Compared to animals, plants show a wide range of reproductive strategies with different degrees of sex separation (e.g. dioecy, monoecy, hermaphroditism). While sex expression was previously thought to be genetically determined and fixed in plants, accumulating evidence suggests that sex expression can change reversibly even within one generation (sex changes), involving non-genetic factors (i.e. environment and epigenetics). In addition, recent work suggests that sex determination itself relies on epigenetic factors. Therefore, in this review, we propose that the border between sex changes and the apparently "fixed" determination of sexes is less clear than previously thought, as they rely on similar mechanisms, in particular epigenetics. Specifically, we propose that within-generation sex changes may facilitate evolutionary transitions between different degrees of sex separation via the assimilation of epimutations into genetic mutations. We then evaluate the (mal)adaptive potential of sex changes. We conclude that in the face of global environmental changes, sex changes may follow a bet-hedging evolutionary strategy, that is a heritable ability to reverse sexes. Sexual bet-hedging with an epigenetic basis (via stochastic epimutations) may help plants alleviate the deleterious consequences of climate change.

Department of Botany Faculty of Science Charles University Benátská 2 Prague 12800 Czech Republic

Institute of Botany Czech Academy of Sciences Zámek 1 Průhonice 252 43 Czech Republic

Institute of Botany Plant Science and Biodiversity Centre Slovak Academy of Sciences Dúbravská cesta 9 Bratislava 845 23 Slovakia

Zobrazit více v PubMed

Acar, M. , Mettetal, J. T. & Van Oudenaarden, A. (2008). Stochastic switching as a survival strategy in fluctuating environments. Nature Genetics 40, 471–475. PubMed

Aguirre, A. , Vallejo‐Marín, M. , Salazar‐Goroztieta, L. , Arias, D. M. & Dirzo, R. (2007). Variation in sexual expression in

Ahmed, I. , Sarazin, A. , Bowler, C. , Colot, V. & Quesneville, H. (2011). Genome‐wide evidence for local DNA methylation spreading from small RNA‐targeted sequences in Arabidopsis. Nucleic Acids Research 39, 6919–6931. PubMed PMC

Akagi, T. , Henry, I. M. , Kawai, T. , Comai, L. & Tao, R. (2016). Epigenetic regulation of the sex determination gene PubMed PMC

Akagi, T. , Henry, I. M. , Tao, R. & Comai, L. (2014). A Y‐chromosome–encoded small RNA acts as a sex determinant in persimmons. In Plant Genetics. A Y‐Chromosome‐Encoded Small RNA Acts as a Sex Determinant in Persimmons. Science (Volume 346), pp. 646–650. American Association for the Advancement of Science, New York, N.Y. PubMed

Arnold, P. A. , Nicotra, A. B. & Kruuk, L. E. B. (2019). Sparse evidence for selection on phenotypic plasticity in response to temperature. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 374, 20180185. PubMed PMC

Ashe, A. , Colot, V. & Oldroyd, B. P. (2021). How does epigenetics influence the course of evolution? Philosophical Transactions of the Royal Society B: Biological Sciences 376, 20200111. PubMed PMC

Ashman, T.‐L. (1999). Determinants of sex allocation in a gynodioecious wild strawberry: implications for the evolution of dioecy and sexual dimorphism. Journal of Evolutionary Biology 12, 648–661.

Bai, Q. , Ma, Z. , Zhang, Y. , Su, S. & Leng, P. (2019). The sex expression and sex determining mechanism in PubMed PMC

Baker, H. G. (1958). Studies in the reproductive biology of West African Rubiaceae. Journal of the West African Science Association 4, 9–24.

Barrett, S. C. H. (2002). The evolution of plant sexual diversity. Nature Reviews Genetics 3, 274–284. PubMed

Barrett, S. C. H. (2013). The evolution of plant reproductive systems: how often are transitions irreversible? Proceedings of the Royal Society B: Biological Sciences 280, 20130913. PubMed PMC

Barrett, S. C. H. & Richards, J. H. (1990). Heterostyly in tropical plants. 55, 35–61.

Baulcombe, D. C. & Dean, C. (2014). Epigenetic regulation in plant responses to the environment. Cold Spring Harbor Perspectives in Biology 6, a019471. PubMed PMC

Bawa, K. S. (1980). Evolution of dioecy in flowering plants. Annual Review of Ecology and Systematics 11, 15–39.

