It is broadly assumed that polyploidy success results from increased fitness associated with whole genome duplication due to higher tolerance to stressful conditions. In agreement, several theoretical models found that, among other factors, a better tolerance to new environmental conditions can promote polyploidy establishment. Here, we investigated the effect of the genetic and environmental factors affecting the architecture of unreduced gamete production, to see how it affects the origin and persistence of autopolyploids in both stable and disturbed environments. We developed a theoretical model in which we modeled the joint evolution of a quantitative trait under selection and the production of unreduced gametes; both traits were pleiotropically linked. We followed the adaptation of initially diploid populations to a new environment to which tetraploid individuals were directly adapted. The generation of these autotetraploid individuals was enabled by the genetic production of unreduced gametes and by the environmental change modifying the average production of these gametes. We found that for realistic values of unreduced gamete production adaptation to new environmental conditions was mainly achieved through adaptation of diploids to the new optimum rather than the persistence of newly adapted tetraploid individuals. In broader parameter sets, we found that the adaptation process led to mixed-ploidy populations, except when the populations were swamped with unreduced gametes, and that pleiotropy and environmental effects favored the co-existence of both cytotypes.

CNRS Univ Lille UMR 8198 Evo Eco Paleo Lille France

Department of Botany Faculty of Science Charles University Prague Czech Republic

Institute of Botany Czech Academy of Sciences Průhonice Czech Republic

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Albertin W, Marullo P (2012) Polyploidy in fungi: evolution after whole-genome duplication. Proc R Soc B 279:2497–509. PubMed DOI PMC

Almeida-Silva F, Van de Peer Y (2023) Whole-genome duplications and the long-term evolution of gene regulatory networks in angiosperms. Mol Biol Evolut 40:msad141. DOI

Bachmann JA, Tedder A, Fracassetti M, Steige KA, Lafon-Placette C, Köhler C et al. (2021) On the origin of the widespread self-compatible allotetraploid Capsella bursa-pastoris (Brassicaceae). Heredity 127:124–34. PubMed DOI PMC

Baduel P, Hunter B, Yeola S, Bomblies K (2018) Genetic basis and evolution of rapid cycling in railway populations of tetraploid Arabidopsis arenosa. PLoS Genet 14:e1007510. PubMed DOI PMC

Bomblies K (2020) When everything changes at once: finding a new normal after genome duplication. Proc R Soc B 287:20202154. PubMed DOI PMC

Bomblies K (2023) Learning to tango with four (or more): the molecular basis of adaptation to polyploid meiosis. Plant Reprod 36:107–124. PubMed DOI

Bomblies K, Peichel CL (2022) Genetics of adaptation. Proc Natl Acad Sci USA 119:e2122152119. PubMed DOI PMC

Bretagnolle F, Thompson JD (1995) Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plants. N Phytol 129:1–22. DOI

Brownfield L, Kohler C (2011) Unreduced gamete formation in plants: mechanisms and prospects. J Exp Bot 62:1659–68. PubMed DOI

Bürger R, Wagner GP, Stettinger F (1989) How much heritable variation can be maintained in finite populations by mutation–selection balance?. Evolution 43:1748–66. PubMed DOI

Burton TL, Husband B (2000a) Fitness differences among diploids, tetraploids, and their triploid progeny in Chamerion angustifolium: mechanisms of inviability and implications for polyploid evolution. Evolution 54:1182–91. PubMed DOI

Clo J (2022a) Polyploidization: Consequences of genome doubling on the evolutionary potential of populations. Am J Bot 109:1213–20. PubMed DOI

Clo J (2022b) The evolution of the additive variance of a trait under stabilizing selection after autopolyploidization. J Evolut Biol 35:891–7. DOI

Clo J, Kolář F (2021) Short- and long-term consequences of genome doubling: a meta-analysis. Am J Bot 108:2315–22. PubMed DOI

Clo J, Opedal ØH (2021) Genetics of quantitative traits with dominance under stabilizing and directional selection in partially selfing species. Evolution 75:1920–35. PubMed DOI

