Polyploidy, or whole-genome duplication (WGD), is usually an evolutionary dead end. Although polyploidy is a frequent and recurrent phenomenon, the number of WGDs that have become established in the long term is low.
The occurrence of WGDs in the tree of life is not random and seems to correlate with periods of environmental upheaval.
WGDs increase the adaptive potential of cells and organisms exposed to stressful conditions.
The biased retention of genes following WGDs offers a unique evolutionary potential to evolve key innovations and to increase biological complexity in the long term.
In cancer, WGD is a transient state that promotes aneuploidy, and is responsible for increased genetic variation and subsequent adaptive potential.
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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Y.V.d.P. and K.M. acknowledge the Multidisciplinary Research Partnership “Bioinformatics: from nucleotides to networks” Project (no. 01MR0310W) of Ghent University, Belgium. Y.V.d.P. acknowledges funding from the European Union Seventh Framework Programme (FP7/2007-2013) under European Research Council Advanced Grant Agreement 322739 –DOUBLEUP. K.M. acknowledges support from the Fonds voor Wetenschappelijk Onderzoek – Flanders (FWO15/PRJ/396). Special thanks go to R. Lohaus for helpful discussions and to P. Novikova for providing Figure 3. Y.V.d.P., E.M. and K.M. also thank the University of Pretoria, South Africa, for general support. The authors apologize to the many researchers whose work was overlooked or could not be included owing to space constraints. Finally, the authors thank the four anonymous reviewers for their comments and suggestions, which greatly helped to improve this Review.
The authors declare no competing financial interests.
The condition in which cells or organisms possess more than two complete sets of chromosomes.
The evolutionary process by which biological populations evolve to become distinct species.
- Recurrent polyploidy
Polyploidy that has occurred multiple times in the same population or evolutionary lineage.
- Neutral processes
Mechanisms that do not immediately lead to specific adaptation.
- Adaptive processes
Evolutionary changes that occur as a consequence of natural selection and that are adaptive to a certain environment. Such changes increase survivorship or reproduction by addressing a specific challenge or opportunity presented by the environment.
- Minority cytotype exclusion
A setting in which one cytotype (for example, diploid) is dominant over the other (for example, tetraploid), such that the less common cytotype has difficulty finding suitable partners to mate with.
- Assortative mating
A mating pattern in which individuals with common traits prefer to mate with one another; for example, polyploids mating with other polyploids, rather than with diploids.
The process by which a gene acquires a novel gene function after a duplication event.
- Niche separation
The process by which competing species use the environment differently in a way that helps them to coexist.
- Sympatric speciation
The process through which new species evolve while inhabiting the same geographical region.
- Prezygotic barriers
Mechanisms that prevent fertilization from occurring.
Duplicated genes (paralogues) that originate from a whole-genome duplication event.
Polyploidies that have occurred at least several million years ago. Most paleopolyploids have lost their polyploid status through a process called diploidization (the evolutionary process by which a polyploid genome turns into a diploid one) and are currently considered as functional diploids.
- Ecological tolerance
The range of conditions — or niche breadth — in which an organism can thrive. More tolerant organisms can withstand a broader range of environmental conditions.
- Key innovations
Important adaptations that lead to subsequent species radiation or that are of major importance for the success of a taxonomic group.
- Dosage balance
The state in which the stoichiometry between all interacting partners (that is, proteins) is maintained.
In evolutionary biology, a spandrel is a by-product of the evolution of some other characteristic or trait, rather than a direct product of adaptive selection. At later stages of evolution, such a by-product can become (that is, can evolve into) an important adaptation.
A term that describes a cell or organism that has an abnormal number of chromosomes. For instance, in humans, trisomy 21 (an extra copy of chromosome 21) is a form of aneuploidy.
The phenomenon by which potentially thousands of chromosomal rearrangements occur in a single event in localized and confined regions of the genome.
- Standing variation
The presence of two or more alleles at a locus in a population that have not yet been fixed in the population.
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Van de Peer, Y., Mizrachi, E. & Marchal, K. The evolutionary significance of polyploidy. Nat Rev Genet 18, 411–424 (2017). https://doi.org/10.1038/nrg.2017.26
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