Abstract
Whole-genome duplication (WGD) is a leading force of plant sympatric speciation. However, the evolutionary mechanisms promoting the establishment of neopolyploid mutants in nature remain elusive. We studied polyploid establishment in a unique natural system of Mimulus guttatus (Phrymaceae) in Shetland where a recently (< 100 years ago) locally formed autotetraploid still coexists with its diploid progenitor. We cytotyped 679 adults and 766 seedlings and scored relevant reproductive traits in the field and performed controlled crossings to infer differences in plant performance and get a first insight into the crossing barriers between ploidies. Tetraploids grew in 25% of Shetland populations, mostly in mixtures with diploids, but triploids were absent both among seedlings and adults. Seeds of both cytotypes sampled in areas of immediate sympatry exhibited similar, high germination rates (98% on average). In contrast, low (2%) germination of progeny from controlled interploidy crosses demonstrated strong postzygotic isolation. Yet, plants simultaneously pollinated by diploid and tetraploid pollen donors set viable progeny with ploidy levels identical to the seed parent. The abundant presence of fertile tetraploids in the field despite strong postzygotic isolation demonstrates the ability of novel autopolyploids to cope with both intrinsic and extrinsic challenges associated with WGD and to successfully establish in nature.
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Acknowledgements
The authors thank Kevin Walker from Botanical Society of Britain and Ireland (Carney) for providing floristic data on Mimulus occurrence in Shetland, and L. Yant and V. Simón-Porcar for help with locating Shetland populations. The authors acknowledge the support of those people who assisted with the laboratory cultivations, M. Brindzák and V. Vlčková. Flow cytometry, growth chamber, and microscopy facilities were provided by the Department of Botany, Charles University in Prague, Czech Republic. This work was supported by the Czech Science Foundation (project 20-22783S to FK). Additional support was provided by the Czech Academy of Sciences (long-term research development project no. RVO 67985939) and a student grant of the Charles University Grant Agency (GAUK project no. 321222 to S.S.).
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SS, and FK designed the methodology with help of materials provided by MVM. SS, JC, and FK carried out the fieldwork. SS conducted the plant cultivation and germination experiments. SS. and JC. carried out data analysis. SS, JC, and FK. wrote the manuscript. SS, JC, and FK reviewed and edited subsequent versions of the manuscript, with contributions from MVM. FK conceived the ideas and supervised the study. All authors gave final approval for publication.
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Online Resource 1. a Population and locality details of 15 sampled populations. b Flow cytometry analysis of Mimulus guttatus. c Trait differences between diploid and tetraploid M. guttatus based on the analysis of all scored individuals from total sampled populations. d Natural progeny array in two mixed-ploidy populations: BIG and QUA. e Natural growth habitat of M. guttatus.
Online Resource 2. a Phenotypic traits of all the sampled individuals, scored in natural populations. b Corolla height of diploids and tetraploids in controlled conditions. c Natural progeny array: performance of diploids Vs. tetraploids in pure Vs. mix transects in natural populations. d Germination success in controlled crossings experiment.
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Salony, S., Clo, J., Vallejo-Marín, M. et al. Establishment of polyploidy in natural populations of Mimulus guttatus. Plant Syst Evol 310, 30 (2024). https://doi.org/10.1007/s00606-024-01914-1
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DOI: https://doi.org/10.1007/s00606-024-01914-1
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