Clo J, Padilla-García N, Kolář F (2022) Polyploidization as an opportunistic mutation: The role of unreduced gametes formation and genetic drift in polyploid establishment. J Evolut Biol 35:1099–109. DOI

Clo J, Ronfort J, Abu Awad D (2020) Hidden genetic variance contributes to increase the short-term adaptive potential of selfing populations. J Evolut Biol 33:1203–15. DOI

De Storme N, Copenhaver GP, Geelen D (2012) Production of diploid male gametes in arabidopsis by cold-induced destabilization of postmeiotic radial microtubule arrays. Plant Physiol 160:1808–1826. PubMed DOI PMC

De Storme N, Geelen D (2013) Sexual polyploidization in plants–cytological mechanisms and molecular regulation. N Phytol 198:670–684. DOI

Doyle JJ, Coate JE (2019) Polyploidy, the nucleotype, and novelty: the impact of genome doubling on the biology of the cell. Int J Plant Sci 180:1–52. DOI

d’Erfurth I, Cromer L, Jolivet S, Girard C, Horlow C, Sun Y et al. (2010) The CYCLIN-A CYCA1;2/TAM Is required for the meiosis I to meiosis II transition and cooperates with OSD1 for the prophase to first meiotic division transition. PLoS Genet 6:e1000989. PubMed DOI PMC

Erilova A, Brownfield L, Exner V, Rosa M, Twell D, Scheid OM et al. (2009) Imprinting of the polycomb group gene MEDEA serves as a ploidy sensor in Arabidopsis. PLoS Genet 5:e1000663. PubMed DOI PMC

Felber F (1991) Establishment of a tetraploid cytotype in a diploid population: Effect of relative fitness of the cytotypes. J Evolut Biol 4:195–207. DOI

Fraïsse C, Puixeu Sala G, Vicoso B (2019) Pleiotropy modulates the efficacy of selection in Drosophila melanogaster. Mol Biol Evolut 36:500–15. DOI

Gaynor, ML, Kortessis, N, Soltis, DE, Soltis, PS Ponciano, JM (2023) Dynamics of mixed-ploidy populations under demographic and environmental stochasticities. BioRxiv, 2023.03. 29.534764

Gengyo-Ando K, Mitani S (2000) Characterization of mutations induced by ethyl methanesulfonate, UV, and trimethylpsoralen in the nematode Caenorhabditis elegans. Biochem Biophys Res Commun 269:64–69. PubMed DOI

Gerstner BP, Wearing HJ, Whitney KD (2024) Why so many polyploids? Accounting for environmental stochasticity in unreduced gamete formation lowers the perceived barriers to polyploid establishment. J Evolut Biol 37:325–35. DOI

Gregory, TR & MABLE, BK (2005) Polyploidy in animals. In: The evolution of the genome. Elsevier, pp. 427–517.

Griswold CK (2021) The effects of migration load, selfing, inbreeding depression, and the genetics of adaptation on autotetraploid versus diploid establishment in peripheral habitats. Evolution 75:39–55. PubMed DOI

Halligan DL, Keightley PD (2009) Spontaneous mutation accumulation studies in evolutionary genetics. Annu Rev Ecol Evolut Syst 40:151–172. DOI

Husband BC (2004) The role of triploid hybrids in the evolutionary dynamics of mixed-ploidy populations: triploids in mixed-ploidy populations. Biol J Linn Soc 82:537–46. DOI

Husband BC, Sabara HA (2004) Reproductive isolation between autotetraploids and their diploid progenitors in fireweed, Chamerion angustifolium (Onagraceae). N Phytol 161:703–13. DOI

Jiang J, Yang N, Li L, Qin G, Ren K, Wang H et al. (2022) Tetraploidy in Citrus wilsonii enhances drought tolerance via synergistic regulation of photosynthesis, phosphorylation, and hormonal changes. Front Plant Sci 13:875011. PubMed DOI PMC

Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE et al. (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473:97–100. PubMed DOI

