PERSPECTIVES OPINION Here,we discuss the relationship bety sms. diversification and speciation of orgar The evolutionary significance of WGDs and speciation and argue that most of the ancient WGDs that survived did so because they occurred at specific times: for ancient genome duplications instance, during major ecological upheavals and periods of extinction. At these times, competition with diploids was reduced and Yves Van de Peer, Steven Maere and Axel Meyer new ecological niches became available Furthermore, when WGDs survive they can Abstract Many organisms are currently polyploid, or have a polyploid ancestry greatly enhance the diversification potential and now have secondarily'diploidizedgenomes This finding is surprising of a lineage through the preferential because retained whole-genome duplications(WGDs)are exceedingly rare, retention of regulatory genes suggesting that polyploidy is usually an evolutionary dead end. We argue that ancient genome doublings could probably have survived only under very Competitive advantage of polyploid In the short term, polyploidy may lead specific conditions, but that, whenever established, they might have had a to transgressive segregation and increased pronounced impact on species diversification, and led to an increase vigour. In this section we argue that these in biological complexity and the origin of evolutionary novelties properties might give newly established genitors and a wider phenotypic range, M species of flowering plants and most polyploidy events have occurred thereby increasing their chances of survival. ates have descended from ancestors near the tips of the evolutionary tree of life who doubled their genomes, either through rather than at deeper branches. Although Reducing the risk of extinction. Crow and from cytogenetic analyses, morphological ancient polyploidy events have survived. tions could reduce the risk of extinction autopolyploidy or allopolyploidy. Evidence any species are currently polyploid, few agner have argued that genome dupli studies of fossil and extant species and, more During 500-600 million years of vertebrate through several by functional redun recently, whole-genome and EST analyses evolution, no more than two(or three for dancy, mutational robustness, and increased uggests that most(60-70%)flowering teleosts)WGDs have persisted. Since the rates of evolution and adaptation. Based on plants have a polyploid ancestry >-. In flow- rise of the flowering plants 150-200 million the work of Donoghue and Purnell, these ring plants, polyploids form at a frequency years ago(mya)3. the number of inferred authors observed that genome duplication of I per 100,000 individuals, and% of ancient WGDs in any angiosperm lineage events in vertebrate history seem to have speciation events involve polyploidization@. is at most four. 6. In the fungal lineage, for been preceded by multiple extinct lineages, As a result, many plants, and most of our genome sequences are sulting in pre-duplication gaps in the domesticated crop species, are polyploid known, there is only evidence for a single phylogeny of extant taxa. By analysing the Although polyploidy is much rarer in ancient WGD event". Paleopolyploidy numbers of families in extinct and extant animals than in plants, there are hundreds events therefore seem to be exceed- vertebrate lineages, they concluded that of known insects and vertebrate species ingly rare, and polyploids, or rather their extinction rates were considerably higher that are polyploid, mainly amphibians and descendants, have not been established for pre-duplication lineages than for fish. Whole-genome duplications(WGDs) tens or hundreds of times. However, all post-duplication lineages. ave also been documented for unicellular vertebrates seem to have shared two ancient The most compelling evidence that organisms: the first ancient WGD to be dis- WGD events, whereas all teleosts, and prob- genome duplications might aid in avoid covered in eukaryotes was that of the yeast ably also eudicots, are derived from ing extinction probably comes from Saccharomyces cerevisiae. More recently, lineage that experienced a WGD event 8-. flowering plants. Fawcett et al. showed it was shown that the unicellular ciliate This would suggest that, although descend- that various plants -including legumes, Paramecium tetraurelia has also undergone ants of WGD events do not survive often, cereals, Solanaceae(such as tomatoes and several wgDss when they do survive their evolutionary potatoes), lettuce and cotton -independ Because ancient WGDs in plants and neage can be very successful. ently underwent a WGD-60-70 mya animals gave rise to some particularly The observation that these WGDs pecies-rich groups, some have argued often gave rise to species-rich groups of me to the K-T boundary (BOX 1], suggest end but that it provides novelopportul.ad hat polyploidy is not an evolutionary de organisms,such as >25,000 species of fish ing that polyploid plants coped better with nd >350,000 species of flowering plants, the markedly changed environment than ties for evolutionary successb-.However, suggests that polyploidy can facilitate their diploid progenitors. Although many NATURE REVIEWS GENETICS VOLUME 10 lOCTOBER 20091725 22009 Macmillan Publishers Limited All rights reservedMost species of flowering plants and ver￾tebrates have descended from ancestors who doubled their