Bawa, K. S. & Opler, P. A. (1977). Spatial relationships between staminate and pistillate plants of dioecious tropical forest trees. Evolution 31, 64–68. PubMed

Becker, C. , Hagmann, J. , Müller, J. , Koenig, D. , Stegle, O. , Borgwardt, K. & Weigel, D. (2011). Spontaneous epigenetic variation in the PubMed

Berjano, R. , Arista, M. , Talavera, M. , Ariza, J. & Ortiz, P. L. (2014). Plasticity and within plant sex‐ratio variation in monoecious

Billiard, S. , Husse, L. , Lepercq, P. , Godé, C. , Bourceaux, A. , Lepart, J. , Vernet, P. & Saumitou‐Laprade, P. (2015). Selfish male‐determining element favors the transition from hermaphroditism to androdioecy. Evolution 69, 683–693. PubMed

Blake‐Mahmud, J. & Struwe, L. (2019). Time for a change: patterns of sex expression, health and mortality in a sex‐changing tree. Annals of Botany 124, 367–377. PubMed PMC

Botero, C. A. , Weissing, F. J. , Wright, J. & Rubenstein, D. R. (2015). Evolutionary tipping points in the capacity to adapt to environmental change. Proceedings of the National Academy of Sciences 112, 184–189. PubMed PMC

Bräutigam, K. & Cronk, Q. (2018). DNA methylation and the evolution of developmental complexity in plants. Frontiers in Plant Science 9, 1447. PubMed PMC

Bull, J. J. & Charnov, E. L. (1985). On irreversible evolution. Evolution 39, 1149–1155. PubMed

Burgess, S. C. & Marshall, D. J. (2014). Adaptive parental effects: the importance of estimating environmental predictability and offspring fitness appropriately. Oikos 123, 769–776.

Bürli, S. , Pannell, J. R. & Tonnabel, J. (2022). Environmental variation in sex ratios and sexual dimorphism in three wind‐pollinated dioecious plant species. Oikos 2022, e08651.

Cardoso, J. C. F. , Viana, M. L. , Matias, R. , Furtado, M. T. , Caetano, A. P. d. S. , Consolaro, H. & de Brito, V. L. G. (2018). Towards a unified terminology for angiosperm reproductive system. Acta Botanica Brasilica 32, 329–348.

Caruso, C. M. & Case, A. L. (2007). Sex ratio variation in gynodioecious PubMed

Caruso, C. M. , Eisen, K. & Case, A. L. (2016). An angiosperm‐wide analysis of the correlates of gynodioecy. International Journal of Plant Sciences 177, 115–121.

Charlesworth, B. & Charlesworth, D. (1978). A model for the evolution of dioecy and gynodioecy. The American Naturalist 112, 975–997.

Charlesworth, D. (2006). Evolution of plant breeding systems. Current Biology 16, R726–R735. PubMed

Charlesworth, D. & Willis, J. H. (2009). The genetics of inbreeding depression. Nature Reviews Genetics 10, 783–796. PubMed

Charnov, E. L. (1987). On sex allocation and selfing in higher plants. Evolutionary Ecology 1, 30–36.

Chen, J. , Liu, Q. , Yu, L. , Korpelainen, H. , Niinemets, Ü. & Li, C. (2021). Elevated temperature and CO

Chen, P. & Zhang, J. (2023). Transcriptomic analysis reveals the rareness of genetic assimilation of gene expression in environmental adaptations. Science Advances 9, eadi3053. PubMed PMC

Consuegra, S. & Rodríguez López, C. M. (2016). Epigenetic‐induced alterations in sex‐ratios in response to climate change: an epigenetic trap? BioEssays 38, 950–958. PubMed

Corl, A. , Bi, K. , Luke, C. , Challa, A. S. , Stern, A. J. , Sinervo, B. & Nielsen, R. (2018). The genetic basis of adaptation following plastic changes in coloration in a novel environment. Current Biology 28, 2970–2977.e7. PubMed

Cossard, G. G. , Gerchen, J. F. , Li, X. , Cuenot, Y. & Pannell, J. R. (2021). The rapid dissolution of dioecy by experimental evolution. Current Biology: CB 31, 1277–1283. PubMed

Cossard, G. G. & Pannell, J. R. (2021). Enhanced leaky sex expression in response to pollen limitation in the dioecious plant PubMed PMC

Cox, P. A. (1981). Niche partitioning between sexes of dioecious plants. The American Naturalist 117, 295–307.

Dang, T. T. T. & Chinnappa, C. C. (2007). The reproductive biology of

Darwin, C. (1877). The Different Forms of Flowers on Plants of the Same Species. John Murray, London. 10.1017/CBO9780511731419. DOI

Datwyler, S. L. & Weiblen, G. D. (2004). On the origin of the fig: phylogenetic relationships of Moraceae from ndhF sequences. American Journal of Botany 91, 767–777. PubMed

Dawson, T. E. & Bliss, L. C. (1989). Patterns of water use and the tissue water relations in the dioecious shrub, PubMed

de Jong, T. J. , Shmida, A. & Thuijsman, F. (2008). Sex allocation in plants and the evolution of monoecy. Evolutionary Ecology Research 10, 1087–1109.

