Chromosome number is key to longevity of polyploid lineages

• Published in: The New phytologist Vol. 231; no. 1; pp. 19 - 28
• Main Authors: Bowers, John E., Paterson, Andrew H.
• Format: Journal Article
• Language: English
• Published: England Wiley 01.07.2021; Wiley Subscription Services, Inc
• Subjects: Alleles; Angiospermae; angiosperms; Bateson–Dobzhansky–Muller incompatibility; Chromosome number; Chromosomes; diploidisation; extinction; Fitness; Gene duplication; Gene flow; Genes; Genomes; Hybrids; karyotype evolution; longevity; Polyploidy; Recombination; Reproductive fitness; Speciation; Species; Species extinction; Subpopulations; Survival; Viewpoints; chromosome number; karyotype evolution; polyploidy; angiosperms; diploidisation; Bateson-Dobzhansky-Muller incompatibility
• ISSN: 0028-646X; 1469-8137; 1469-8137
• DOI: 10.1111/nph.17361

Polyploidy is ubiquitous and often recursive in plant lineages, most frequently resulting in extinction but occasionally associated with great evolutionary success. However, instead of chromosome numbers exponentially increasing due to recurrent polyploidy, most angiosperm species have fewer than 14 chromosome pairs. Following genome duplication, diploidisation can render one copy of essential genes nonfunctional without fitness cost. In isolated subpopulations, alternate (homoeologous) gene copies can be lost, creating incompatibilities that reduce fitness of hybrids between subpopulations, constraining exchange of favourable genetic changes and reducing species fitness. When multiple sets of incompatible genes are genetically linked, their deleterious effects are not independent. The effective number of independently acting sets of incompatible loci in hybrids is limited by chromosome number and recombination. Therefore, species with many chromosomes are subject to a higher fitness penalty during diploidisation. Karyotypic changes, especially fusions, that reduce gene flow are normally fitness disadvantages, but during the diploidisation process, can increase fitness by reducing mixing of differentially diploidised alleles. Fitness penalties caused by diploidisation favour accelerated karyotypic change, with each change increasing barriers to gene flow, contributing to speciation. Lower chromosome numbers and increased chromosome fusions confer advantages to surviving the diploidisation process following polyploid formation, by independent mechanisms.