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The evolutionary significance of ancient genome duplications

Nature Reviews Genetics volume 10, pages 725–732 (2009)Cite this article

Abstract

Many organisms are currently polyploid, or have a polyploid ancestry and now have secondarily 'diploidized' genomes. This finding is surprising because retained whole-genome duplications (WGDs) are exceedingly rare, suggesting that polyploidy is usually an evolutionary dead end. We argue that ancient genome doublings could probably have survived only under very specific conditions, but that, whenever established, they might have had a pronounced impact on species diversification, and led to an increase in biological complexity and the origin of evolutionary novelties.

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Figure 1: Survival of the fittest.
Figure 2: Reciprocal gene loss or subfunctionalization facilitates speciation.

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Acknowledgements

Y.V.d.P. acknowledges support from the IUAP P6/25 (BioMaGNet). A.M. thanks the Deutsche Forschungsgemeinschaft, University of Konstanz and the Institute for Advanced Study Berlin for support. S.M. is a fellow of the Fund for Scientific Research — Flanders (FWO). We thank two anonymous reviewers for valuable comments and suggestions and apologize to those whose work could not be cited because of space limitations.

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Authors and Affiliations

  1. Yves Van de Peer and Steven Maere are at the Department of Plant Systems Biology, Department of Plant Biotechnology and Genetics, VIB (Flanders Institute of Biotechnology), B-9052 Ghent, Belgium, and the Bioinformatics and Evolutionary Genomics research group, Ghent University, B-9052 Ghent, Belgium.,

    Yves Van de Peer & Steven Maere

  2. Axel Meyer is at the Department of Biology, University of Konstanz, D-78457 Konstanz, Germany, and the Institute for Advanced Study, Wallotstraβe 19, D-14193 Berlin, Germany.,

    Axel Meyer

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

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Glossary

Accession

A sample of a plant variety collected at a specific location and time. This term is used to describe the Arabidopsis thaliana laboratory lines collected initially from the wild.

Allopolyploidy

The generation of the polyploid state by the fusion of nuclei from different species. For example, two fertilized diploid oocytes can fuse such that the newly formed single egg has two complete sets of chromosomes.

Autopolyploidy

In contrast to allopolyploidy, different sets of chromosomes are derived from the same species. This can occur in the fertilized oocyte if the nucleus divides but the cell does not.

Bateson–Dobzhansky–Muller model

Describes incompatibilities between organisms on the basis of the synergistic interaction of genes that have functionally diverged among the respective parents. Such incompatibilities can lead to speciation.

Carpel

A leaf-like structure that encloses the ovules and seeds and is the defining characteristic of flowering plants. In some species, multiple carpels might be present in a compound structure called an ovary.

Dosage balance effects

The components of macromolecular complexes must be balanced to avoid dominant fitness defects. Therefore, both under- and overexpression of individual protein subunits within a complex — for example, through duplication — tend to lower fitness.

Haploinsufficient

Describes the situation in which a lower than normal amount of a wild-type gene product confers a detectable phenotype.

Heterosis

The greater fitness of a hybrid individual carrying different alleles of genes relative to either of the two corresponding homozygous parents. Also called hybrid vigour. A more precise definition is non-additive inheritance, in which a trait in the first filial generation transgresses both parental values.

K–T boundary

The K–T event — which occurred ∼65 million years ago at the end of the Cretaceous period and the beginning of the Tertiary — is the most recent large-scale mass extinction of animal and plant species. There is general consensus that the K–T extinction was caused by one or more catastrophic events, such as a massive asteroid impact and increased volcanic activity.

Mutational robustness

Describes the extent to which the phenotype of an organism remains constant in spite of mutations. If an organism has an extra copy of a gene through gene or genome duplication, the effect of the loss of one copy might be limited.

Neural crest

A migratory cell population that gives rise to numerous differentiated cell types in vertebrates.

Orthologues

Loci in two species that are derived from a common ancestral locus by a speciation event.

Paralogues

Genes in the same organism that have evolved from a gene duplication, usually with a subsequent, sometimes subtle, divergence of function.

Phenotype space

A multi-dimensional continuum of all possible phenotypes.

Pleiotropic gene

A gene that is responsible for several distinct and seemingly unrelated phenotypic effects.

Transgressive segregation

Refers to the formation of extreme phenotypes that are observed in segregating hybrid populations when compared with parental lines.

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Van de Peer, Y., Maere, S. & Meyer, A. The evolutionary significance of ancient genome duplications. Nat Rev Genet 10, 725–732 (2009). https://doi.org/10.1038/nrg2600

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