Delaigue, M. , Poulain, T. & Durand, B. (1984). Phytohormone control of translatable RNA populations in sexual organogenesis of the dioecious plant PubMed

Delph, L. F. (2009). Sex allocation: evolution to and from dioecy. Current Biology 19, R249–R251. PubMed

Delph, L. F. & Wolf, D. E. (2005). Evolutionary consequences of gender plasticity in genetically dimorphic breeding systems. New Phytologist 166, 119–128. PubMed

DeWitt, T. J. , Sih, A. & Wilson, D. S. (1998). Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution 13, 77–81. PubMed

Diggle, P. K. (1994). The expression of andromonoecy in

Diggle, P. K. & Miller, J. S. (2013). Developmental plasticity, genetic assimilation, and the evolutionary diversification of sexual expression in Solanum. American Journal of Botany 100, 1050–1060. PubMed

Donelan, S. C. , Hellmann, J. K. , Bell, A. M. , Luttbeg, B. , Orrock, J. L. , Sheriff, M. J. & Sih, A. (2020). Transgenerational plasticity in human‐altered environments. Trends in Ecology & Evolution 35, 115–124. PubMed PMC

Dorken, M. E. & Barrett, S. C. H. (2004). Sex determination and the evolution of dioecy from monoecy in PubMed PMC

Dornier, A. & Dufay, M. (2013). How selfing, inbreeding depression, and pollen limitation impact nuclear‐cytoplasmic gynodioecy: a model. Evolution 67, 2674–2687. PubMed

Du, Z. Y. & Wang, Q. F. (2014). Correlations of life form, pollination mode and sexual system in aquatic angiosperms. PLoS One 9, e115653. PubMed PMC

Duan, T. , Deng, X. , Chen, S. , Luo, Z. , Zhao, Z. , Tu, T. , Khang, N. S. , Razafimandimbison, S. G. & Zhang, D. (2018). Evolution of sexual systems and growth habit in PubMed

Dubin, M. J. , Zhang, P. , Meng, D. , Remigereau, M. S. , Osborne, E. J. , Casale, F. P. , Drewe, P. , Kahles, A. , Jean, G. , Vilhjálmsson, B. , Jagoda, J. , Irez, S. , Voronin, V. , Song, Q. , Long, Q. , PubMed PMC

Dudley, L. S. (2006). Ecological correlates of secondary sexual dimorphism in PubMed

Dufay, M. , Champelovier, P. , Käfer, J. , Henry, J. P. , Mousset, S. & Marais, G. A. B. (2014). An angiosperm‐wide analysis of the gynodioecy–dioecy pathway. Annals of Botany 114, 539–548. PubMed PMC

Durand, B. & Durand, R. (1991). Sex determination and reproductive organ differentiation in

Eckhart, V. M. (1992). Resource compensation and the evolution of gynodioecy in PubMed

Edwards, A. W. F. (2000). Carl Düsing (1884) on the regulation of the sex‐ratio. Theoretical Population Biology 58, 255–257. PubMed

Ehlers, B. K. & Bataillon, T. (2007). “Inconstant males” and the maintenance of labile sex expression in subdioecious plants. New Phytologist 174, 194–211. PubMed

El‐Keblawy, A. & Freeman, D. C. (1999). Spatial segregation by gender of the subdioecious shrub

El‐Keblawy, A. , Lovett Doust, J. , Lovett Doust, L. & Shaltout, K. H. (1995). Labile sex expression and dynamics of gender in

Engen, S. , Lande, R. & Sæther, B. E. (2003). Demographic stochasticity and allee effects in populations with two sexes. Ecology 84, 2378–2386.

Eppley, S. M. (2005). Spatial segregation of the sexes and nutrients affect reproductive success in a dioecious wind‐pollinated grass. Plant Ecology 181, 179–190.

Field, D. L. , Pickup, M. & Barrett, S. C. H. (2013). Ecological context and metapopulation dynamics affect sex‐ratio variation among dioecious plant populations. Annals of Botany 111, 917–923. PubMed PMC

Finnegan, E. J. , Genger, R. K. , Peacock, W. J. & Dennis, E. S. (1998). DNA methylation in plants. Annual Review of Plant Physiology and Plant Molecular Biology 49, 223–247. PubMed

Fox, R. J. , Donelson, J. M. , Schunter, C. , Ravasi, T. & Gaitán‐Espitia, J. D. (2019). Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. Philosophical Transactions of the Royal Society B: Biological Sciences 374, 20180174. PubMed PMC

Fraser, D. & Kærn, M. (2009). A chance at survival: gene expression noise and phenotypic diversification strategies. Molecular Microbiology 71, 1333–1340. PubMed

