Are polyploids really evolutionary dead‐ends (again)? A critical reappraisal of Mayroseet al. (2011)

Citations Over TimeTop 1% of 2014 papers

Abstract

Throughout the past century, hybridization and polyploidization have variously been viewed as drivers of biodiversity (e.g. Arnold, 1997) or evolutionary noise, unimportant to the main processes of evolution (e.g. Stebbins, 1950; Wagner, 1970). Wagner (1970) argued that while polyploids have always existed, they have never diversified or played a major role in the evolution of plants, and that the study of polyploidy (as well as inbreeding, apomixis, and hybridization) has led researchers to be 'carried away with side branches and blind alleys that go nowhere'. However, the use of molecular tools revolutionized the study of polyploidy, revealing that a given polyploid species often forms multiple times (reviewed in Soltis & Soltis, 1993, 1999, 2000). The realization that recurrent polyploidization from genetically differentiated parents is the rule that shattered the earlier perceptions of polyploids as genetically depauperate (Stebbins, 1950; Wagner, 1970). Because of multiple origins, polyploid species can maintain high levels of segregating genetic variation through the incorporation of genetic diversity from multiple populations of their diploid progenitors (e.g. Soltis & Soltis, 1993, 1999, 2000; Tate et al., 2005). Numerous studies have also shown that polyploid genomes are highly dynamic, with enormous potential for generating novel genetic variation (e.g. Gaeta et al., 2007; Doyle et al., 2008; Leitch & Leitch, 2008; Flagel & Wendel, 2009; Hawkins et al., 2009; Chester et al., 2012; Hao et al., 2013; Roulin et al., 2013). Furthermore, genomic studies have also revealed numerous ancient polyploidy events across the angiosperms (e.g. Vision et al., 2000; Bowers et al., 2003; Blanc & Wolfe, 2004; Paterson et al., 2004; Schlueter et al., 2004; Van de Peer & Meyer, 2005; Cannon et al., 2006; Cui et al., 2006; Tuskan et al., 2006; Jaillon et al., 2007; Barker et al., 2008, 2009; Lyons et al., 2008; Ming et al., 2008; Shi et al., 2010; Van de Peer, 2011; Jiao et al., 2012; McKain et al., 2012; Tayale & Parisod, 2013; reviewed in Soltis et al., 2009); all angiosperms have undergone at least one round of polyploidy (e.g. Jiao et al., 2011; Amborella Genome Consortium, 2013). Polyploidy is now viewed not as a mere side branch of evolution, but as a major mechanism of evolution and diversification. Based on analyses of ferns and angiosperms, Mayrose et al. (2011) and Arrigo & Barker (2012) revived the concept of polyploids as 'blind alleys'. Arrigo & Barker (2012, p. 140) refer to 'rarely successful polyploids' and state that 'despite leaving a substantial legacy in plant genomes, only rare polyploids survive over the long term and most are evolutionary dead-ends'. Mayrose et al. (2011) also refer to polyploids as 'dead-ends'. However, these authors use 'evolutionary dead-end' in a sense that differs from the traditional view of Stebbins (1950) and Wagner (1970). Whereas Stebbins (1950) and Wagner (1970) were concerned that polyploids did not contribute significantly to evolution, Arrigo & Barker (2012) argue that the analyses of Mayrose et al. (2011) indicate that polyploids are more likely to go extinct than are diploids and in this sense are typically 'dead-ends'. We agree that most new polyploids likely go extinct early, probably at the population level before they are even detected; this has long been espoused (e.g. Levin, 1975; Ramsey & Schemske, 1998; reviewed in Rieseberg & Willis, 2007; Soltis et al., 2010). Ramsey & Schemske (1998) estimated that the rate of autotetraploid formation is high – comparable to the genic mutation rate – but most do not survive. However, these very early, extinction-prone stages of polyploids are much younger than the timeframe considered by Mayrose et al. (2011) and Arrigo & Barker (2012), who concluded that established polyploid species are more likely to go extinct than diploid congeners. We revisit the analyses and conclusions of Mayrose et al. (2011) and Arrigo & Barker (2012) and ask: Is there convincing evidence to support the hypothesis that extinction rates in established polyploids are higher than those of diploids? Perhaps this is true, but we do not feel that these authors have made a compelling case. While we have focused our review and examples on angiosperms, most of our criticisms are equally applicable to the fern dataset included in their studies. We emphasize philosophical, statistical, and analytical arguments against the study of Mayrose et al. (2011), as well as problems with sampling and their data-mining methods. We support our views by drawing on numerous examples from the recent and classic literature on polyploid complexes (most not included in Mayrose et al., 2011). We stress that our goals are to correct errors and stimulate discussion, not attack the authors of Mayrose et al. (2011) and Arrigo & Barker (2012). Increased diversification rates are more likely to arise in large clades than in small ones, simply because there are more opportunities for increased speciation or retarded extinction rates. Thus, large, old clades will, on average, yield more clades with increased diversification rates than young, small ones, and this probabilistic statement has relevance for patterns of diversification in polyploids relative to their diploid relatives (including their parents). By definition, a polyploid species is younger than its parents. The parental species are part of a clade that is more numerous and older than the single polyploid derivative – thus, through chance, greater diversification could occur at the diploid than the polyploid level. This relationship between clade age, clade size, and diversification – and its particular relevance to diploid–polyploid comparisons – was not considered by Mayrose et al. (2011). Because a polyploid can never be the same age as its parents, analyses within genera with both diploids and polyploids are biased in favor of greater diversification at the diploid level. A more appropriate comparison would be between related diploid and polyploid clades of the same age. Although evolutionary history is represented using bifurcating phylogenetic trees, it is well known that complex sequences of evolutionary events are poorly represented with a branching tree structure (Doolittle, 1999; Huson & Bryant, 2006). Hybridization, hybrid speciation, and allopolyploidy are not described well by bifurcating trees (e.g. Wagner, 1983; Linder & Rieseberg, 2004; McBreen & Lockhart, 2006; Brysting et al., 2007; Soltis & Soltis, 2009; Huson & Scornavacca, 2010). Thus, the evolutionary history of many plant groups is not tree-like, but a network with numerous reticulation events (e.g. Guggisberg et al., 2009; Marcussen et al., 2012; Pellicer et al., 2012; Abbott et al., 2013; Garcia et al., 2014). To reconstruct and visualize complex reticulate evolutionary scenarios, various methods may be employed, including splits graphs, other networks, and analysis of incongruence among gene trees (McBreen & Lockhart, 2006). Comparison of numerous nuclear gene trees is perhaps the best approach to tease apart the complexity of reticulation events (e.g. Linder & Rieseberg, 2004), but to date few studies have used this approach. Mayrose et al. (2011), however, relied entirely on phylogenetic and diversification analyses that have as an underlying assumption that evolution is strictly bifurcating. While we agree that diversification methods have not been developed for nonbifurcating evolutionary histories, we urge caution in interpreting results derived from analyses that violate many of the underlying assumptions of the algorithms used. How polyploids affect phylogeny reconstruction is poorly understood – even at the level of how the topology may be influenced (Soltis et al., 2008; Lott et al., 2009; Marcussen et al., 2012). How those effects cascade onto the accuracy of branch length estimation is unexplored. Finally, how these effects on topology and branch lengths influence diversification analyses is also untested. Again, improved methods and understanding of these nonbifurcating evolutionary influences will help address the question. However, we conclude that current methods are poorly suited when it comes to the complex evolution of polyploids. The conclusions of Mayrose et al. (2011) hinge upon accurate estimation of speciation and extinction rates from molecular phylogenies. Here, we focus on the problems with estimating speciation and extinction rates, as well as the statistical interpretation of the results. Estimating extinction rates from molecular phylogenies based solely upon extant taxa in the absence of a fossil record, as in Mayrose et al. (2011), is problematic (Rabosky, 2009, 2010; Quental & Marshall, 2010). Rabosky (2010) showed that when diversification rates vary among lineages, 'simple estimators based on the birth–death process are unable to recover true extinction rates' (p. 1816). Because variation in diversification rate is 'ubiquitous,' Rabosky (2010) cautioned that extinction rates should not be estimated in the absence of fossils. Similarly, Quental & Marshall (2010) stress that 'a wide range of processes can give similarly shaped molecular phylogenies'. Mayrose et al. (2011) found relatively little difference in speciation rates between diploids and polyploids; their conclusion that polyploids diversify at a lower rate is based on higher inferred extinction rates in polyploids – if that rate is unreliably estimated, as