087–3101.
Joyce, D. A., D. H. Lunt, R. Bills, G. F. Turner, C. Katongo, N. Duftner, C. Sturmbauer & O. Seehausen, 2005. An extant cichlid fish radiation emerged in an extinct Pleistocene lake. Nature 435: 90–95.
Joyce, D. A., D. H. Lunt, M. J. Genner, G. F. Turner, R. Bills & O. Seehausen, 2011. Repeated colonization and hybridization characterize the Lake Malawi cichlid fish species flock. Current Biology 21: R108–R109.
Knight, M. E. & G. F. Turner, 2004. Laboratory mating trials indicate incipient speciation by sexual selection among populations of the cichlid fish Pseudotropheus zebra from Lake Malawi. Proceedings of the Royal Society of London B 271: 675–680.
Knight, M. E., G. F. Turner, C. Rico, M. J. H. Van Oppen & G. M. Hewett, 1998. Microsatellite paternity analysis on captive Lake Malawi cichlids supports reproductive isolation by direct mate choice. Molecular Ecology 7: 1605–1610.
Koblmüller, S., U. K. Schliewen, N. Duftner, K. M. Sefc, C. Katongo & C. Sturmbauer, 2008. Age and spread of the haplochromine cichlid fishes in Africa. Molecular Phylogenetics and Evolution 49: 153–169.
Koblmüller, S., W. Salzburger, B. Obermueller, E. Eigner, C. Sturmbauer & K. M. Sefc, 2011. Separated by sand, fused by dropping water: habitat barriers and fluctuating water levels steer the evolution of rock-dwelling cichlid populations in Lake Tanganyika. Molecular Ecology 20: 2272–2290.
Konings, A., 2007. Malawi Cichlids in their Natural Habitat, 4th ed. Cichlid Press, El Paso.
Kullmer, O., 2008. The fossil suidae from the Plio-Pleistocene Chiwondo Beds of northern Malawi, Africa. Journal of Vertebrate Paleontology 208: 208–216.
Li, H. & R. Durbin, 2011. Inference of human population history from individual whole-genome sequences. Nature 475: 493–496.
Loh, Y. H., E. Bezault, F. M. Muenzel, R. B. Roberts, R. Swofford, M. Barluenga, C. E. Kidd, A. E. Howe, F. Di Palma, K. Lindblad-Toh, J. Hey, O. Seehausen, W. Salzburger, T. D. Kocher & J. T. Streelman, 2013. Origins of shared genetic variation in African cichlids. Molecular Biology and Evolution 30: 906–917.
Lyons, R. P., C. A. Scholz, M. R. Buoniconti & M. R. Martin, 2011. Late Quaternary stratigraphic analysis of the Lake Malawi Rift, East Africa: an integration of drill-core and seismic-reflection data. Palaeogeography Palaeoclimatology and Palaeoecology 303: 20–37.
Meyer, M. & W. Foerster, 1984. Un nouveau Pseudotropheus du lac Malawi avec des remarques sur le complexe Pseudotropheus-Melanochromis (Pisces, Perciformes, Cichlidae). Revue française d'Aquariologie et Herpetologie 10: 107-112.
Mims, M. C., C. D. Hulsey, B. M. Fitzpatrick & J. T. Streelman, 2010. Geography disentangles introgression from ancestral polymorphism in Lake Malawi cichlids. Molecular Ecology 19: 940–951.
Murray, A. M., 2001. The fossil record and biogeography of the Cichlidae (Actinopterygii: Labroidei). Biological Journal of the Linnean Society 74: 517–532.
Nevado, B., S. Mautner, C. Sturmbauer & E. Verheyen, 2013. Water-level fluctuations and metapopulation dynamics as drivers of genetic diversity in populations of three Tanganyikan cichlid fish species. Molecular Ecology 22: 3933–3948.
Pereyra, R., M. I. Taylor, G. F. Turner & C. Rico, 2004. Variation in habitat preference and population structure among three species of the Lake Malawi cichlid genus Protomelas. Molecular Ecology 13: 2691–2697.
Posada, D. & K. A. Crandall, 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818.
Reinthal, P. N., A. S. Cohen & D. L. Dettman, 2011. Fish fossils as paleo-indicators of ichthyofauna composition and climatic change in Lake Malawi, Africa. Palaeogeography Palaeoclimatology and Palaeoecology 303: 126–132.
Ribbink, A. J., B. A. Marsh, A. C. Marsh, A. C. Ribbink & B. J. Sharp, 1983. A preliminary survey of the cichlid fishes of rocky habitats in Lake Malawi. South African Journal of Zoology 18: 149–310.
Ricklefs, R. E. & E. Bermingham, 2004. Application of Johnson et al.’s speciation threshold model to apparent colonization times of island biotas. Evolution 58: 1664–1673.
Sandrock, O., O. Kullmer, F. Schrenk, Y. M. Juwayeyi & T. G. Bromage, 2007. Fauna, taphonomy, and ecology of the Plio-Pleistocene Chiwondo Beds, northern Malawi. In Bobe, R., Z. Alemseged & A. K. Behrensmeyer (eds), Hominin Environments in the East African Pliocene: An Assessment of the Faunal Evidence. Springer, Dordrecht.