Freeman, D. C. , Harper, K. T. & Charnov, E. L. (1980). Sex change in plants: old and new observations and new hypotheses. Oecologia 47, 222–232. PubMed

Freeman, D. C. , Klikoff, L. G. & Harper, K. T. (1976). Differential resource utilization by the sexes of dioecious plants. Science 193, 597–599. PubMed

Freeman, D. C. & McArthur, E. D. (1984). The relative influences of mortality, nonflowering, and sex change on the sex ratios of six

Freeman, D. C. , McArthur, E. D. & Harper, K. T. (1984). The adaptive significance of sexual lability in plants using

Freeman, D. C. , McArthur, E. D. , Harper, K. T. & Blauer, A. C. (1981). Influence of environment on the floral sex ratio of monoecious plants. Evolution 35, 194. PubMed

Friedman, J. & Barrett, S. C. H. (2011). Genetic and environmental control of temporal and size‐dependent sex allocation in a wind‐pollinated plant. Evolution 65, 2061–2074. PubMed

Gabriel, W. (2005). How stress selects for reversible phenotypic plasticity. Journal of Evolutionary Biology 18, 873–883. PubMed

Ganders, F. R. (1979). The biology of heterostyly. New Zealand Journal of Botany 17, 607–635.

Garbarino, M. , Weisberg, P. J. , Bagnara, L. & Urbinati, C. (2015). Sex‐related spatial segregation along environmental gradients in the dioecious conifer,

Gerashchenkov, G. A. & Rozhnova, N. A. (2013). The involvement of phytohormones in the plant sex regulation. Russian Journal of Plant Physiology 60, 597–610.

Godin, V. N. & Demyanova, E. I. (2013). On the distribution of gynodioecy in flowering plants. Botanicheskii Zhurnal 93, 1465–1487.

Goldberg, E. E. , Otto, S. P. , Vamosi, J. C. , Mayrose, I. , Sabath, N. , Ming, R. & Ashman, T. (2017). Macroevolutionary synthesis of flowering plant sexual systems. Evolution 71, 898–912. PubMed

Golenberg, E. M. & West, N. W. (2013). Hormonal interactions and gene regulation can link monoecy and environmental plasticity to the evolution of dioecy in plants. American Journal of Botany 100, 1022–1037. PubMed

Hayward, A. P. , Moreno, M. A. , Howard, T. P. , Hague, J. , Nelson, K. , Heffelfinger, C. , Romero, S. , Kausch, A. P. , Glauser, G. , Acosta, I. F. , Motinger, J. P. & Dellaporta, S. L. (2016). Control of sexuality by the PubMed PMC

Heilbuth, J. C. (2000). Lower species richness in dioecious clades. The American Naturalist 156, 221–241. PubMed

Himmelreich, S. , Breitwieser, I. & Oberprieler, C. (2012). Phylogeny, biogeography, and evolution of sex expression in the southern hemisphere genus PubMed

Horovitz, A. & Galil, J. (1972). Gynodioecism in East Mediterranean

Jablonka, E. & Lamb, M. J. (1998). Epigenetic inheritance in evolution. Journal of Evolutionary Biology 11, 159–183.

Jablonka, E. V. A. & Raz, G. A. L. (2009). Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Quarterly Review of Biology 84, 131–176. PubMed

Jang, T. S. & Hong, S. P. (2011). Gynodioecy and floral dimorphism of

Janoušek, B. , Široký, J. & Vyskot, B. (1996). Epigenetic control of sexual phenotype in a dioecious plant, PubMed

Johannes, F. & Schmitz, R. J. (2019). Spontaneous epimutations in plants. New Phytologist 221, 1253–1259. PubMed

Käfer, J. , Marais, G. A. B. & Pannell, J. R. (2017). On the rarity of dioecy in flowering plants. Molecular Ecology 26, 1225–1241. PubMed

Käfer, J. , Méndez, M. & Mousset, S. (2022). Labile sex expression in angiosperm species with sex chromosomes. Philosophical Transactions of the Royal Society B: Biological Sciences 377, 20210216. PubMed PMC

Käfer, J. , Talianová, M. , Bigot, T. , Michu, E. , Guéguen, L. , Widmer, A. , Žlůvová, J. , Glémin, S. & Marais, G. A. B. (2013). Patterns of molecular evolution in dioecious and non‐dioecious PubMed

Karasawa, M. M. G. (ed.) (2015). Reproductive Diversity of Plants: An Evolutionary Perspective and Genetic Basis. Springer, Cham.