Kauai F, Bafort Q, Mortier F, Van Montagu M, Bonte D, Van De Peer Y (2024) Interspecific transfer of genetic information through polyploid bridges. Proc Natl Acad Sci USA 121:e2400018121. PubMed DOI PMC

Kauai F, Mortier F, Milosavljevic S, Van De Peer Y, Bonte D (2023) Neutral processes underlying the macro eco-evolutionary dynamics of mixed-ploidy systems. Proc R Soc B 290:20222456. PubMed DOI PMC

Kolář F, Čertner M, Suda J, Schönswetter P, Husband BC (2017) Mixed-ploidy species: progress and opportunities in polyploid research. Trends Plant Sci 22:1041–55. PubMed DOI

Kreiner JM, Kron P, Husband BC (2017a) Evolutionary dynamics of unreduced gametes. Trends Genet 33:583–93. PubMed DOI

Kreiner JM, Kron P, Husband BC (2017b) Frequency and maintenance of unreduced gametes in natural plant populations: associations with reproductive mode, life history and genome size. N Phytol 214:879–89. DOI

Levin DA (1975) Minority cytotype exclusion in local plant populations. TAXON 24:35–43. DOI

Levin DA (2019) Why polyploid exceptionalism is not accompanied by reduced extinction rates. Plant Syst Evol 305:1–11. DOI

Lv Z, Addo Nyarko C, Ramtekey V, Behn H, Mason, AS (2024) Defining autopolyploidy: Cytology, genetics, and taxonomy. Am J Bot 111:e16292.

Mackay TF, Anholt RR (2024) Pleiotropy, epistasis and the genetic architecture of quantitative traits. Nat Rev Genet 25(9):639–57. DOI

Madlung A (2013) Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity 110:99–104. PubMed DOI

Maherali H, Walden AE, Husband BC (2009) Genome duplication and the evolution of physiological responses to water stress. N Phytol 184:721–31. DOI

Mai Y, Li H, Suo Y, Fu J, Sun P, Han W et al. (2019) High temperature treatment generates unreduced pollen in persimmon (Diospyros kaki Thunb.). Sci Horticulturae 258:108774. DOI

Manna F, Martin G, Lenormand T (2011) Fitness landscapes: an alternative theory for the dominance of mutation. Genetics 189:923–37. PubMed DOI PMC

Mason AS, Nelson MN, Yan G, Cowling WA (2011) Production of viable male unreduced gametes in Brassica interspecific hybrids is genotype specific and stimulated by cold temperatures. BMC Plant Biol 11: 103. PubMed DOI PMC

Mason AS, Pires JC (2015) Unreduced gametes: meiotic mishap or evolutionary mechanism?. Trends Genet 31:5–10. PubMed DOI

Mayrose I, Zhan SH, Rothfels CJ, Magnuson-Ford K, Barker MS, Rieseberg LH et al. (2011) Recently formed polyploid plants diversify at lower rates. Science 333:1257–57. PubMed DOI

Nocchi G, Whiting JR, Yeaman S (2024) Repeated global adaptation across plant species. Proc Natl Acad Sci 121:e2406832121. PubMed DOI PMC

Novikova PY, Brennan IG, Booker W, Mahony M, Doughty P, Lemmon AR et al. (2020) Polyploidy breaks speciation barriers in Australian burrowing frogs Neobatrachus. PLoS Genet 16:e1008769. PubMed DOI PMC

Orr HA (2000) Adaptation and the cost of complexity. Evolution 54:13–20. PubMed DOI

Oswald BP, Nuismer SL (2011) A unified model of autopolyploid establishment and evolution. Am Naturalist 178:687–700. DOI

Otto SP (2007) The evolutionary consequences of polyploidy. Cell 131:452–62. PubMed DOI

Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–37. PubMed DOI

Parrott W, Smith R (1986) Recurrent selection for 2n pollen formation in red clover 1. Crop Sci 26:1132–5. DOI

Pecrix Y, Rallo G, Folzer H, Cigna M, Gudin S, Le Bris M (2011) Polyploidization mechanisms: temperature environment can induce diploid gamete formation in Rosa sp. J Exp Bot 62:3587–97. PubMed DOI