Scholz, C. A., T. C. Johnson, A. S. Cohen, J. W. King, J. A. Peck, J. T. Overpeck, M. R. Talbot, E. T. Brown, L. Kalindekafe, P. Y. O. Amoako, R. P. Lyons, T. M. Shanahan, I. S. Castañeda, C. W. Heil, S. L. Forman, L. R. McHargue, K. R. Beuning, J. Gomez & J. Pierson, 2007. East African megadroughts between 135 and 75 thousand years ago and bearing on early-modern human origins. Proceedings of the National Academy of Sciences of the USA 104: 16416–16421.
Schrenk, F., T. G. Bromage, A. Gorthner & O. Sandrock, 1995. Paleoecology of the Malawi Rift: vertebrate and invertebrate faunal contexts of the Chiwondo Beds, northern Malawi. Journal of Human Evolution 28: 59–70.
Seehausen, O., 2004. Hybridization and adaptive radiation. Trends in Ecology and Evolution 19: 198–207.
Seehausen, O., Y. Terai, I. S. Magalhaes, K. L. Carleton, H. D. J. Mrosso, R. Miyagi, I. Van der Sluijs, M. V. Schneider, M. Maan, H. Tachida, H. Imai & N. Okada, 2008. Speciation through sensory drive in cichlid fish. Nature 455: 620–627.
Shaw, P. W. G. F., M. R. Turner, R. L. Robinson Idid & G. R. Carvalho, 2000. Genetic population structure indicates sympatric speciation of Lake Malawi pelagic cichlids. Proceedings of the Royal Society of London B 267: 2273–2280.
Smith, P. F. & I. Kornfield, 2002. Phylogeography of Lake Malawi cichlids of the genus Pseudotropheus: significance of allopatric colour variation. Proceedings of the Royal Society of London B 269: 2495–2502.
Stauffer, J. R. Jr., N. J. Bowers, K. A. Kellogg & K. R. McKaye, 1997. A revision of the blue-black Pseudotropheus zebra (Teleostei: Cichlidae) complex from Lake Malawi, Africa, with a description of a new genus and ten new species. Proceedings of the Academy of Natural Sciences of Philadelphia 148: 189–230.
Stewart, K. M. & A. M. Murray, 2013. Earliest fish remains from the Lake Malawi Basin, Malawi, and biogeographical implications. Journal of Vertebrate Paleontology 33: 532–539.
Sturmbauer, C., S. Baric, W. Salzburger, L. Rüber & E. Verheyen, 2001. Lake level fluctuations synchronize genetic divergences of cichlid fishes in African lakes. Molecular Biology and Evolution 18: 144–154.
Tyers, A. M., D. Bavin, G. M. Cooke, C. Griggs & G. F. Turner, 2014. Peripheral isolate speciation of a Lake Malawi cichlid fish from shallow muddy habitats. Evolutionary Biology. doi:10.1007/s11692-014-9277-4.
Van Damme, D. & M. Pickford, 2003. The Late Cenozoic Thiaridae (Mollusca, Gastropoda) of the Albertine rift valley (Uganda-Zaire). Hydrobiologia 498: 1–83.
van Oppen, M. J., G. F. Turner, C. Rico, R. L. Robinson, J. C. Deutsch, M. J. Genner & G. M. Hewitt, 1998. Assortative mating among rock-dwelling cichlid fishes supports high estimates of species richness from Lake Malawi. Molecular Ecology 7: 991–1001.
Won, Y. J., Y. Wang, A. Sivasundar, J. Raincrow & J. Hey, 2006. Nuclear gene variation and molecular dating of the cichlid species flock of Lake Malawi. Molecular Biology and Evolution 23: 828–837.
Xia, X. & Z. Xie, 2001. DAMBE: data analysis in molecular biology and evolution. Journal of Heredity 92: 371–373.
Zidana, H., G. F. Turner, C. Van Oosterhout & B. Haenfling, 2009. Elevated mtDNA diversity in introduced populations of Cynotilapia afra (Günther 1894) in Lake Malawi National Park is evidence for multiple source populations and hybridization. Molecular Ecology 18: 4380–4389.
We thank the Department of Fisheries of the Government of Malawi for assistance with sampling. We are grateful to Georgia Donnan and Emily Creaser for generating the Diplotaxodon sequences used here.
Guest editors: S. Koblmüller, R. C. Albertson, M. J. Genner, K. M. Sefc & T. Takahashi / Advances in Cichlid Research: Behavior, Ecology and Evolutionary Biology
About this article
Cite this article
Genner, M.J., Turner, G.F. Timing of population expansions within the Lake Malawi haplochromine cichlid fish radiation. Hydrobiologia 748, 121–132 (2015). https://doi.org/10.1007/s10750-014-1884-7
- Bayesian skyline plots
- Mitochondrial DNA
- Cichlid fish evolution