genomes, either through autopolyploidy or allopolyploidy. Evidence from cytogenetic analyses, morphological studies of fossil and extant species and, more recently, whole-genome and EST analyses suggests that most (60–70%) flowering plants have a polyploid ancestry1,2–4. In flow￾ering plants, polyploids form at a frequency of 1 per 100,000 individuals5 , and ∼2–4% of speciation events involve polyploidization6 . As a result, many plants, and most of our domesticated crop species, are polyploid7 . Although polyploidy is much rarer in animals than in plants, there are hundreds of known insects and vertebrate species that are polyploid, mainly amphibians and fish6 . Whole-genome duplications (WGDs) have also been documented for unicellular organisms: the first ancient WGD to be dis￾covered in eukaryotes was that of the yeast Saccharomyces cerevisiae8 . More recently, it was shown that the unicellular ciliate Paramecium tetraurelia has also undergone several WGDs9 . Because ancient WGDs in plants and animals gave rise to some particularly species-rich groups, some have argued that polyploidy is not an evolutionary dead end but that it provides novel opportuni￾ties for evolutionary success10–13. However, most polyploidy events have occurred near the tips of the evolutionary tree of life rather than at deeper branches. Although many species are currently polyploid, few ancient polyploidy events have survived. During 500–600 million years of vertebrate evolution, no more than two (or three for teleosts) WGDs have persisted. Since the rise of the flowering plants 150–200 million years ago (mya)13,14, the number of inferred ancient WGDs in any angiosperm lineage is at most four15,16. In the fungal lineage, for which many more genome sequences are known, there is only evidence for a single ancient WGD event17. Paleopolyploidy events therefore seem to be exceed￾ingly rare, and polyploids, or rather their descendants, have not been established tens or hundreds of times. However, all vertebrates seem to have shared two ancient WGD events, whereas all teleosts, and prob￾ably also eudicots, are derived from a lineage that experienced a WGD event15,18–21. This would suggest that, although descend￾ants of WGD events do not survive often, when they do survive their evolutionary lineage can be very successful. The observation that these WGDs often gave rise to species-rich groups of organisms, such as >25,000 species of fish and >350,000 species of flowering plants, suggests that polyploidy can facilitate diversification and speciation of organisms. Here, we discuss the relationship between WGDs and speciation and argue that most of the ancient WGDs that survived did so because they occurred at specific times: for instance, during major ecological upheavals and periods of extinction. At these times, competition with diploids was reduced and new ecological niches became available. Furthermore, when WGDs survive they can greatly enhance the diversification potential of a lineage through the preferential retention of regulatory genes. Competitive advantage of polyploids In the short term, polyploidy may lead to transgressive segregation and increased vigour. In this section we argue that these properties might give newly established polyploids an edge over their diploid pro￾genitors and a wider phenotypic range, thereby increasing their chances of survival. Reducing the risk of extinction. Crow and Wagner22 have argued that genome duplica￾tions could reduce the risk of extinction through several means: by functional redun￾dancy, mutational robustness, and increased rates of evolution and adaptation. Based on the work of Donoghue and Purnell23, these authors observed that genome duplication events in vertebrate history seem to have been preceded by multiple extinct lineages, resulting in pre-duplication gaps in the phylogeny of extant taxa. By analysing the numbers of families in extinct and extant vertebrate lineages, they concluded that extinction rates were considerably higher for pre-duplication lineages than for post-duplication lineages. The most compelling evidence that genome duplications might aid in avoid￾ing extinction probably comes from flowering plants. Fawcett et al.24 showed that various plants — including legumes, cereals, Solanaceae (such as tomatoes and potatoes), lettuce and cotton — independ￾ently underwent a WGD ~60–70 mya. This wave of WGDs occurred close in time to the K–T boundary (BOX 1), suggest￾ing that polyploid plants coped better with the markedly changed environment than their diploid progenitors. Although many OpiniOn The evolutionary significance of ancient genome duplications Yves Van de Peer, Steven Maere and Axel Meyer Abstract | Many organisms are currently polyploid, or have a polyploid ancestry and now have secondarily ‘diploidized’ genomes. This finding is surprising because retained whole-genome duplications (WGDs) are exceedingly rare, suggesting that polyploidy is usually an evolutionary dead end. We argue that ancient genome doublings could probably have survived only under very specific conditions, but that, whenever established, they might have had a pronounced impact on species diversification, and led to an increase in biological complexity and the origin of evolutionary novelties. PersPecTives nATurE rEvIEWS | Genetics voluME 10 | oCToBEr 2009 | 725 © 2009 Macmillan Publishers Limited. All rights reserved