PERSPECTIVES possibly coincides with the origin and In fish, the correlation between WGD Late Cretaceous and Tertiary periods, mo divergence of the core Poaceae, a large clade and species diversification rates is less clear. than 150 million years later. This observa containing-10,000 species. Early-branching Fish constitute half of all vertebrate species tion could be taken to indicate that genome subclades of the Poaceae, as well as closely and are a highly successful and diverse evo- duplication was not an important factor in related non-Poaceae families, contain only lutionary lineage. The fish-specific genome the rapid radiation of teleosts. However, both a small number of species. Whole-genome duplication(3R)in the teleost lineage is esti- RGL and subfunction partitioning can occur duplications have also been reported for mated to have occurred 226-350 myas rer tens of millions of years after a WGD the Brassicaceae(3, 700 species), Asteraceae The inferred phylogenetic timing of 3R and can continue to promote speciation over (23,000 species), the Fabaceae(19, 400 spe- seems to separate the species-poor, early- long periods of times. It is conceivable that cies)and the Solanaceae(>3,000 species), to branching lineages of ray-finned fish from 3R continued to increase the propensity for name but a few, and these WGDs also seem the species-rich teleost lineage, and therefore speciation until a suitable ecological occa- to correlate with species-rich plant families, seems to provide evidence that 3R might sion presented itself, such as the K-Tmass Ithough the precise phylogenetic placement be causally related to an increase in species extinction. As an example of such stored of these WGDs is unclear. Furthermore, and biological diversity. However, there is diversifying potential, X laevis still main the rate of diversification is also high in these a large period of time between 3R and the tains-32-47%of its genes in duplicate, families compared with other families in the main teleost radiations, which, according ome 40 million years after its most recent same orders to fossil evidence, did not occur until the polyploidization event, and its genome 姒“ Figure 1 Survival of the fittest. The figure illustrates one of many.2-s a new niche(the new peak is indicated by an arrow in c). None of the exi simplified fitness landscape models. The upper and lower panels show the ing species has the evolutionary potential to fill this niche, but a polyploid fitness landscape with tw ary phenotype axes, 1 and 2. These axes species(white dot in b and d) may be able to develop the necessary phe- do not represent single quantitative traits but rather a flattened version of notypic innovationse, f In another scenario, the fitness landscape changes phenotype space. The black dots It well-adapted organisms that drastically. for example, through a catastrophic event. Most organisms can- ccupy the peaks in phenotype space(red indicates the most well adapted, not adapt to the changed environment and perish (red crosses). Some blue the least well adapted), which correspond to niches in which that par- organisms (near the centre of the landscape) live in relatively unaltered ticular combination of phenotypic characters is advantageous. The full niches and can adapt enough to survive. Others may manage to survive ircles represent the phenotypes accessible to the organisms, whereas the initially through polyploidization (white dots), outcompeting their diploid dashed circles are a simplified representation of the phenot of parents because of, for example, heterotic effects. These polyploi their polyploid relatives. Blue regions of the phenotype space are not via- harbour the potential to develop innovations that in time may enable them ble, so there is little room for successful genome duplication events. to colonize empty niches in phenotype space that cannot be reached by a-d In one scenario, there is an unoccupied peak in the fitness landscape other organisms. Differential realization of this potential among the polyploid offspring may lead to phenotype diversifi 22009 Macmillan Publishers Limited All rights reservedNature Reviews | Genetics 0 0.5 0.1 1.5 Phenotype 1 Phenotype 1 Phenotype 2 Phenotype 1 Phenotype 2 Phenotype 1 Phenotype 2 Phenotype 2 0 0.5 0.1 1.5 c Phenotype 1 Phenotype 2 d 0 0.5 0.1 1.5 e Phenotype 1 Phenotype 2 f Fitness Fitness Fitness a b possibly coincides with the origin and divergence of the core Poaceae, a large clade containing ~10,000 species. Early-branching subclades of the Poaceae, as well as closely related non-Poaceae families, contain only a small number of species. Whole-genome duplications have also been reported for the Brassicaceae (3,700 species), Asteraceae (23,000 species), the Fabaceae (19,400 spe￾cies) and the Solanaceae (>3,000 species), to name but a few, and these WGDs also seem to correlate with species-rich plant families, although the precise phylogenetic placement of these WGDs is unclear13. Furthermore, the rate of diversification is also high in these families compared with other families in the same orders54. In fish, the correlation between WGD and species diversification rates is less clear. Fish constitute half of all vertebrate species and are a highly successful and diverse evo￾lutionary lineage21. The fish-specific genome duplication (3r) in the teleost lineage is esti￾mated to have occurred 226–350 mya44,55–57. The inferred phylogenetic timing of 3r seems to separate the species-poor, early￾branching lineages of ray-finned fish from the species-rich teleost lineage, and therefore seems to provide evidence that 3r might be causally related to an increase in species and biological diversity. However, there is a large period of time between 3r and the main teleost radiations, which, according to fossil evidence, did not occur until the late Cretaceous and Tertiary periods, more than 150 million years later. This observa￾tion could be taken to indicate that genome duplication was not an important factor in the rapid radiation of teleosts. However, both rGl and subfunction partitioning can occur over tens of millions of years after a WGD and can continue to promote speciation over long periods of time47,48. It is conceivable that 3r continued to increase the propensity for speciation until a suitable ecological occa￾sion presented itself, such as the K–T mass extinction. As an example of such stored diversifying potential, X. laevis still main￾tains ~32–47%58 of its genes in duplicate, some 40 million years after its most recent polyploidization event, and its genome Figure 1 | survival of the fittest. The figure illustrates one of many92,95,112–115 simplified fitness landscape models. The upper and lower panels show the fitness landscape with two imaginary phenotype axes, 1 and 2. These axes do not represent single quantitative traits but rather a flattened version of phenotype space. The black dots represent well-adapted organisms that occupy the peaks in phenotype space (red indicates the most well adapted, blue the least well adapted), which correspond to niches in which that par￾ticular combination of phenotypic characters is advantageous. The full circles represent the phenotypes accessible to the organisms, whereas the dashed circles are a simplified representation of the phenotype space of their polyploid relatives. Blue regions of the phenotype space are not via￾ble, so there is little room for successful genome duplication events. a–d | in one scenario, there is an unoccupied peak in the fitness landscape (a,b) or a new fitness peak emerges (c,d), for instance, through evolution of a new niche (the new peak is indicated by an arrow in c). None of the exist￾ing species has the evolutionary potential to fill this niche, but a polyploid species (white dot in b and d) may be able to develop the necessary phe￾notypic innovations. e,f | in another scenario, the fitness landscape changes drastically, for example, through a catastrophic event. Most organisms can￾not adapt to the changed environment and perish (red crosses). some organisms (near the centre of the landscape) live in relatively unaltered niches and can adapt enough to survive. Others may manage to survive initially through polyploidization (white dots), outcompeting their diploid parents because of, for example, heterotic effects. These polyploids also harbour the potential to develop innovations that in time may enable them to colonize empty niches in phenotype space that cannot be reached by other organisms. Differential realization of this potential among the polyploid offspring may lead to phenotype diversification and speciation. Pers P ectives 728 | oCToBEr 2009 | voluME 10 www.nature.com/reviews/genetics © 2009 Macmillan Publishers Limited. All rights reserved