Whole-genome duplication leads to significant but inconsistent changes in climatic niche
Language English Country United States Media print-electronic
Document type Journal Article
Grant support
22-29078 K
Grantová Agentura České Republiky (GAČR)
ERC-StG 850852
EC | European Research Council (ERC)
RVO 67985939
Akademie Věd České Republiky (CAS)
PubMed
40504159
PubMed Central
PMC12184512
DOI
10.1073/pnas.2424785122
Knihovny.cz E-resources
- Keywords
- ecological differentiation, environmental niche modelling, meta-analysis, niche evolution, polyploidy,
- MeSH
- Biological Evolution MeSH
- Gene Duplication * MeSH
- Ecosystem * MeSH
- Genome, Plant * MeSH
- Magnoliopsida * genetics MeSH
- Ploidies MeSH
- Climate * MeSH
- Polyploidy * MeSH
- Publication type
- Journal Article MeSH
Polyploidization (whole-genome duplication, WGD) is a widespread large-effect macromutation with far-reaching genomic, phenotypic, and evolutionary consequences. Yet, we do not know whether the consistent phenotypic changes that are associated with polyploidization translate into predictable changes in ecological preferences. Niche modeling studies in mixed-ploidy species provide an opportunity to compare recently originated polyploids with their lower-ploidy ancestors. However, the available isolated studies provide contrasting results and the diverse methodologies used limit generalization. Based on 25,857 georeferenced ploidy-verified occurrence data for 129 mixed-ploidy flowering plant species, we tested in a unified statistical framework whether WGD is associated with consistent changes in climatic niche and in past, current, and predicted future range size. We found that 74% of species exhibited significant niche shifts associated with ploidy transition. However, there was no consistent environmental parameter underlying ploidy differentiation across species, nor was there consistent support for polyploid range or niche expansion in a subset of 75 densely sampled species with sufficient data for modeling. Our results demonstrate that polyploidization is an important factor affecting niche evolution of a species, but the environmental parameters underlying the ploidy-related niche shifts vary from species to species, demonstrating limited predictability of the outcomes of WGD in ecological space.
Department of Botany Charles University of Prague Prague 128 01 Czechia
Institute of Botany The Czech Academy of Sciences Průhonice 252 43 Czechia
See more in PubMed
Comai L., The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6, 836–846 (2005). PubMed
Fox D. T., Soltis D. E., Soltis P. S., Ashman T.-L., Van de Peer Y., Polyploidy: A biological force from cells to ecosystems. Trends Cell Biol. 30, 688–694 (2020). PubMed PMC
Van de Peer Y., Mizrachi E., Marchal K., The evolutionary significance of polyploidy. Nat. Rev. Genet. 18, 411–424 (2017). PubMed
Bomblies K., When everything changes at once: Finding a new normal after genome duplication. Proc. R. Soc. B, Biol. Sci. 287, 20202154 (2020). PubMed PMC
del Pozo J. C., Ramirez-Parra E., Whole genome duplications in plants: An overview from PubMed
Doyle J. J., Coate J. E., Polyploidy, the nucleotype, and novelty: The impact of genome doubling on the biology of the cell. Int. J. Plant Sci. 180, 1–52 (2018).
Stebbins G. L., Chromosomal Evolution in Higher Plants (Edward Arnold Ltd., London, UK, 1971).
Clo J., Kolář F., Short- and long-term consequences of genome doubling: A meta-analysis. Am. J. Bot. 108, 2315–2322 (2021). PubMed
Madlung A., Polyploidy and its effect on evolutionary success: Old questions revisited with new tools. Heredity 110, 99–104 (2013). PubMed PMC
Robinson D. O., et al. , Ploidy and size at multiple scales in the PubMed PMC
Rice A., et al. , The chromosome counts database (CCDB)—A community resource of plant chromosome numbers. New Phytol. 206, 19–26 (2015). PubMed
Hagerup O., Studies on polyploid ecotypes in
Hagerup O., Über polyploidie in beziehung zu klima, ökologie und phylogenie. Hereditas 16, 19–40 (1932).
