PERSPECTIVES (Hox)clusters and other Hox genes03773 fact that genome duplications provide the enough species roam the fitness landscape, transforming growth factor-P pathway raw material for increased complexity does for some species further changes are likely to genes', insulin receptors", nuclear recep- not imply that they should always lead to become adaptive or previous changes may be tors and genes that specify the neural crest. more complex organisms. For instance, -opted for a novel purpose there is no indication that morphological Donoghue and Purnellargued against Increase in complexity. It is unclear whether complexity increased substantially after the a link between genome duplications and or not polyploidy caused the evolution of the WGD in S cerevisiae and, despite undergo- increasing complexity based on the observa fining innovations in angiosperm and ver- ing three genome duplications, P tetraurelia tion that when extinct lineages are taken into tebrate lineages(BOX 1). Rather than facilitat- is still a unicellular(although well evolved) account, there are no bursts in morphologi ing innovation from scratch, the power of organism. Accordingly, the over-retention cal innovation or jumps in complexity in genome duplications may be their ability to of regulatory duplicates after the WGDs in post-WGD clades. However, morphological perfect primitive versions or precursors of these organisms is less pronounced evolution after wgd does not need to be innovative features and fully exploit their In this respect, the duplicated genome, saltational. Genome duplication merely potential, for example, by lifting constraints although maybe not immediately useful, enhances the diversification potential of a on pleiotropic genes and facilitating their could be regarded as a genomic'spandrels lineage; the ensuing process of morpholog co-option for specialized purposes" 2. It is that occasionally might have been used for cal elaboration is likely to take time and to onceivable that an increase in regulatory adaptive or complexity-increasing ember- spawn intermediate forms that might g gene complexity fuelled by WGD would lishments. An increased rate of speciation extinct because they are later outcompeted tend to increase the potential of an organism after polyploidy could have facilitated this by more derived relatives*s. As with species to become more complex, providing a 'drive process by providing a lineage with more diversity, a better indicator of the diversify towards more complex organisms". But the opportunities to sample phenotype space. If ing force of WGDs is obtained by comparing orphological innovations in WGD clades with those of their non - WGD sister clades Glossary (or their closest living non-WGD relatives) Basal chordates(such as urochordates and cephalochordates)do not exhibit the A sample of a plant variety collected at a specific location inheritance, in which a trait in the first filial generation and time. This term is used to describe the Arabidopsis transgresses both parental values. morphological evolution of vertebrates; for thaliana laboratory lines collected initially from the wild example, amphioxus is considered a living K-T boundary fossils(for other examples, see REFS 4, 21) The K-T event-which occurred-65 million years ago at Concerning the more recent wave of The generation of the polyploid state by the fusion of the end of the Cretaceous period and the beginning of the nuclei from different species. For example, two fertilized Tertiary- is the most recent large-scale mass extinctio genome duplications around the K-T diploid oocytes can fuse such that the newty formed single of animal and plant species. There is general consensus boundary in plants, the phylogenetic place that the k-T extinction was caused by one or more ment of the WGD events is too uncertain to catastrophic events, such as a massive asteroid impact and allow the accurate identification of WGD and non -WGD Sister clades. so an assess- In contrast to allopolyp from the sam Mutational robustness ment of the correlation or causation between fertilized oocyte if the nucleus divides but the cell does not Describes the extent to which the phenotype of an ccurrence of these WGDs and morpho- gical innovations is difficult. However, the Bateson-Dobzhansky-Muller model an organism has an extra copy of a gene through gene or ct that these WGDs have occurred in many Describes incompatibilities between organisms on the basis genome duplication, the effect of the loss of one copy of the most rich and morphologi- diverged among the respective parents. Such cally diverse angiosperm families is prob incompatibilities can lead to speciation. Neural crest ably no coincidence.L337-. It is not known A migratory cell population that gives rise to numerous whether genome duplications are also Carpel differentiated cell types in vertebrates. involved in the diversification of other large A leaf-like structure that encloses the ovules and seeds and is the defining characteristic of flowering plants. In some families, such as the orchids, although species, multiple carpels might be present in a compound Loci in two species that are derived from a common morphological innovations in orchid flowers structure called an ovary. ancestral locus by a speciation event. have been linked to an expansion of DEF- like MADS-box genes that could have been Dosage balance effects The components of macromolecular complexes must be enes in the same organism that have evolved from a gen caused by genome duplication balanced to avoid dominant fitness defects. therefore duplication, usually with a subsequent, sometimes subte, both under-and overexpression of individual protein divergence of function. Conclusions and perspectives subunits within a complex- for example, through Arguably the greatest consequence of Phenotype space polyploidy is an increase in the attainable onal continuum of all possible phenotypes. Haploinsufficient morphospace. But the potential for phe scribes the situation in which a lower than normal notypic enhancement provided by WGDs amount of a wild-type gene product confers a detectable a gene that is responsible for several distinct and is less useful when there are no niches in phenotype seemingly unrelated phenotypic effects. which the newly available phenotypes are Heterosis efers to the formation of extreme phenotypes that are formed polyploids are probably not able to different alleles of genes relative to either of the tw observed in segregating hybrid populations when compete with the highly adapted occupants compared with parental lines. of existing niches, including their diploid 22009 Macmillan Publishers Limited All rights reserved(Hox) clusters and other Hox genes40,77,78, transforming growth factor-β pathway genes79, insulin receptors80, nuclear recep￾tors81 and genes that specify the neural crest40. Increase in complexity. It is unclear whether or not polyploidy caused the evolution of the defining innovations in angiosperm and ver￾tebrate lineages (BOX 1). rather than facilitat￾ing innovation from scratch, the power