others have cautioned, their conclusions cannot be supported. Speciation and diversification rates were estimated with BiSSE (Maddison et al., 2007; FitzJohn et al., 2009). However, Davis et al. (2013) examined the power of the BiSSE method and showed that phylogenies with fewer than 300 taxa should be treated with extreme caution. However, only three datasets in Mayrose et al. (2011) have over 100 terminals. Additionally, Davis et al. (2013) caution against using datasets where the frequency of one of the two states is under 10% – 11 of the 63 genera studied have frequencies outside this range (nine with polyploidy frequencies under 10% and two with polyploidy frequencies over 90%, another is reported as 10% polyploid species). Mayrose et al. (2011) cannot be criticized based on conclusions reached in 2013. However, even when BiSSE was published (Maddison et al., 2007), the authors stressed that large phylogenetic trees would be needed, suggesting c. 500 terminals. 'It remains to be studied how the probability of rejecting a false null hypothesis (power) varies with number of species and with the degree of difference in rates. From our initial exploration, however, we suspect that large phylogenetic trees will generally be needed to have sufficient power' (p. 708). They also note (p. 706), 'This shows at least some power to reject the null hypothesis with trees of 500 species when there is a twofold difference in speciation rates'. Mayrose et al. (2011) show the results of the significance tests for each study but do not draw the reader's attention to the meaning of the information. The last three columns of supplementary material Table S2 from Mayrose et al. (2011) show the percent of the MCMC chains where the difference in diversification, speciation, and extinction estimates of diploids minus polyploids is positive (higher in diploids than polyploids). The test of significance is whether zero (no difference in rates) is outside of the 95% credible interval – or outside of the range seen in 95% of the MCMC steps. Thus, under equal rates, the percent is expected to be 50%, while if 95% of the MCMC steps show higher parameter estimates in diploids than polyploids, this would be a significant result (similarly, if only 5% show higher rates, this would be a significant result in favor of polyploids having higher rates). For diversification rate, only six of 63 genera support significantly higher diversification in diploids, and three of the 63 support significantly lower diversification in diploids relative to polyploids – hardly results that support a conclusion of dramatic differences in diversification rates. For speciation, none of the differences support significantly higher speciation in diploids, while 13 of 63 support higher speciation rates in polyploids – in fact, when examined within each MCMC step (as these data do), speciation is higher in polyploids on average, with only an average of 22% of the MCMC steps showing higher speciation in diploids than polyploids vs 50% for equal rates. While the estimated average speciation rates are higher in diploids (columns 1 and 2 of Table S2 in the supplementary material of Mayrose et al. (2011)), when association with MCMC steps is accounted for, the trend is the opposite. For the extinction results, we assume that the table is mislabeled (while the file has been corrected once since publication, the latest version was updated September 1, 2011, and remains labeled %(μD > μP), that is, that extinction in diploids is higher than polyploids), and the authors intended the label to be '%(μD six of are et al., 2012) and from million yr diploid and two of the recurrent polyploidization with within the last million yr has in two and one et al., 2012). speciation within polyploid clades has been a major to diversification in et al., 2012). Many angiosperm genera numerous polyploids but phylogenetic data. classic polyploid complexes simply because they are Thus, the examples analyzed by Mayrose et al. based on Wood et al., are not representative of angiosperm and their conclusions (and Arrigo & 2012) are to some of the most problematic polyploid complexes (Table in favor of clades for which of cladogenesis are appropriate and results may be examples of genera (Stebbins, are and comprises over cytotypes in this single recognized species, with ranging from to c. reviewed in comprises perhaps species, half of which are polyploid et al., Furthermore, genetic data and the of the based on high chromosome number (Stebbins, that and are ancient polyploids (Soltis & Soltis, Tuskan et al., 2006). Other examples of groups in part to & & and several other genera of et al., as well as multiple genera of examples are by hybridization and apomixis, but to be into the polyploid if we are to whether polyploids