Tischler G., Die bedeutung der polyploidie für die verbreitung der angiospermen. Bot. Jahrb. 76, 1–35 (1935).
Rohweder H., Beiträge zur systematik und phylogenie des genus
Manton I., The problem of
Ehrendorfer F., Beiträge zur phylogenie der gattung
Ehrendorfer F., Die geographische und ökologische Entfaltung des europäisch-alpinen polyploidkomplexes
Ehrendorfer F., Cytotaxonomische beiträge zur genese der mitteleuropäischen flora und vegetation. Ber. Dtsch. Bot. Ges. 75, 137–152 (1962).
Stebbins G. L., Polyploid complexes in relation to ecology and the history of floras. Am. Nat. 76, 36–45 (1942).
Müntzing A., The evolutionary significance of autopolyploidy. Hereditas 21, 363–378 (1936).
Clausen J., Keck D. D., Hiesey W. M.,
Clausen J. C., Keck D. D., Hiesey W. M., Experimental Studies on The Nature of Species. II: Plant Evolution Through Amphiploidy and Autoploidy, with Examples from The Madiinae (Carnegie Institution of Washington, Washington, DC, 1945).
Lewis W. H., “Polyploidy in species populations” in Polyploidy: Biological Relevance, Lewis W. H., Ed. (Plenum Press, New York, NY, 1980), pp. 103–144.
Ramsey J., Ramsey T. S., Ecological studies of polyploidy in the 100 years following its discovery. Philos. Trans. R. Soc. B, Biol. Sci. 369, 20130352 (2014). PubMed PMC
Favarger C., “Cytogeography and biosystematics” in Plant Biosystematics, Grant W. F., Ed. (Academic Press, Toronto, ON, Canada, 1984), pp. 453–476.
Folk R. A., Siniscalchi C. M., Soltis D. E., Angiosperms at the edge: Extremity, diversity, and phylogeny. Plant Cell Environ. 43, 2871–2893 (2020). PubMed
Levin D. A., Polyploidy and novelty in flowering plants. Am. Nat. 122, 1–25 (1983).
Stebbins G. L., Variation and Evolution in Plants (Columbia University Press, New York, NY, 1950).
Thompson J. D., Lumaret R., The evolutionary dynamics of polyploid plants: Origins, establishment and persistence. Trends Ecol. Evol. 7, 302–307 (1992). PubMed
Maherali H., Walden A. E., Husband B. C., Genome duplication and the evolution of physiological responses to water stress. New Phytol. 184, 721–731 (2009). PubMed
Ramsey J., Polyploidy and ecological adaptation in wild yarrow. Proc. Natl. Acad. Sci. U.S.A. 108, 7096–7101 (2011). PubMed PMC
Van de Peer Y., Ashman T.-L., Soltis P. S., Soltis D. E., Polyploidy: An evolutionary and ecological force in stressful times. Plant Cell 33, 11–26 (2020). PubMed PMC
Warner D. A., Edwards G. E., Effects of polyploidy on photosynthesis. Photosynth. Res. 35, 135–147 (1993). PubMed
Li W.-L., Berlyn G. P., Ashton P. M. S., Polyploids and their structural and physiological characteristics relative to water deficit in
Garbutt K., Bazzaz F. A., Leaf demography, flower production and biomass of diploid and tetraploid populations of
Brochmann C., et al. , Polyploidy in arctic plants. Biol. J. Linn. Soc. 82, 521–536 (2004).
Grant V., Plant Speciation (Columbia University Press, New York, NY, 1981).
Rice A., et al. , The global biogeography of polyploid plants. Nat. Ecol. Evol. 3, 265–273 (2019). PubMed
Love A., Love D., The significance of differences in the distribution of diploids and polyploids. Hereditas 29, 145–163 (1943).
te Beest M., et al. , The more the better? The role of polyploidy in facilitating plant invasions. Ann. Bot. 109, 19–45 (2012). PubMed PMC
Mosquin T., Evidence for autopolyploidy in PubMed
Hardy O. J., Vanderhoeven S., Loose M. D., Meerts P., Ecological, morphological and allozymic differentiation between diploid and tetraploid knapweeds ( PubMed
Lewis W. H., Terrell E. E., Chromosomal races in eastern North American species of
Sharma A. K., Dey D., A comprehensive cytotaxonomic study on the family Chenopodiaceae. J. Cytol. Genet. 2, 114–127 (1967).
