Female heterogamety (ZW systems) in 22% of flowering plants with sex chromosomes: Theoretical expectations and correlates

Genetic sex determination usually involves males and females that differ in their gametes, with one sex producing two types of gametes, the other a single type. When females produce two types, this is called female heterogamety and the sex chromosomes are denoted Z and W, while the reverse is male heterogamety, with the sex chromosomes denoted X and Y (Muller, 1915). Sex chromosomes can only occur in separate-sexed species, but inferring which sex is heterogametic can be difficult (Correns, 1917; Westergaard, 1958). Here I present a compilation of plant species with ZW sex chromosomes and briefly relate findings from plants to those from animals and to theoretical expectations about genetic degeneration and ecological correlates of female heterogamety. This seems relevant because theoretical studies are handicapped by the assumption that ZW sex chromosome systems are extremely rare (e.g., Marais and Lemaitre, 2022; Lesaffre et al., 2024). In land plants, female heterogamety is only known from flowering plants. This is surprising because almost half of all gymnosperms are dioecious (all 337 species of cycads, Ginkgo biloba, all 70 species of Gnetales, and a few conifers) and likely have sex chromosomes. In bryophytes, male or female heterogamety is not possible because the sexual generation is haploid, and unisexual plants thus have either a U or a V chromosome, but never both. Ferns and lycophytes have few sexually specialized species (Renner, 2014). Female heterogamety was discovered in chickens and a magpie moth (Muller, 1915), and today we know that this type of sex determination characterizes most birds (10,000 species), butterflies and moths (perhaps 180,000 species), snakes (perhaps 4000 species), and many fish and amphibians. Some fish, such as Xiphophorus maculatus, have strains in which the females are the heterogametic sex and others in which the males are heterogametic (Kallman, 1965). Frog species also can have W, Z, and Y sex chromosomes in different populations (e.g., Ezaz et al., 2006; Furman et al., 2020). The first plant ZW systems were inferred at the same time as those in animals, using experimental interspecific crossings and resulting sex ratios, not microscopy. These first experiments focused on Fragaria chiloensis and F. virginiana (Muller, 1915 interpreting experiments by Richardson, 1914). My compilation (Table 1) updates a database of green plants with sex chromosomes that includes 124 angiosperms with male heterogamety and 33 with female heterogamety (Garcia et al., 2023). These lists of ZW species differ because of corrections and additions, which are coming rapidly because of genomic research. How many of the approximately 15,600 dioecious angiosperms (Renner, 2014) may have XY or ZW systems could be extrapolated if the 157 so-far known species with sex chromosomes were a random sample. This seems unlikely, however, because dioecy is concentrated among tropical tree families, while research has concentrated on Northern Hemisphere herbs and shrubs. In some genera, such as Populus, Salix, and Silene, both XY and ZW systems occur in closely related species although not in populations of the same species (Balounova et al., 2019; Li et al., 2022; Wang et al., 2024), and this is another reason why extrapolation may be risky. Nevertheless, as of this writing, 34 species in 14 genera (Table 1), that is, 22%, of 157 flowering plants known to have sex chromosomes have ZW systems. 2n = 26 Homomorphic Molecular cytogenetics (FISH); molecular linkage maps from offspring n = 52 Homomorphic n = c. 130 Homomorphic n = 52 Homomorphic n = c. 76, I04, 130 Homomorphic 2n = 24 Homomorphic 2n = 24 Homomorphic 2n = 24 Homomorphic 2n = 20 Heteromorphic 2n = 20 ? 2n = 34 Homomorphic 2n = 16 Homomorphic 2n = 44 Heteromorphic 2n = 14, 28, 42 Homomorphic 2n = 56 Homomorphic 2n = 42 Heteromorphic 2n = 56 Homomorphic 2n = 56 Homomorphic 2n = 42 Homomorphic 2n = 38 Homomorphic 2n = 38 Homomorphic 2n = 38 Homomorphic 2n = 38 Homomorphic 2n = 38 Homomorphic 2n = 38 Homomorphic 2n = 38, 76 Homomorphic ZZZW/ZZZZ 2n = 38 Homomorphic 2n = 38 Homomorphic 2n = 38 Homomorphic 2n = 38 Homomorphic 2n = 28 Homomorphic In XY species with a 1:1 sex ratio, the X chromosome is present in females two-thirds of the time and in males one-third of the time. In ZW species, the situation is the opposite. However, the two systems are by no means mirror images of each other (Figure 1). Instead, the speed of degeneration of Y chromosomes is expected to exceed that of W chromosomes as long as males have a greater variance in reproductive success than females (all females get to reproduce, but not all males do) and therefore a smaller effective population size, which might cause Y chromosomes to suffer more from genetic