Khadka, J. , Yadav, N. S. , Guy, M. , Grafi, G. & Golan‐Goldhirsh, A. (2019). Epigenetic aspects of floral homeotic genes in relation to sexual dimorphism in the dioecious plant PubMed PMC

Klironomos, F. D. , Berg, J. & Collins, S. (2013). How epigenetic mutations can affect genetic evolution: model and mechanism. BioEssays 35, 571–578. PubMed

Koelewijn, H. P. & Van Damme, J. M. M. (1996). Gender variation, partial male sterility and labile sex expression in gynodioecious PubMed

Korpelainen, H. (1998). Labile sex expression in plants. Biological Reviews 73, 157–180.

Kučera, J. , Svitok, M. , Gbúrová Štubňová, E. , Mártonfiová, L. , Lafon Placette, C. & Slovák, M. (2021). Eunuchs or females? Causes and consequences of gynodioecy on morphology, ploidy, and ecology of PubMed PMC

Kussell, E. & Leibler, S. (2005). Phenotypic diversity, population growth, and information in fluctuating environments. Science (New York, N.Y.) 309, 2075–2078. PubMed

Lachmann, M. & Jablonka, E. (1996). The inheritance of phenotypes: an adaptation to fluctuating environments. Journal of Theoretical Biology 181, 1–9. PubMed

Lai, Y.‐S. , Shen, D. , Zhang, W. , Zhang, X. , Qiu, Y. , Wang, H. , Dou, X. , Li, S. , Wu, Y. , Song, J. , Ji, G. & Li, X. (2018). Temperature and photoperiod changes affect cucumber sex expression by different epigenetic regulations. BMC Plant Biology 18, 1–13. PubMed PMC

Leite Montalvão, A. P. , Kersten, B. , Fladung, M. & Müller, N. A. (2021). The diversity and dynamics of sex determination in dioecious plants. Frontiers in Plant Science 11, 580488. PubMed PMC

Lester, D. T. (1963). Variation in sex expression in

Leung, C. , Breton, S. & Angers, B. (2016). Facing environmental predictability with different sources of epigenetic variation. Ecology and Evolution 6, 5234–5245. PubMed PMC

Lloyd, D. G. (1972). Breeding systems in

Lloyd, D. G. (1975). Breeding systems in

Lloyd, D. G. (1980). The distributions of gender in four angiosperm species illustrating two evolutionary pathways to dioecy. Evolution 34, 123–134. PubMed

Maini, J. S. & Coupland, R. T. (2011). Anomalous floral organization in Populus tremuloides. 42, 835–839. 10.1139/b64-076. DOI

Mangla, Y. , Das, K. , Bali, S. , Ambreen, H. , Raina, S. N. , Tandon, R. & Goel, S. (2019). Occurrence of subdioecy and scarcity of gender‐specific markers reveal an ongoing transition to dioecy in Himalayan seabuckthorn ( PubMed PMC

Masuda, K. , Akagi, T. , Esumi, T. & Tao, R. (2020). Epigenetic flexibility underlies somaclonal sex conversions in hexaploid Persimmon. Plant and Cell Physiology 61, 393–402. PubMed

Maury, S. , Sow, M. D. , Le Gac, A. L. , Genitoni, J. , Lafon‐Placette, C. & Mozgova, I. (2019). Phytohormone and chromatin crosstalk: the missing link for developmental plasticity? Frontiers in Plant Science 10, 395. PubMed PMC

Melnikova, N. V. , Borkhert, E. V. , Snezhkina, A. V. , Kudryavtseva, A. V. & Dmitriev, A. A. (2017). Sex‐specific response to stress in PubMed PMC

Miller, T. E. X. & Compagnoni, A. (2022). Two‐sex demography, sexual niche differentiation, and the geographic range limits of Texas bluegrass ( PubMed

Müller, N. A. , Kersten, B. , Leite Montalvão, A. P. , Mähler, N. , Bernhardsson, C. , Bräutigam, K. , Carracedo Lorenzo, Z. , Hoenicka, H. , Kumar, V. , Mader, M. , Pakull, B. , Robinson, K. M. , Sabatti, M. , Vettori, C. , Ingvarsson, P. K. , PubMed

Muyle, A. , Bachtrog, D. , Marais, G. A. B. & Turner, J. M. A. (2021). Epigenetics drive the evolution of sex chromosomes in animals and plants. Philosophical Transactions of the Royal Society B 376, 20200124. PubMed PMC

Nagamitsu, T. & Futamura, N. (2014). Sex expression and inbreeding depression in progeny derived from an extraordinary hermaphrodite of PubMed PMC

Naiki, A. & Kato, M. (1999). Pollination system and evolution of dioecy from distyly in

Nanami, S. , Kawaguchi, H. & Yamakura, T. (2004). Sex change towards female in dying PubMed PMC

Niederhuth, C. E. & Schmitz, R. J. (2014). Covering your bases: inheritance of DNA methylation in plant genomes. Molecular Plant 7, 472–480. PubMed PMC