Grünig S., Patsiou T., Parisod C., Ice age-driven range shifts of diploids and expanding autotetraploids of PubMed
Hämälä T., et al. , Impact of whole-genome duplications on structural variant evolution in PubMed PMC
Ehrendorfer F., “Polyploidy and distribution” in Polyploidy. Biological Relevance, Lewis W. H., Ed. (Plenum Press, New York, NY, 1980), pp. 45–60.
Hegarty M. J., Hiscock S. J., Genomic clues to the evolutionary success of polyploid plants. Curr. Biol. 18, R435–R444 (2008). PubMed
Parisod C., Holderegger R., Brochmann C., Evolutionary consequences of autopolyploidy. New Phytol. 186, 5–17 (2010). PubMed
Afonso A., et al. , Ecological niches in the polyploid complex PubMed PMC
Gunn B. F., et al. , Evolution of lomandroideae: Multiple origins of polyploidy and biome occupancy in Australia. Mol. Phylogenet. Evol. 149, 106836 (2020). PubMed
Manzaneda A. J., et al. , Environmental aridity is associated with cytotype segregation and polyploidy occurrence in PubMed PMC
Thompson K. A., Husband B. C., Maherali H., Climatic niche differences between diploid and tetraploid cytotypes of PubMed
Karunarathne P., et al. , Intraspecific ecological niche divergence and reproductive shifts foster cytotype displacement and provide ecological opportunity to polyploids. Ann. Bot. 121, 1183–1196 (2018). PubMed PMC
Kirchheimer B., et al. , Reconstructing geographical parthenogenesis: Effects of niche differentiation and reproductive mode on holocene range expansion of an alpine plant. Ecol. Lett. 21, 392–401 (2018). PubMed PMC
Kirchheimer B., et al. , A matter of scale: Apparent niche differentiation of diploid and tetraploid plants may depend on extent and grain of analysis. J. Biogeogr. 43, 716–726 (2016). PubMed PMC
Yang S.-J., et al. , Divergence in cold tolerance promotes niche differentiation between diploid and polyploid kiwifruits along an altitudinal gradient in Southwest China. Oikos 2024, e10181 (2024).
Arrigo N., et al. , Is hybridization driving the evolution of climatic niche in PubMed
Chung M. Y., et al. , Polyploidy in
Duchoslav M., et al. , Intricate distribution patterns of six cytotypes of PubMed PMC
Gaynor M. L., Marchant D. B., Soltis D. E., Soltis P. S., Climatic niche comparison among ploidal levels in the classic autopolyploid system, PubMed
Hanzl M., Kolář F., Nováková D., Suda J., Nonadaptive processes governing early stages of polyploid evolution: Insights from a primary contact zone of relict serpentine PubMed
Morgan E. J., et al. , Niche similarity in diploid-autotetraploid contact zones of PubMed
Sonnleitner M., et al. , Ecological differentiation of diploid and polyploid cytotypes of PubMed PMC
Muñoz-Pajares A. J., et al. , Niche differences may explain the geographic distribution of cytotypes in PubMed
Visger C. J., et al. , Niche divergence between diploid and autotetraploid PubMed
Glennon K. L., Ritchie M. E., Segraves K. A., Evidence for shared broad-scale climatic niches of diploid and polyploid plants. Ecol. Lett. 17, 574–582 (2014). PubMed
Fowler N. L., Levin D. A., Ecological constraints on the establishment of a novel polyploid in competition with its diploid progenitor. Am. Nat. 124, 703–711 (1984).
Rodriguez D. J., A model for the establishment of polyploidy in plants. Am. Nat. 147, 33–46 (1996).
Baniaga A. E., Marx H. E., Arrigo N., Barker M. S., Polyploid plants have faster rates of multivariate niche differentiation than their diploid relatives. Ecol. Lett. 23, 68–78 (2020). PubMed
Chesson P., Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Evol. Syst. 31, 343–366 (2000).
