Phylogenetic evidence for cladogenetic polyploidization in land plants

Zhan, Shing Hei; Drori, Michal; Goldberg, Emma E.; Otto, Sarah P.; Mayrose, Itay

doi:10.3732/ajb.1600108

Cited by 36 publications

(24 citation statements)

References 46 publications

(62 reference statements)

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“…Unassigned species in our analyses were those with assignment probability lower than 0.9. Finally, we note that some authors refer to PIP-inferred polyploids as neopolyploids (77,78). However, we refer to these lineages as polyploid given that the subtrees do not follow taxonomic limits (i.e., generic-level analyses as used in other studies).…”

Section: Methodsmentioning

confidence: 99%

Polyploidy increases overall diversity despite higher turnover than diploids in the Brassicaceae

Román‐Palacios

Molina-Henao

Barker

2019

Preprint

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Although polyploidy, or whole-genome duplication, is widespread across the Plant Tree of Life, its long-term evolutionary significance is still poorly understood. Here we examine the effects of polyploidy in driving macroevolutionary patterns within the angiosperm family Brassicaceae, a speciose clade exhibiting extensive inter-specific variation in chromosome numbers. We inferred ploidal levels from haploid chromosome numbers for 80% of species in the most comprehensive species-level chronogram for the Brassicaceae published to date. After evaluating a total of 54 phylogenetic models of diversification, we found that ploidy drives diversification rates across the Brassicaceae, with polyploids experiencing faster rates of speciation and extinction, but relatively slower rates of diversification. Nevertheless, diversification rates are, on average, positive for both polyploids and diploids. We also found that despite diversifying significantly slower than diploids, polyploids have played a significant role in driving present-day differences in species richness among clades. Overall, although most polyploids go extinct before sustainable populations are established, rare successful polyploids persist and significantly contribute to the long-term evolution of lineages. Our findings suggest that polyploidy has played a major role in shaping the long-term evolution of the Brassicaceae and highlight the importance of polyploidy in shaping present-day diversity patterns across the plant Tree of Life. Significance statementAlthough polyploidy is a source of innovation, its long-term evolutionary significance is still debated. Here we analyze the evolutionary role of polyploidy within the Brassicaceae, a diverse clade exhibiting extensive variation in chromosome numbers among species. We found that, although polyploids diversify slower than diploids, polyploids have faster extinction and speciation rates. Our results also suggest that polyploidy has played an important role in shaping present-day differences in species richness within the Brassicaceae, with potential implications in explaining diversity patterns across the plant Tree of Life.\body IntroductionAlthough polyploidy-the heritable condition of carrying more than two complete sets of chromosomes-is widespread across the plant phylogeny (1), its evolutionary significance is still debated (2-6). Discussions on the evolutionary role of polyploidy date back to Stebbins (7,8) and Wagner (9) who considered polyploidy to have negligible effects on the long-term evolution of plants. This idea, later known as the 'dead-end' hypothesis, was recently reframed as an expectation that polyploid species will undergo extinction more frequently than diploids (4, 5, 10-12). However, polyploidy can influence the long-term evolution of lineages (1,(13)(14)(15)(16)(17) regardless of whether polyploids are more likely to go extinct than diploids (4,5, 10-12). Both interpretations of the 'dead-end' hypothesis are thus not equivalent to each other. The original hypothesis focused on t...

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Section: Methodsmentioning

confidence: 99%

Polyploidy increases overall diversity despite higher turnover than diploids in the Brassicaceae

Román‐Palacios

Molina-Henao

Barker

2019

Preprint

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“…Mayrose et al , 2011; Soltis et al , 2016; reviewed in Vamosi et al , 2018). In particular, polyploid formation as a mode of speciation motivated the development of cladogenetic state-dependent diversification models, in which the rate of speciation coincident with state change is parameterized (Mayrose et al , 2011; Zhan et al , 2016; see also Goldberg & Igić, 2012). These have since been used to show that neopolyploids tend to be evolutionary 'dead ends' (Mayrose et al , 2011; Arrigo & Barker, 2012) due to effects such as gene imbalance of the sex chromosomes during the meiosis (Orr, 1990), increased abortion in heteroploid hybrids (Ramsey & Schemske, 2002), and inefficiency of selection for multi-copy genes in polyploids (Wright, 1969).…”

