Picking up the Ball at the K/Pg Boundary: The Distribution of Ancient Polyploidies in the Plant Phylogenetic Tree as a Spandrel of Asexuality with Occasional Sex

Freeling, Michael

doi:10.1105/tpc.16.00836

Cited by 34 publications

(29 citation statements)

References 31 publications

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“…Polyploidy, a spandrel of occasional sex Evidence is accumulating that polyploidy can increase mutational and environmental robustness, which might increase the potential for specific adaptation under changing environmental conditions or reduce the risk of extinction during periods of environmental upheaval. Recently, Freeling 155 proposed an interesting alternative hypothesis about how or why polyploids might be able to survive periods of mass extinction (Fig. 1, K/Pg boundary).…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, an asteroid impacting Earth would cause depletion of the Earth's protective ozone layer 156 , which in turn leads to a serious increase in surface UV-B irradiance causing mutation and breakage of DNA. If the polyploid could however shield its reproductive meristems and avoid meiosis altogether, and reproduce asexually for a while, it would increase its chances of survival 155 . During, or after its 'hiding out' under unfavourable conditions within the soma of plants that reproduce asexually, for instance by budding underground or under water, the polyploid can then undergo diploidization, which is necessary for again establishing accurate meiosis.…”

Section: Discussionmentioning

confidence: 99%

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The evolutionary significance of polyploidy

2017

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Polyploidy, or the duplication of entire genomes, has been observed in prokaryotic and eukaryotic organisms, and in somatic and germ cells. The consequences of polyploidization are complex and variable, and they differ greatly between systems (clonal or non-clonal) and species, but the process has often been considered to be an evolutionary 'dead end'. Here, we review the accumulating evidence that correlates polyploidization with environmental change or stress, and that has led to an increased recognition of its short-term adaptive potential. In addition, we discuss how, once polyploidy has been established, the unique retention profile of duplicated genes following whole-genome duplication might explain key longer-term evolutionary transitions and a general increase in biological complexity.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

The evolutionary significance of polyploidy

2017

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“…More refined placement and denser sampling of ancient WGDs in insects will provide a new opportunity to test Muller's classic hypothesis. Similarly, a recent study proposed that the phylogenetic distribution of ancient WGD among plants may be a byproduct of asexuality rather than an intrinsic advantage of polyploidy itself (58). Given the diversity of insect sexual systems, a better understanding of ancient WGDs in insects would provide an improved context for testing this hypothesis in other eukaryotes.…”

Section: Discussionmentioning

confidence: 99%

Multiple large-scale gene and genome duplications during the evolution of hexapods

Tiley

Galuska

et al. 2018

Proc. Natl. Acad. Sci. U.S.A.

171

161

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Polyploidy or whole genome duplication (WGD) is a major contributor to genome evolution and diversity. Although polyploidy is recognized as an important component of plant evolution, it is generally considered to play a relatively minor role in animal evolution. Ancient polyploidy is found in the ancestry of some animals, especially fishes, but there is little evidence for ancient WGDs in other metazoan lineages. Here we use recently published transcriptomes and genomes from more than 150 species across the insect phylogeny to investigate whether ancient WGDs occurred during the evolution of Hexapoda, the most diverse clade of animals. Using gene age distributions and phylogenomics, we found evidence for 18 ancient WGDs and six other large-scale bursts of gene duplication during insect evolution. These bursts of gene duplication occurred in the history of lineages such as the Lepidoptera, Trichoptera, and Odonata. To further corroborate the nature of these duplications, we evaluated the pattern of gene retention from putative WGDs observed in the gene age distributions. We found a relatively strong signal of convergent gene retention across many of the putative insect WGDs. Considering the phylogenetic breadth and depth of the insect phylogeny, this observation is consistent with polyploidy as we expect dosage balance to drive the parallel retention of genes. Together with recent research on plant evolution, our hexapod results suggest that genome duplications contributed to the evolution of two of the most diverse lineages of eukaryotes on Earth.

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“…Polyploid frequency‐based diversification can be achieved through recurrent origins (Soltis & Soltis, ), triploid bridges (Köhler et al ., ), asexual reproduction (Freeling, ), or perennial life forms (Stebbins, ). Recurrent origins of polyploidy are common in Allium , given the high rate of unreduced pollen grains (Levan, ).…”

Section: Discussionmentioning

confidence: 99%

“…Additionally, ecologically driven diversification events seem to be associated with key innovations of functional traits (Čertner et al ., ; Wei et al ., ). Accordingly, we also hypothesise that trait shifts, including shifts in mating system or growth form, could facilitate polyploid speciation (Freeling, ; Van Drunen & Husband, ).…”

Section: Introductionmentioning

confidence: 99%

Polyploidy promotes species diversification of Allium through ecological shifts

et al. 2019

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Summary Despite the role of polyploidy in multiple evolutionary processes, its impact on plant diversification remains controversial. An increased polyploid frequency may facilitate speciation through shifts in ecology, morphology or both. Here we used Allium to evaluate: (1) the relationship between intraspecific polyploid frequency and species diversification rate; and (2) whether this process is associated with habitat and/or trait shifts. Using eight plastid and nuclear ribosomal markers, we built a phylogeny of 448 Allium species, representing 46% of the total. We quantified intraspecific ploidy diversity, heterogeneity in diversification rates and their relationship along the phylogeny using trait‐dependent diversification models. Finally, we evaluated the association between polyploidisation and habitat or trait shifts. We detected high ploidy diversity in Allium and a polyploidy‐related diversification rate shift with a probability of 95% in East Asia. Allium lineages with high polyploid frequencies had higher species diversification rates than those of diploids or lineages with lower polyploid frequencies. Shifts in speciation rates were strongly correlated with habitat shifts linked to particular soil conditions; 81.7% of edaphic variation could be explained by polyploidisation. Our study emphasises the role of intraspecific polyploid frequency combined with ecological drivers on Allium diversification, which may explain plant radiations more generally.

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Picking up the Ball at the K/Pg Boundary: The Distribution of Ancient Polyploidies in the Plant Phylogenetic Tree as a Spandrel of Asexuality with Occasional Sex

Cited by 34 publications

References 31 publications

The evolutionary significance of polyploidy

The evolutionary significance of polyploidy

Multiple large-scale gene and genome duplications during the evolution of hexapods

Polyploidy promotes species diversification of Allium through ecological shifts

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