Porturas LD, Anneberg TJ, Curé AE, Wang S, Althoff DM, Segraves KA (2019) A meta-analysis of whole genome duplication and the effects on flowering traits in plants. Am J Bot 106:469–76. PubMed DOI

Ravi M, Marimuthu MP, Siddiqi I (2008) Gamete formation without meiosis in Arabidopsis. Nature 451:1121–4. PubMed DOI

Rice A, Šmarda P, Novosolov M, Drori M, Glick L, Sabath N et al. (2019) The global biogeography of polyploid plants. Nat Ecol Evol 3:265–73. PubMed DOI

Ronce O, Shaw FH, Rousset F, Shaw RG (2009) Is inbreeding depression lower in maladapted populations? A quantitative genetics model. Evolution 63:1807–19. PubMed DOI

Schindfessel C, De Storme N, Trinh HK, Geelen D (2023) Asynapsis and meiotic restitution in tomato male meiosis induced by heat stress. Front Plant Sci 14:1210092. PubMed DOI PMC

Soltis PS, Marchant DB, Van De Peer Y, Soltis DE (2015) Polyploidy and genome evolution in plants. Curr Opin Genet Dev 35:119–25. PubMed DOI

Spoelhof JP, Keeffe R, McDaniel, SF (2020) Does reproductive assurance explain the incidence of polyploidy in plants and animals? New Phytol 227:14–21.

Tavoletti S, Mariani A, Veronesi F (1991a) Cytological analysis of macro- and microsporogenesis of a diploid alfalfa clone producing male and female 2 n gametes. Crop Sci 31:1258–63. DOI

Tavoletti S, Mariani A, Veronesi F (1991b) Phenotypic recurrent selection for 2n pollen and 2n egg production in diploid alfalfa. Euphytica 57:97–102. DOI

Van de Peer Y, Ashman, TL, Soltis PS, Soltis DE (2021) Polyploidy: an evolutionary and ecological force in stressful times. The Plant Cell, vol 33. Oxford Academic, pp 11–26.

Van Drunen WE, Friedman J (2022) Autopolyploid establishment depends on life-history strategy and the mating outcomes of clonal architeOxford Academiccture. Evolution 76:1953–1970. PubMed DOI

Wang C, Ge W, Yin H, Zhang Y, Li J (2024) MicroRNAs and their targets involved in unreduced pollen formation induced by heat stress in Camellia nitidissima. Sci Horticulturae 323:112462. DOI

Wang C-J, Zhang L-Q, Dai S-F, Zheng Y-L, Zhang H-G, Liu D-C (2010) Formation of unreduced gametes is impeded by homologous chromosome pairing in tetraploid Triticum turgidum × Aegilops tauschii hybrids. Euphytica 175:323–9. DOI

Wang J, Li D, Shang F, Kang X (2017) High temperature-induced production of unreduced pollen and its cytological effects in Populus. Sci Rep 7: 5281. PubMed DOI PMC

Wang Z, Zhao Z, Fan G, Dong Y, Deng M, Xu E et al. (2019) A comparison of the transcriptomes between diploid and autotetraploid Paulownia fortunei under salt stress. Physiol Mol Biol Plants 25:1–11. PubMed DOI

Whiting JR, Booker TR, Rougeux C, Lind BM, Singh P, Lu M et al. (2024) The genetic architecture of repeated local adaptation to climate in distantly related plants. Nat Ecol Evol 8:1933–47. PubMed DOI PMC

Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH (2009) The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci USA 106:13875–79. PubMed DOI PMC

Wu G-Q, Lin L-Y, Jiao Q, Li S-J (2019) Tetraploid exhibits more tolerant to salinity than diploid in sugar beet (Beta vulgaris L.). Acta Physiol Plant 41:52. DOI

Zhang J (2023) Patterns and evolutionary consequences of pleiotropy. Annu Rev Ecol Evol Syst 54:1–19. PubMed DOI PMC