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

dc.contributor.authorMilosavljevic, Silvija
dc.contributor.authorKauai, Felipe
dc.contributor.authorMortier, Frederik
dc.contributor.authorVan de Peer, Yves
dc.contributor.authorBonte, Dries
dc.date.accessioned2024-08-20T13:20:36Z
dc.date.issued2024-08
dc.descriptionDATA AVAILABILITY STATEMENT : All relevant data are within the manuscript and supporting material (Appendices S1 and S2). The code developed for the simulations is available on GitHub at https://github.com/silvijamilosavljevic/polyploidy-model-metabolic-perspective.en_US
dc.descriptionAPPENDIX S1. Individual-based model description following the ODD (overview, design concepts, details) protocol.en_US
dc.descriptionAPPENDIX S2. Supplementary results of the model analysis (Figures S1–S7).en_US
dc.description.abstractPREMISE : Whole-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. METHODS : We 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. RESULTS : Polyploid 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. CONCLUSIONS : Feedback 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.en_US
dc.description.departmentBiochemistryen_US
dc.description.departmentGeneticsen_US
dc.description.departmentMicrobiology and Plant Pathologyen_US
dc.description.embargo2025-08-07
dc.description.librarianhj2024en_US
dc.description.sdgSDG-15:Life on landen_US
dc.description.sponsorshipThe European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program and Ghent University (Methusalem funding).en_US
dc.description.urihttp://www.wileyonlinelibrary.com/journal/AJBen_US
dc.identifier.citationMilosavljevic, S., F. Kauai, F. Mortier, Y. Van de Peer, and D. Bonte. 2024. A metabolic perspective on polyploid invasion and the emergence of life histories: insights from a mechanistic model. American Journal of Botany 111: e16387. https://doi.org/10.1002/ajb2.16387.en_US
dc.identifier.issn0002-9122 (print)
dc.identifier.issn1537-2197 (online)
dc.identifier.other10.1002/ajb2.16387
dc.identifier.urihttp://hdl.handle.net/2263/97754
dc.language.isoenen_US
dc.publisherWileyen_US
dc.rights© 2024 Botanical Society of America. This is the pre-peer reviewed version of the following article : A metabolic perspective on polyploid invasion and the emergence of life histories: insights from a mechanistic model. American Journal of Botany 111: e16387. https://doi.org/10.1002/ajb2.16387, which has been published in final form at http://www.wileyonlinelibrary.com/journal/AJB.en_US
dc.subjectWhole-genome duplication (WGD)en_US
dc.subjectPolyploidizationen_US
dc.subjectMetabolismen_US
dc.subjectIndividual-based modelen_US
dc.subjectEnergy budgetsen_US
dc.subjectBody sizeen_US
dc.subjectSDG-15: Life on landen_US
dc.titleA metabolic perspective on polyploid invasion and the emergence of life histories : insights from a mechanistic modelen_US
dc.typePostprint Articleen_US

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