A metabolic perspective on polyploid invasion and the emergence of life histories: Insights from a mechanistic model

Author:

Milosavljevic Silvija12ORCID,Kauai Felipe12ORCID,Mortier Frederik12ORCID,Van de Peer Yves134ORCID,Bonte Dries2ORCID

Affiliation:

1. Department of Plant Biotechnology and Bioinformatics Ghent University VIB ‐ UGent Center for Plant Systems Biology, B‐9052 Ghent Belgium

2. Department of Biology Terrestrial Ecology Unit, Ghent University Karel Lodewijk Ledeganckstraat 35, BE‐9000 Ghent Belgium

3. Department of Biochemistry Genetics and Microbiology, University of Pretoria Pretoria South Africa

4. College of Horticulture Nanjing Agricultural University Nanjing China

Abstract

AbstractPremiseWhole‐genome duplication (WGD, polyploidization) has been identified as a driver of genetic and phenotypic novelty, having pervasive consequences for the evolution of lineages. While polyploids are widespread, especially among plants, the long‐term establishment of polyploids is exceedingly rare. Genome doubling commonly results in increased cell sizes and metabolic expenses, which may be sufficient to modulate polyploid establishment in environments where their diploid ancestors thrive.MethodsWe developed a mechanistic simulation model of photosynthetic individuals to test whether changes in size and metabolic efficiency allow autopolyploids to coexist with, or even invade, ancestral diploid populations. Central to the model is metabolic efficiency, which determines how energy obtained from size‐dependent photosynthetic production is allocated to basal metabolism as opposed to somatic and reproductive growth. We expected neopolyploids to establish successfully if they have equal or higher metabolic efficiency as diploids or to adapt their life history to offset metabolic inefficiency.ResultsPolyploid invasion was observed across a wide range of metabolic efficiency differences between polyploids and diploids. Polyploids became established in diploid populations even when they had a lower metabolic efficiency, which was facilitated by recurrent formation. Competition for nutrients is a major driver of population dynamics in this model. Perenniality did not qualitatively affect the relative metabolic efficiency from which tetraploids tended to establish.ConclusionsFeedback between size‐dependent metabolism and energy allocation generated size and age differences between plants with different ploidies. We demonstrated that even small changes in metabolic efficiency are sufficient for the establishment of polyploids.

Publisher

Wiley

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