Abstract

Ancient whole-genome duplications (WGDs), also referred to as paleopolyploidizations, have been reported in most evolutionary lineages. Their attributed role remains a major topic of discussion, ranging from an evolutionary dead end to a road toward evolutionary success, with evidence supporting both fates. Previously, based on dating WGDs in a limited number of plant species, we found a clustering of angiosperm paleopolyploidizations around the Cretaceous–Paleogene (K–Pg) extinction event about 66 million years ago. Here we revisit this finding, which has proven controversial, by combining genome sequence information for many more plant lineages and using more sophisticated analyses. We include 38 full genome sequences and three transcriptome assemblies in a Bayesian evolutionary analysis framework that incorporates uncorrelated relaxed clock methods and fossil uncertainty. In accordance with earlier findings, we demonstrate a strongly nonrandom pattern of genome duplications over time with many WGDs clustering around the K–Pg boundary. We interpret these results in the context of recent studies on invasive polyploid plant species, and suggest that polyploid establishment is promoted during times of environmental stress. We argue that considering the evolutionary potential of polyploids in light of the environmental and ecological conditions present around the time of polyploidization could mitigate the stark contrast in the proposed evolutionary fates of polyploids.

Highlights

  • The omnipresence of whole-genome duplications (WGDs) in evolution is striking

  • We focused on dating the most recent WGD in each plant species, because these can be most identified based on collinearity information

  • The node joining the homeologous pair in each orthogroup phylogeny, representing the WGD of interest, was dated using the uncorrelated lognormal (UCLD) relaxed clock model implemented in the BEAST package (Drummond et al 2006, 2012) based on several primary fossil calibrations

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Summary

Introduction

The omnipresence of whole-genome duplications (WGDs) in evolution is striking Both angiosperm and vertebrate ancestors have undergone at least two separate WGDs, all of their descendants are ancient polyploids (paleopolyploids) (Putnam et al 2008; Jiao et al 2011). Formed polyploids are traditionally considered to be good colonizers that have a broad ecological tolerance, which gives them an adaptive advantage as an invasive species (Thompson and Lumaret 1992; Otto and Whitton 2000) The latter can be attributed to their phenotypic instability, which can be viewed as increased phenotypic variability and plasticity (te Beest et al 2012). Be treated with caution because of the paucity of large-scale systematic data on the subject and the many exceptions that can be found (Soltis et al 2010)

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