of genome duplications may be their ability to perfect primitive versions or precursors of innovative features and fully exploit their potential, for example, by lifting constraints on pleiotropic genes and facilitating their co-option for specialized purposes40,82. It is conceivable that an increase in regulatory gene complexity fuelled by WGD would tend to increase the potential of an organism to become more complex, providing a ‘drive’ towards more complex organisms72. But the fact that genome duplications provide the raw material for increased complexity does not imply that they should always lead to more complex organisms83. For instance, there is no indication that morphological complexity increased substantially after the WGD in S. cerevisiae and, despite undergo￾ing three genome duplications, P. tetraurelia is still a unicellular (although well evolved) organism. Accordingly, the over-retention of regulatory duplicates after the WGDs in these organisms is less pronounced9 . In this respect, the duplicated genome, although maybe not immediately useful, could be regarded as a genomic ‘spandrel’84 that occasionally might have been used for adaptive or complexity-increasing embel￾lishments. An increased rate of speciation after polyploidy could have facilitated this process by providing a lineage with more opportunities to sample phenotype space. If enough species roam the fitness landscape, for some species further changes are likely to become adaptive or previous changes may be co-opted for a novel purpose. Donoghue and Purnell23 argued against a link between genome duplications and increasing complexity based on the observa￾tion that when extinct lineages are taken into account, there are no bursts in morphologi￾cal innovation or jumps in complexity in post-WGD clades. However, morphological evolution after WGD does not need to be saltational. Genome duplication merely enhances the diversification potential of a lineage; the ensuing process of morphologi￾cal elaboration is likely to take time and to spawn intermediate forms that might go extinct because they are later outcompeted by more derived relatives43,85. As with species diversity, a better indicator of the diversify￾ing force of WGDs is obtained by comparing morphological innovations in WGD clades with those of their non-WGD sister clades (or their closest living non-WGD relatives). Basal chordates (such as urochordates and cephalochordates) do not exhibit the morphological evolution of vertebrates; for example, amphioxus is considered a living fossil86 (for other examples, see REFS 4,21). Concerning the more recent wave of genome duplications around the K–T boundary in plants, the phylogenetic place￾ment of the WGD events is too uncertain to allow the accurate identification of WGD and non-WGD sister clades13, so an assess￾ment of the correlation or causation between the occurrence of these WGDs and morpho￾logical innovations is difficult. However, the fact that these WGDs have occurred in many of the most species-rich and morphologi￾cally diverse angiosperm families is prob￾ably no coincidence2,4,13,87–89. It is not known whether genome duplications are also involved in the diversification of other large families, such as the orchids, although the morphological innovations in orchid flowers have been linked to an expansion of DEF￾like MADS-box genes that could have been caused by genome duplication90,91. Conclusions and perspectives Arguably the greatest consequence of polyploidy is an increase in the attainable ‘morphospace’. But the potential for phe￾notypic enhancement provided by WGDs is less useful when there are no niches in which the newly available phenotypes are advantageous. In stable ecosystems, newly formed polyploids are probably not able to compete with the highly adapted occupants of existing niches, including their diploid Glossary Accession A sample of a plant variety collected at a specific location and time. This term is used to describe the Arabidopsis thaliana laboratory lines collected initially from the wild. Allopolyploidy The generation of the polyploid state by the fusion of nuclei from different species. For example, two fertilized diploid oocytes can fuse such that the newly formed single egg has two complete sets of chromosomes. Autopolyploidy In contrast to allopolyploidy, different sets of chromosomes are derived from the same species. This can occur in the fertilized oocyte if the nucleus divides but the cell does not. Bateson–Dobzhansky–Muller model Describes incompatibilitiesbetween organismson the basis of the synergistic interaction of genes that havefunctionally diverged among the respective parents. Such incompatibilities can lead to speciation. Carpel A leaf-like structure that encloses the ovules and seeds and is the defining characteristic of flowering plants. In some species, multiple carpels might be present in a compound structure called an ovary. Dosage balance effects The components of macromolecular complexes must be balanced to avoid dominant fitness defects. Therefore, both under- and overexpression of individual protein subunits within a complex — for example, through duplication — tend to lower fitness. Haploinsufficient Describes the situation in which a lower than normal amount of a wild-type gene product confers a detectable phenotype. Heterosis The greater fitness of a hybrid individual carrying different alleles of genes relative to either of the two corresponding homozygous parents. Also called hybrid vigour. A more precise definition is non-additive inheritance, in which a trait in the first filial generation transgresses both parental values. K–T boundary The K–T event — which occurred ∼65 million years ago at the end of the Cretaceous period and the beginning of the Tertiary — is the most recent large-scale mass extinction of animal and plant species. There is general consensus that the K–T extinction was caused by one or more catastrophic events, such as a massive asteroid impact and increased volcanic activity. Mutational robustness Describes the extent to which the phenotype of an organism remains constant in spite of mutations. If an organism has an extra copy of a gene through gene or genome duplication, the effect of the loss of one copy might be limited. Neural crest A migratory cell population that gives rise to numerous differentiated cell types in vertebrates. Orthologues Loci in two species that are derived from a common ancestral locus by a speciation event. Paralogues Genes in the same organism that have evolved from a gene duplication, usually with a subsequent, sometimes subtle, divergence of function. Phenotype space A multi-dimensional continuum of all possible phenotypes. Pleiotropic gene A gene that is responsible for several distinct and seemingly unrelated phenotypic effects. Transgressive segregation Refers to the formation of extreme phenotypes that are observed in segregating hybrid populations when compared with parental lines. Pers P ectives 730 | oCToBEr 2009 | voluME 10 www.nature.com/reviews/genetics © 2009 Macmillan Publishers Limited. All rights reserved