have higher extinction rates than diploids. can argue that we are polyploid complexes to Mayrose et al. (2011) and Arrigo & Barker (2012) and that these complexes are also not representative of However, our point is – many complex of the angiosperm tree of are highly to more of those complexes are included in studies, of diploid vs polyploid and extinction are Throughout their Mayrose et al. (2011) to the methods that they However, as we show later, in they some of the published trees, conclusions regarding the impact of We review the methods used by Mayrose et al. (2011), of The of the dataset is based on Wood et al. which data for were from the phylogenetic or when not from other as the to and the there were the data reported in the phylogenetic study were in the but in the supplementary data for species with multiple chromosome the was generating a bias against polyploids within In many known chromosome were with between the dataset of Mayrose et al. (2011) and the were For example, for Mayrose et al. (2011) only two and However, the for several species, including three with polyploid of In and are all in the study as both and et al., 2004), but all were considered only in Mayrose et al. (2011). occur for and This of chromosome biased results having fewer polyploid in the trees, a tree that is more diploid than For each Mayrose et al. (2011) molecular data and the published For studies with multiple only those taxa included in the analysis were In some this led to clades of polyploids that only been for some While Mayrose et al. (2011) were how the datasets were and some taxa were the effects of their are not in of how many studies were or in how the may have biased the results. In some the dataset by Mayrose et al. (2011) in to be an use of 35 to of taxa from the studies of the published dataset (Table 1). The of taxa can have a major in taxa were from the species used in et al. – because they were not all for all – with major (see and Brysting et al., in and of taxa were removed et al., in of species were et al., 2006). Table 1 examples where Mayrose et al. (2011) excluded species from their analyses – of the studies there is of how this may have the results, or whether the was biased in of In some the dataset by Mayrose et al. (2011) in the of polyploid the trees than they really c. species, is an in which several polyploids were excluded et al., (Fig. Mayrose et al. (2011) only used those taxa that were included in the et al. However, six polyploid species were included in et al. these polyploids would have increased the sampled polyploids from three of species to of (Fig. We the analyses of Mayrose et al. (2011) using a and dataset from et al. but including all taxa for which data were With most of the polyploids Mayrose et al. (2011) that diversification is higher in diploid in of the MCMC with the this is only the in of the steps. speciation is estimated to be higher in polyploids in both was estimated to be higher in polyploids in of the MCMC steps by Mayrose et al. (2011), but in the only of the MCMC steps show this (Fig. This is consistent with et al. who found that the large polyploid clade in shows high diversification in a of time six million et al. that this polyploid diversification is with into a new and the evolution of novel The of taxa from as well as by Mayrose et al. (2011) also has a major comprises c. 100 species, all of which are a few species have the number of has C. has many species have The species and form a clade with best represented as a The of genetic variation and among the species a recent and et al., However, Mayrose et al. (2011) the chromosome for C. as when they to Thus, was considered the number in and taxa with were as in a percentage of polyploids in the genus of (Fig. However, C. is in et al. as is the known of was as in Mayrose et al. (2011). is with including the for C. the percentage of polyploidy in is c. (Fig. BiSSE is with the corrected of diversification higher in diploids in of the MCMC steps as reported by Mayrose et al. (2011), it is only higher in of the MCMC steps, an given the of that the of BiSSE for these The results for are a of the of significance in the results reported by Mayrose et al. (2011). of the steps indicating higher diversification in diploids a conclusion in favor of the Mayrose et al. (2011) that diversification is higher in

Related Papers

• → EFFECT OF THE NEMATODE PHASMARHABDITIS HERMAPHRODITA ON YOUNGSTAGES OF THE PEST SLUG ARION LUSITANICUS(2002)40 cited
• → Cloning and Characterization of Rat BAT3 cDNA(1999)20 cited
• → Anthoxanthum Mosaic Virus(1970)6 cited
• → HLA-B-associated transcript 3 (Bat3)/Scythe is essential for p300-mediated acetylation of p53(2007)127 cited
• → ИСПОЛЬЗОВAНИЕ ПОТЕНЦИAЛA СОЦИAЛЬНЫХ ПAРТНЕРОВ В ПОДГОТОВКЕ БУДУЩИХ ПЕДAГОГОВ(2024)