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The evolutionary significance of polyploidy

Nature Reviews Genetics volume 18, pages 411–424 (2017)Cite this article

Subjects

Key Points

  • 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.

Abstract

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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Figure 1: A phylogenetic tree showing known whole-genome duplications.
Figure 2: A schematic representation of the effects of whole-genome duplication and environmental stress on the evolution of gene number and fitness.
Figure 3: The distribution of diploid and tetraploid Neobatrachus species.
Figure 4: Polyploidy in different systems.

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Acknowledgements

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.

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Authors and Affiliations

  1. Department of Plant Biotechnology and Bioinformatics, Ghent University, Technologiepark 927

    Yves Van de Peer & Kathleen Marchal

  2. Center for Plant Systems Biology, VIB, Technologiepark 927

    Yves Van de Peer

  3. Bioinformatics Institute Ghent, Ghent University, Technologiepark 927, Ghent, B-9052, Belgium

    Yves Van de Peer & Kathleen Marchal

  4. Genomics Research Institute, University of Pretoria,

    Yves Van de Peer & Eshchar Mizrachi

  5. Department of Genetics, Forestry and Agricultural Biotechnology Institute, University of Pretoria, Private Bag X20, Pretoria, 0028, South Africa

    Eshchar Mizrachi & Kathleen Marchal

  6. Department of Information Technology, IDLab, imec, Ghent University, Ghent, B-9052, Belgium

    Kathleen Marchal

Authors
  1. Yves Van de Peer
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Correspondence to Yves Van de Peer.

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Glossary

Polyploidy

The condition in which cells or organisms possess more than two complete sets of chromosomes.

Speciation

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.

Neofunctionalization

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.

Ohnologues

Duplicated genes (paralogues) that originate from a whole-genome duplication event.

Paleopolyploidies

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.

Spandrel

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.

Aneuploid

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.

Chromothripsis

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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