Section: Introductionmentioning

confidence: 99%

Polyploidy and elevation contribute to opposing latitudinal gradients in diversification and species richness in lady ferns (Athyriaceae)

Wei

Ree

Sundue

et al. 2018

Preprint

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In ferns, the temperate-tropical sister clades Athyrium and Diplazium present an opportunity to study a latitudinal contrast in diversification dynamics. We generated a taxonomically expanded molecular chronogram and used macroevolutionary models to analyze how diversification rates have changed through time, across lineages, and in concert with changes in elevation and ploidy. We tested a novel model of cladogenetic state-change in which polyploidy can arise as an infraspecific polymorphism, with diversification parameters distinct from those of pure diploids and polyploids. Both Athyrium and Diplazium accelerated their diversification near the Oligocene-Miocene transition. In Diplazium, the rate shift is older, with subsequent net diversification somewhat slower and suggestive of diversity-dependence. In Athyrium, diversification is faster and associated with higher elevations. In both clades, polyploids have the highest rate of net accumulation but lowest (negative) net diversification, while the converse is true for polymorphic species; diploids have low rates of both net accumulation and diversification. Diversification in Athyrium may have responded to ecological opportunities in expanding temperate habitats during the Neogene, especially in mountains, while the pattern in Diplazium suggests saturation in the tropics. Neopolyploids are generated rapidly, primarily through accelerated cladogenesis in polymorphic species, but are evolutionary dead ends.

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“…In addition to providing a source of novel and potentially adaptive traits, gene and genome duplications can also serve as mechanisms of speciation (Winge, 1917;Lynch and Force, 2000). Whole-genome duplications, in particular, frequently coincide with speciation events in flowering plants (Otto and Whitton, 2000;Wood et al, 2009;Zhan et al, 2016). An association between WGD and subsequent increases in net diversification rate is also emerging (Otto and Whitton, 2000;Soltis et al, 2009;Tank et al, 2015; but see Kellogg, 2016), implicating WGD as a potentially important driver of species diversification in angiosperms.…”

Section: Introductionmentioning

confidence: 99%

Phylogenomics reveals an extensive history of genome duplication in diatoms (Bacillariophyta)

Parks¹,

Nakov

Ruck

et al. 2017

Preprint

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Premise of the study: Diatoms are one of the most species-rich lineages of microbial eukaryotes.Similarities in clade age, species richness, and contributions to primary production motivate comparisons to flowering plants, whose genomes have been inordinately shaped by whole genome duplication (WGD).These events that have been linked to speciation and increased rates of lineage diversification, identifying WGDs as a principal driver of angiosperm evolution. We synthesized a relatively large but scattered body of evidence that, taken together, suggests that polyploidy may be common in diatoms.Methods: We used data from gene counts, gene trees, and patterns of synonymous divergence to carry out the first large-scale phylogenomic analysis of genome-scale duplication histories for a phylogenetically diverse set of 37 diatom taxa.Key results: Several methods identified WGD events of varying age across diatoms, though determining the exact number and placement of events and, more broadly, inferences of WGD at all, were greatly impacted by gene-tree uncertainty. Gene-tree reconciliations supported allopolyploidy as the predominant mode of polyploid formation, with particularly strong evidence for ancient allopolyploid events in the thalassiosiroid and pennate diatom clades. Conclusions:Whole genome duplication appears to have been an important driver of genome evolution in diatoms. Denser taxon sampling will better pinpoint the timing of WGDs and likely reveal many more of them. We outline potential challenges in reconstructing paleopolyploid events in diatoms that, together with these results, offer a framework for understanding the evolutionary roles of genome duplication in a group that likely harbors substantial genomic diversity.

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Phylogenetic evidence for cladogenetic polyploidization in land plants

Abstract: Overall, these phylogenetic analyses provide the first broad confirmation that polyploidization is temporally associated with speciation events, suggesting that it is indeed a major speciation mechanism in plants, at least in some genera.

Cited by 36 publications

References 46 publications

Polyploidy increases overall diversity despite higher turnover than diploids in the Brassicaceae

Polyploidy increases overall diversity despite higher turnover than diploids in the Brassicaceae

Polyploidy and elevation contribute to opposing latitudinal gradients in diversification and species richness in lady ferns (Athyriaceae)

Phylogenomics reveals an extensive history of genome duplication in diatoms (Bacillariophyta)

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