Niederhuth, C. E. & Schmitz, R. J. (2017). Putting DNA methylation in context: from genomes to gene expression in plants. Biochimica et Biophysica Acta. Gene Regulatory Mechanisms 1860, 149–156. PubMed PMC

Nishikawa, K. & Kinjo, A. R. (2018). Mechanism of evolution by genetic assimilation. Biophysical Reviews 10, 667–676. PubMed PMC

Novotná, K. & Štochlová, P. (2013). Aspects of sexual reproduction in rare monoecious

O'Dea, R. E. , Noble, D. W. A. , Johnson, S. L. , Hesselson, D. & Nakagawa, S. (2016). The role of non‐genetic inheritance in evolutionary rescue: epigenetic buffering, heritable bet hedging and epigenetic traps. Environmental Epigenetics 2, 1–12. PubMed PMC

Othmani, A. , Collin, M. , Sellemi, A. , Jain, S. M. , Drira, N. & Aberlenc, F. (2017). First reported case of spontaneous hermaphrodism in female date palm (

Pannell, J. R. (2002). The evolution and maintenance of androdioecy. Annual Review of Ecology and Systematics 33, 397–425.

Pannell, J. R. (2017). Plant sex determination. Current Biology 27, R191–R197. PubMed

Pannell, J. R. , Dorken, M. E. , Pujol, B. & Berjano, R. (2008). Gender variation and transitions between sexual systems in

Pannell, J. R. & Korbecka, G. (2010). Mating‐system evolution: rise of the irresistible males. Current Biology 20, R482–R484. PubMed

Parkinson, S. E. , Gross, S. M. & Hollick, J. B. (2007). Maize sex determination and abaxial leaf fates are canalized by a factor that maintains repressed epigenetic states. Developmental Biology 308, 462–473. PubMed

Petry, W. K. , Soule, J. D. , Iler, A. M. , Chicas‐Mosier, A. , Inouye, D. W. , Miller, T. E. X. & Mooney, K. A. (2016). Sex‐specific responses to climate change in plants alter population sex ratio and performance. Science (New York, N.Y.) 353, 69–71. PubMed

Philippi, T. & Seger, J. (1989). Hedging one's evolutionary bets, revisited. Trends in Ecology & Evolution 4, 41–44. PubMed

Piferrer, F. (2021). Epigenetic mechanisms in sex determination and in the evolutionary transitions between sexual systems. Philosophical Transactions of the Royal Society B 376, 20200110. PubMed PMC

Pigliucci, M. & Murren, C. J. (2003). Perspective: genetic assimilation and a possible evolutionary paradox: can macroevolution sometimes be so fast as to pass us by? Evolution; International Journal of Organic Evolution 57, 1455–1464. PubMed

Pikaard, C. S. & Scheid, O. M. (2014). Epigenetic regulation in plants. Cold Spring Harbor Perspectives in Biology 6, a019315. PubMed PMC

Punja, Z. K. & Holmes, J. E. (2020). Hermaphroditism in Marijuana ( PubMed PMC

Putnins, M. & Androulakis, I. P. (2021). Self‐selection of evolutionary strategies: adaptive versus non‐adaptive forces. Heliyon 7, e06997. PubMed PMC

Rajon, E. , Desouhant, E. , Chevalier, M. , Débias, F. & Menu, F. (2014). The evolution of bet hedging in response to local ecological conditions. The American Naturalist 184, E1–E15. PubMed

Reed, T. E. , Robin, S. W. , Schindler, D. E. , Hard, J. J. & Kinnison, M. T. (2010). Phenotypic plasticity and population viability: the importance of environmental predictability. Proceedings. Biological sciences 277, 3391–3400. PubMed PMC

Renner, S. S. (2014). The relative and absolute frequencies of angiosperm sexual systems: Dioecy, monoecy, gynodioecy, and an updated online database. American Journal of Botany 101, 1588–1596. PubMed

Renner, S. S. , Beenken, L. , Grimm, G. W. , Kocyan, A. & Ricklefs, R. E. (2007). The evolution of dioecy, heterodichogamy, and labile sex expression in PubMed

Renner, S. S. & Müller, N. A. (2021). Plant sex chromosomes defy evolutionary models of expanding recombination suppression and genetic degeneration. Nature Plants 7, 392–402. PubMed

Renner, S. S. & Ricklefs, R. E. (1995). Dioecy and its correlates in the flowering plants. American Journal of Botany 82, 596–606.

