The evolutionary conundrum of whole‐genome duplication

Abstract

Whole‐genome duplication (WGD) is a dramatic, common event in plants. Because of the detrimental effects arising from doubling the entire chromosome set, such as minority cytotype exclusion, genomic instability, mitotic and meiotic abnormalities, alterations in cell architecture, or epigenetic changes (Comai, 2005), purifying selection is expected to quickly remove polyploids from the population. Nevertheless, polyploidy is common, and many diploids bear traces of a polyploid ancestry (Soltis et al., 2015; Van de Peer et al., 2017). Some of these ancestral polyploidy events can be traced back to the origin of large and diverse taxonomic lineages; also, most crops are neopolyploids, suggesting an important role for WGDs in promoting phenotypic diversity, speciation, and domestication.

Interestingly, the long‐term fixation of polyploidy does not seem to occur randomly. One notable example is the biased distribution of WGD events across independent plant lineages at the Cretaceous–Paleogene or K‐Pg boundary, about 66 million years ago (Ma). Many lineages seem to have undergone a WGD around the time of the K‐Pg extinction event, while their nonpolyploid ancestors died out, suggesting that polyploidy might confer an adaptive advantage under stressful environments and periods of environmental turmoil (Van de Peer et al., 2017). There might be other examples of “waves” of WGDs during periods of environmental change. For instance, the timing of WGD events in the Malpighiales may correlate with periods of global climatic change during the Paleocene–Eocene, ca. 56–54 mya (Cai et al., 2019). However, the evolutionary mechanisms underlying the relationship between WGD and evolutionary success remain elusive, despite vivid discussions on the topic, as witnessed by a recent special series of review papers and several other essays in the “On the Nature of Things” section of this very same journal. Here, we try to reconcile and discuss some recent findings about the putative adaptive role of WGD during evolution under scenarios of global ecological challenge.