Pii: S0169-5347(97)01239-1

1 T explosive speciation of cichlid fishes in the African great lakes has intrigued biologists for many decades. Interest was revitalized in 1996 after the publication in Science of geological data1 indicating that the youngest lake, Lake Victoria, must have been completely dry during the most recent Ice Age – perhaps as recently as 12 400 years ago. This implies that the approximately 500 haplochromine cichlid species must have evolved within this extremely short timespan from a single ancestral species2. But even with lower estimates of species number and higher estimates of the age of the species flock, the haplochromine cichlids still present one of the most dramatic examples of speciation and diversification in vertebrates. An old hypothesis – concerning the importance of temporary geographical isolation of cichlid fishes in satellite lakes around Lake Victoria for speciation of cichlid fishes3 – is no longer much in favour4,5. Such satellite lakes only have very few species of cichlids and can therefore not explain the bulk of the speciation events in Lake Victoria. More specifically, this hypothesis cannot explain the large diversity of ‘rock’ species – since there are no rocky islands in these satellite lakes and each group of rock islands in Lake Victoria has its own species assemblage. Seehausen et al.6 have now put forward a persuasive hypothesis explaining the high frequency of speciation events that must have occurred. They show how sexual selection could be the driving force behind speciation in the haplochromine cichlids of Lake Victoria, because mate choice of females for differently coloured males maintains reproductive isolation between sympatric species and colour morphs. Females have a strong preference for males of a particular colour when light conditions are sufficiently good7. Males of sympatric, closely related species always differ in colour, one species having blue males, the other red or yellow males (females are usually inconspicuously coloured). This colour dichotomy of blue versus red/yellow also holds for conspecific male colour morphs that occur abundantly in the lake. The colours of the males coincide well with the visual sensitivity of cichlids. Cichlid eyes have three retinal cone pigments and the greatest sensitivity is either for blue or for red and yellow. In deeper water, red/yellow is better visible than blue. Small evolutionary changes can modify the maximum sensitivity of the eye from red/yellow to blue and vice versa (polymorphism in colour vision is known in guppies8). Changes in colouration of the males happen frequently, judging from the large number of blue and red/yellow sibling species. If females prefer conspicuous males, individual variation in sensitivity for colours (in females) and in pigmentation (males) will lead to such a frequent occurrence of colour dichotomy (see also Refs 9,10). Evidence for the importance of sexual selection for the maintenance of reproductive isolation comes from behavioural experiments in monochromatic light, which masks colour differences8. Under these light conditions, a breakdown of preferences for conspecific mates occurs. Sadly, important additional evidence comes from a recent loss of cichlid species in Lake Victoria. The increased turbidity of the water owing to human activities is causing a breakdown of reproductive barriers. Females can no longer distinguish males of sibling species from their own when visibility is poor and hybridize with males from other species6,7. Hybrids are fully fertile and therefore the species diversity of parts of Lake Victoria has seriously declined with increasing turbidity of the water. There is a great danger of further decline because of the continuing pollution. Seehausen et al.’s hypothesis can explain allopatric speciation where, after allopatric divergence, incipient species later overlap in distribution. But their hypothesis also allows for fully sympatric speciation, solely by mate choice of the females – as in the models of Lande11, Turner and Burrows12 and Payne and Krakauer13. Spatial heterogeneity plays a role in the sympatric speciation scenario as well, because depth differences are correlated with differences in colour perception, which is relevant for mate preferences; speciation can only take off when novel ‘compatible’ male and female types (i.e. red males with females that prefer red males) temporarily stay together. Allopatric speciation of cichlid species will certainly have played a role in Lake Victoria, because of its size and diversity of habitats. However, the abundance of sympatrically occurring colour morphs as well as the common absence of mating barriers other than behavioural ones suggests that sympatric speciation has played an important role. Seehausen et al.’s hypothesis6 nicely augments a much older hypothesis on the speciosity of cichlid fishes. This muchdiscussed hypothesis was first proposed in 1973 by Liem14, and bears on the importance of the versatile pharyngeal jaw apparatus in the evolution of cichlid fishes. A large number of speciation events and mating barriers produced by sexual selection is not enough to maintain species diversity. Species diversity is determined by the balance of the numbers of species that originate and go extinct. When, after speciation events, the new species are indistinguishable ecologically, species will be lost in a process akin to random drift15. However, the species will never be exactly similar ecologically, in which case the extinction process will be considerably more rapid, except when the differences lead to niche differentiation16,17. This niche differentiation has taken place in cichlids on a large scale, leading to a spectacular adaptive radiation. Adaptive radiation can only take place when species are splitting up repeatedly and mate recognition systems or other mechanisms are keeping the adaptively diverging populations apart18. Conversely, the many newly emerged species can only continue to coexist when adaptive radiation takes place. Thus, the origination of large numbers of species and a rapid adaptive radiation necessarily go together. The striking diversity of feeding niches that characterizes cichlids of Lake Victoria4,14,19 suggests that niche differentiation occurred by rapid specialization for different feeding niches. This implication is strengthened by the observation that sibling species are always characterized by small differences in feeding behaviour (Ref. 20, and N. Bouton, pers. commun.). Recent support for Liem’s19 hypothesis comes from a comparison of the pharyngeal jaw apparatus in cichlid fishes with that of the presumed generalized percoid ancestors21,22. This comparison supports a hypothesis of Vermeij23 that speciose taxa are characterized by more independent elements than taxa that are less speciose. A large number of independent elements increases the number of potential solutions for a particular biomechanical problem. Therefore, body plans with more independent elements can be more easily modified and diversified than those with fewer independent elements. During the evolution of the cichlid pharyngeal jaw apparatus, two decouplings have occurred21. These decouplings have increased the number of independent elements and, thus, the number of degrees of freedom of the cichlid pharyngeal jaw apparatus compared to that of generalized percoids. There are two reasons why the flexible and versatile pharyngeal jaw apparatus of