Renner, S. S. & Won, H. (2001). Repeated evolution of dioecy from monoecy in Siparunaceae (Laurales). Systematic Biology 50, 700–712. PubMed

Richards, C. L. , Alonso, C. , Becker, C. , Bossdorf, O. , Bucher, E. , Colomé‐Tatché, M. , Durka, W. , Engelhardt, J. , Gaspar, B. , Gogol‐Döring, A. , Grosse, I. , van Gurp, T. P. , Heer, K. , Kronholm, I. , Lampei, C. , PubMed

Richards, C. L. , Verhoeven, K. J. F. & Bossdorf, O. (2012). Evolutionary significance of epigenetic variation. In Plant Genome Diversity Volume 1: Plant Genomes, their Residents, and their Evolutionary Dynamics (ed. Bossdorf O.), pp. 257–274. Springer‐Verlag, Vienna.

Richards, E. J. (2006). Inherited epigenetic variation — revisiting soft inheritance. Nature Reviews Genetics 7, 395–401. PubMed

Rieseberg, L. H. , Hanson, M. A. & Philbrick, C. T. (1992). Androdioecy is derived from dioecy in Datiscaceae: evidence from restriction site mapping of PCR‐amplified chloroplast DNA fragments. Systematic Botany 17, 324.

Ross, M. D. (1978). The evolution of gynodioecy and subdioecy. Evolution 32, 174–188. PubMed

Rottenberg, A. (1998). Sex ratio and gender stability in the dioecious plants of Israel. Botanical Journal of the Linnean Society 128, 137–148.

Rottenberg, A. (2000). Fertility of exceptional bisexual individuals in four dioecious plant species. Sexual Plant Reproduction 12, 219–221.

Rottenberg, A. (2007). Fertility and sexual structure in a polygamous willow population. Plant Systematics and Evolution 268, 257–260.

Ruffatto, D. M. , Zaya, D. N. & Molano‐Flores, B. (2015). Reproductive success of the gynodioecious

Sammarco, I. , Díez Rodríguez, B. , Galanti, D. , Nunn, A. , Becker, C. , Bossdorf, O. , Münzbergová, Z. & Latzel, V. (2024). DNA methylation in the wild: epigenetic transgenerational inheritance can mediate adaptation in clones of wild strawberry ( PubMed

Saumitou‐Laprade, P. , Vernet, P. , Vassiliadis, C. , Hoareau, Y. , de Magny, G. , Dommée, B. & Lepart, J. (2010). A self‐incompatibility system explains high male frequencies in an androdioecious plant. Science (New York, N.Y.) 327, 1648–1650. PubMed

Sauquet, H. , von Balthazar, M. , Magallón, S. , Doyle, J. A. , Endress, P. K. , Bailes, E. J. , Barroso de Morais, E. , Bull‐Hereñu, K. , Carrive, L. , Chartier, M. , Chomicki, G. , Coiro, M. , Cornette, R. , El Ottra, J. H. L. , Epicoco, C. , PubMed PMC

Saze, H. (2008). Epigenetic memory transmission through mitosis and meiosis in plants. Seminars in Cell & Developmental Biology 19, 527–536. PubMed

Schaefer, H. & Renner, S. S. (2010). A three‐genome phylogeny of PubMed

Scheiner, S. M. (2013). The genetics of phenotypic plasticity. XII. Temporal and spatial heterogeneity. Ecology and Evolution 3, 4596–4609. PubMed PMC

Scheiner, S. M. (2014). The genetics of phenotypic plasticity. XIII. Interactions with developmental instability. Ecology and Evolution 4, 1347–1360. PubMed PMC

Scheiner, S. M. & Holt, R. D. (2012). The genetics of phenotypic plasticity. X. Variation versus uncertainty. Ecology and Evolution 2, 751. PubMed PMC

Scutt, C. P. , Li, Y. , Robertson, S. E. , Willis, M. E. & Gilmartin, P. M. (1997). Sex determination in dioecious PubMed PMC

Seger, J. & Brockmann, H. J. (1987). What is bet‐hedging? In Oxford Surveys in Evolutionary Biology. Oxford University Press, UK.

Shea, M. M. , Dixon, P. M. & Sharitz, R. R. (1993). Size differences, sex ratio, and spatial distribution of male and female water tupelo,

Sinclair, J. P. , Kameyama, Y. , Shibata, A. & Kudo, G. (2016). Male‐biased hermaphrodites in a gynodioecious shrub, PubMed

Skof, S. , Cerenak, A. , Jakse, J. , Bohanec, B. & Javornik, B. (2012). Ploidy and sex expression in monoecious hop (

Spigler, R. B. & Ashman, T.‐L. (2012). Gynodioecy to dioecy: are we there yet? Annals of Botany 109, 531–543. PubMed PMC

Stettler, R. F. (1971). Variation in sex expression of black cottonwood and related hybrids. Silvae Genetica 20, 42–46.

