Wide variation in the rates of diversification among lineages is a feature of evolution that has fascinated biologists since Darwin1,2. With approximately 2,000 known species, hundreds of which coexist in individual African lakes, cichlid fish are amongst the most striking examples of adaptive radiation, the phenomenon whereby a single lineage diversifies into many ecologically varied species in a short span of time3 (Fig. 1). The largest radiations, which in Lakes Victoria, Malawi and Tanganyika, have generated between 250 (Tanganyika) and 500 (Malawi and Victoria) species per lake, took no more than 15,000 to 100,000 years for Victoria and less than 5 million years for Malawi3,4,5, but 10–12 million years for Lake Tanganyika6. The radiations in Lake Victoria and Malawi thus display the highest sustained rates of speciation known to date in vertebrates7. The evolution of these lineages and their genomes has presumably been shaped by cycles of population expansion, fragmentation and contraction as lineages colonized lakes, diversified, collapsed when lakes dried up, and re-colonized lakes, and by episodic adaptation to a multitude of ecological niches coupled with strong sexual selection. Genetic diversity within lake radiations has been influenced by admixture following multiple colonization events and periodic infusions through hybridization8,9.

Figure 1: The adaptive radiation of African cichlid fish. Top left, map of Africa showing lakes in which cichlid fish have radiated. Right, the five sequenced species: Pundamilia nyererei (endemic of Lake Victoria); Neolamprologus brichardi (endemic of Lake Tanganyika); Metriaclima zebra (endemic of Lake Malawi); Oreochromis niloticus (from rivers across northern Africa); Astatotilapia burtoni (from rivers connected to Lake Tanganyika). Major ecotypes are shown from each lake: a, pelagic zooplanktivore; b, rock-dwelling algae scraper; c, paedophage (absent from Lake Tanganyika); d, scale eater; e, snail crusher; f, reef-dwelling planktivore; g, lobe-lipped insect eater; h, pelagic piscivore; i, ancestral river-dweller also found in lakes (absent from Lake Tanganyika). Bottom left, phylogenetic tree illustrating relationships between the five sequenced species (red), major adaptive radiations and major river lineages. The tree is from ref. 4, pruned to the major lineages. Upper timescale (4), lower timescale (32). Photos by Ad Konings (Tanganyika a, b, d, e, g, h; Malawi a, c, d, e, f, g, h, i), O.S. (Victoria a–g, i; Malawi b), Frans Witte (Victoria h), W.S. (Tanganyika f), Oliver Selz (Victoria f, A. burtoni), Marcel Haesler (O. niloticus). PowerPoint slide Full size image

Cichlid phenotypic diversity encompasses variation in behaviour, body shape, coloration and ecological specialization. The frequent occurrence of convergent evolution of similar ecotypes (Fig. 1) suggests a primary role of natural selection in shaping cichlid phenotypic diversity10,11. In addition, the importance of sexual selection is demonstrated by a profusion of exaggerated sexually dimorphic traits like male nuptial colour and elaborate bower building by males3. Ecological and sexual selection converge in the cichlid visual system, where trichromatic colour vision, eight different opsin genes and novel spherical lenses promote sensitivity in the highly dimensional visual world of clear-water lakes12,13,14. Rapidly evolving sex determination systems, often linked to male and female colour patterns, may also speed cichlid diversification15,16. Ecological, social and behavioural variation correlates with striking diversity in brain structures17 that appears early in development18.

Exceptional phenotypic variation, even among closely related species, makes cichlids different from most other fish groups, including those that share the same habitats with them but have not diversified as much, as well as those that have radiated into much smaller species flocks in northern temperate lakes19. However, how cichlids evolve in this exceptionally highly dimensional phenotype space remains unexplained.

We sequenced the genomes of five representative cichlid species from throughout the East African haplo-tilapiine lineage (Extended Data Fig 1a), which gave rise to all East African cichlid radiations. These five lineages diverged primarily through geographical isolation, and three of them subsequently underwent adaptive radiations in the three largest lakes of Africa (Fig. 1). Here we describe the comparative analyses of the five genomes coupled with an analysis of the genetic basis of species divergence in the Lake Victoria species flock to examine the genomic substrate for rapid evolutionary diversification.