Chesson P., General theory of competitive coexistence in spatially-varying environments. Theor. Popul. Biol. 58, 211–237 (2000). PubMed
Čertner M., Sudová R., Weiser M., Suda J., Kolář F., Ploidy-altered phenotype interacts with local environment and may enhance polyploid establishment in PubMed
Keller S. R., Taylor D. R., History, chance and adaptation during biological invasion: Separating stochastic phenotypic evolution from response to selection. Ecol. Lett. 11, 852–866 (2008). PubMed
Li Z., et al. , Patterns and processes of diploidization in land plants. Annu. Rev. Plant Biol. 72, 387–410 (2021). PubMed
Wendel J. F., The wondrous cycles of polyploidy in plants. Am. J. Bot. 102, 1753–1756 (2015). PubMed
Moody M. E., Mueller L. D., Soltis D. E., Genetic variation and random drift in autotetraploid populations. Genetics 134, 649–657 (1993). PubMed PMC
Otto S. P., Whitton J., Polyploid incidence and evolution. Annu. Rev. Genet. 34, 401–437 (2000). PubMed
Levin D. A., The Role of Chromosomal Change in Plant Evolution (Oxford University Press, Oxford, UK, 2002).
Martin S. L., Husband B. C., Influence of phylogeny and ploidy on species ranges of North American angiosperms. J. Ecol. 97, 913–922 (2009).
Petit C., Thompson J. D., Species diversity and ecological range in relation to ploidy level in the flora of the pyrenees. Evol. Ecol. 13, 45–65 (1999).
Vandel A., La parthénogenèse géographique. Contribution à l’étude biologique et cytologique de la parthénogenèse naturelle. Bull. Biol. Fr. Belg. 62, 164 (1928).
Meirmans P. G., Niche divergence contributes to geographical parthenogenesis in two dandelion taxa. J. Evol. Biol. 34, 1071–1086 (2021). PubMed PMC
Sochor M., et al. , Distinct geographic parthenogenesis in spite of niche conservatism and a single ploidy level: A case of PubMed
Pannell J. R., et al. , The scope of Baker’s law. New Phytol. 208, 656–667 (2015). PubMed
López-Jurado J., Mateos-Naranjo E., Balao F., Niche divergence and limits to expansion in the high polyploid PubMed
Padilla-García N., et al. , The importance of considering the evolutionary history of polyploids when assessing climatic niche evolution. J. Biogeogr. 50, 86–100 (2023).
Soltis D. E., et al. , Autopolyploidy in angiosperms: Have we grossly underestimated the number of species? Taxon 56, 13–30 (2007).
Paule J., et al. , Chromosome numbers of the flora of germany—A new online database of georeferenced chromosome counts and flow cytometric ploidy estimates. Plant Syst. Evol. 303, 1123–1129 (2017).
Kolář F., Čertner M., Suda J., Schönswetter P., Husband B. C., Mixed-ploidy species: Progress and opportunities in polyploid research. Trends Plant Sci. 22, 1041–1055 (2017). PubMed
Di Cola V., et al. , Ecospat: An R package to support spatial analyses and modeling of species niches and distributions. Ecography 40, 774–787 (2017).
Phillips S. J., Anderson R. P., Schapire R. E., Maximum entropy modeling of species geographic distributions. Ecol. Model. 190, 231–259 (2006).
Hijmans R. J., Cameron S. E., Parra J. L., Jones P. G., Jarvis A., Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).
Oksanen J., et al., vegan: Community ecology package (R project Version 2.6-10, 2025). https://CRAN.R-project.org/package=vegan. Accessed 27 May 2025.
Broennimann O., et al. , Measuring ecological niche overlap from occurrence and spatial environmental data. Glob. Ecol. Biogeogr. 21, 481–497 (2012).
Naimi B., Araújo M. B., SDM: A reproducible and extensible R platform for species distribution modelling. Ecography 39, 368–375 (2016).
Liu C., White M., Newell G., Selecting thresholds for the prediction of species occurrence with presence-only data. J. Biogeogr. 40, 778–789 (2013).