Thiebaut, F. , Hemerly, A. S. & Ferreira, P. C. G. (2019). A role for epigenetic regulation in the adaptation and stress responses of non‐model plants. Frontiers in Plant Science 10, 246. PubMed PMC

Tonnabel, J. , David, P. & Pannell, J. R. (2017). Sex‐specific strategies of resource allocation in response to competition for light in a dioecious plant. Oecologia 185, 675–686. PubMed PMC

Torices, R. , Méndez, M. & Gómez, J. M. (2011). Where do monomorphic sexual systems fit in the evolution of dioecy? Insights from the largest family of angiosperms. New Phytologist 190, 234–248. PubMed

Uller, T. , English, S. & Pen, I. (2015). When is incomplete epigenetic resetting in germ cells favoured by natural selection? Proceedings of the Royal Society B: Biological Sciences 282, 20150682. PubMed PMC

Van Der Graaf, A. , Wardenaara, R. , Neumann, D. A. , Taudt, A. , Shaw, R. G. , Jansen, R. C. , Schmitz, R. J. , Colomé‐Tatché, M. & Johannes, F. (2015). Rate, spectrum, and evolutionary dynamics of spontaneous epimutations. Proceedings of the National Academy of Sciences of the United States of America 112, 6676–6681. PubMed PMC

Vandepitte, K. , Honnay, O. , de Meyer, T. , Jacquemyn, H. & Roldán‐Ruiz, I. (2010). Patterns of sex ratio variation and genetic diversity in the dioecious forest perennial

Varga, S. & Kytöviita, M. M. (2016). Light availability affects sex lability in a Gynodioecious plant. American Journal of Botany 103, 1928–1936. PubMed

Varga, S. & Soulsbury, C. D. (2020). Environmental stressors affect sex ratios in sexually dimorphic plant sexual systems. Plant Biology 22, 890–898. PubMed

Velanis, C. N. & Goodrich, J. (2017). Vernalization and epigenetic inheritance: a game of histones. Current Biology 27, R1324–R1326. PubMed

Venkatasamy, S. , Khittoo, G. & Keeley, S. (2007). Leaky dioecy in

Weller, S. G. & Sakai, A. K. (1991). The genetic basis of male sterility in

West, N. W. & Golenberg, E. M. (2018). Gender‐specific expression of GIBBERELLIC ACID INSENSITIVE is critical for unisexual organ initiation in dioecious PubMed

Willson, M. F. (1979). Sexual selection in plants. The American Naturalist 113, 777–790.

Wolf, D. E. & Takebayashi, N. (2004). Pollen limitation and the evolution of androdioecy from dioecy. The American Naturalist 163, 122–137. PubMed

Wood, D. P. , Holmberg, J. A. , Osborne, O. G. , Helmstetter, A. J. , Dunning, L. T. , Ellison, A. R. , Smith, R. J. , Lighten, J. & Papadopulos, A. S. T. (2023). Genetic assimilation of ancestral plasticity during parallel adaptation to zinc contamination in PubMed PMC

Xu, X. , Peng, G. , Wu, C. , Korpelainen, H. & Li, C. (2008). Drought inhibits photosynthetic capacity more in females than in males of PubMed

Yonemori, K. , Honsho, C. , Kanzaki, S. , Ino, H. , Ikegami, A. , Kitajima, A. , Sugiura, A. & Parfitt, D. E. (2008). Sequence analyses of the ITS regions and the

Zhang, D. (2000). Resource allocation and the evolution of self‐fertilization in plants. The American Naturalist 155, 187–199. PubMed

Zhang, H. , Lang, Z. & Zhu, J. K. (2018). Dynamics and function of DNA methylation in plants. Nature Reviews Molecular Cell Biology 19, 489–506. PubMed

Zhang, H. , Zhang, R. , Yang, X. , Gu, K.‐J. , Chen, W. , Chang, Y. , Xu, Q. , Liu, Q. , Qin, Y. , Hong, X. , Yin Seim, I. , Lin, H.‐Y. , Li, W.‐H. , Tian, J. , DOI

Zhang, L. B. , Simmons, M. P. , Kocyan, A. & Renner, S. S. (2006). Phylogeny of the Cucurbitales based on DNA sequences of nine loci from three genomes: implications for morphological and sexual system evolution. Molecular Phylogenetics and Evolution 39, 305–322. PubMed

Zhang, Y. , Fischer, M. , Colot, V. & Bossdorf, O. (2013). Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytologist 197, 314–322. PubMed

Zhou, P. , Zhang, X. , Fatima, M. , Ma, X. , Fang, H. , Yan, H. & Ming, R. (2020). DNA methylome and transcriptome landscapes revealed differential characteristics of dioecious flowers in papaya. Horticulture Research 7, 1–15. PubMed PMC

Zimmerman, J. K. (1991). Ecological correlates of labile sex expression in the orchid