drift. We know little about the size of such reproductive skews in plants, however, and there is so far little evidence of genetic decay in their sex chromosomes (Renner and Müller, 2021). A second difference between XY and ZW systems arises from sex-determining mechanisms being inextricably linked to sex ratios (Muller, 1915; Correns, 1917, 1922, 1928; Bulmer and Bull, 1982): Whenever chromosomes determine sex, the primary sex ratio is controlled by the segregation of these chromosomes in the heterogametic sex. Because of this link, any deviation of the sex ratio from the optimum generates selection on sex-determining genes (Bulmer and Bull, 1982). Carl Correns (1917, 1922) was the first to use controlled pollination experiments in Silene latifolia (under the synonym Melandrium album) and Rumex acetosa to test the hypothesis that in males with two types of gametes, pollen tubes carrying these gametes might grow at different speeds, which should influence the primary sex ratio. When he applied abundant pollen grains to a stigma, offspring sex ratios were strongly female biased, while when he applied few pollen grains, he obtained balanced offspring sex ratios, which he attributed to inferior competitive abilities of one kind of gamete compared to the other. He called the phenomenon “certation,” and this type of experiment was long used to infer male or female heterogamety (Correns, 1917, 1922; Westergaard, 1958). Certation has been supported in other species (Beaudry et al., 2020) and presents a clear difference in the potential for gametophytic selection on pollen tube growth between XY and ZW systems. The origin of ZW chromosomes is perhaps best understood in Fragaria, where a female-specific region of DNA is associated with sex and has repeatedly changed its genomic location, each time increasing the size of the hemizygous female-specific sequence on the W sex chromosome (Tennessen et al., 2018). Plant sex regions can thus ‘jump’, locking new genes into linkage with sex. Switches between ZW and XY systems are known from genomic studies in Salix and Populus. An example is S. babylonica, a hybrid species that has a ZW sex chromosome system with a sex-determining region on Chrom15, likely by an ancestral Y chromosome becoming the Z chromosome of the hybrid, while the ancestral X became the W chromosome (Wang et al., 2024). In Populus sect. Populus, an XY system of sex determination, which is found in P. tremula and P. tremuloides, likely re-evolved from the ZW system present in P. alba, P. adenopoda, and P. qiongdaoensis (Kim et al., 2021). Evolutionary transitions have also been inferred in Silene section Otites, albeit not yet using phased chromosome-level genomes (Balounova et al., 2019). Given that at least 34 flowering plants have ZW sex chromosomes (Table 1), three proposed hypotheses about ZW systems in principle might be tested. First, data from animals suggest that the heterogametic sex has a shorter life span than the homogametic sex (Marais and Lemaitre, 2022). For example, in XY systems, males should express deleterious mutations on their single X chromosome (the so-called toxic X). The expectation of a reduced lifespan in the heterogametic sex has been tested for plants, but the study lacked statistical power because of the small number of ZW systems included, namely eight ZW species of which some remain doubtful (Buchloe dactyloides, Distichlis spicata, Simarouba glauca). With the new compilation, which includes three ZW species with heteromorphic sex chromosomes (Table 1), the hypothesis might be retested. Second, Lessafre et al. (2024) suggested that XY systems are more likely to evolve when dioecy is a mechanism of inbreeding avoidance, while ZW systems are more likely to evolve when inbreeding depression is not a key factor in the evolution of dioecy and sex chromosomes. Testing this hypothesis requires finding suitable sets of XY and ZW systems with population-genetic data on inbreeding, although this will be difficult because of great phylogenetic distances among potential study species (Table 1). Third, the expected increased efficacy of selection on pollen tubes growing through stylar tissue in XY systems, in which there is an X-carrying and a Y-carrying pollen tube compared to ZW systems, in which both tubes carry a Z chromosome (Correns, 1917, 1922; Westergaard, 1958; Beaudry et al., 2020; Figure 1), might be tested by comparing ZW and XY species with heteromorphic sex chromosomes. Models and theories are useful, but rely heavily on simplifying assumptions, especially concerning the genetics of sex determination. Because we are only starting to understand sex determination pathways in plants, the frequencies of the three sex chromosome systems known in land plants (XY, ZW, and UV) will change, and according to what we will find, models may or may not apply. I am grateful to Jos Käfer, an anonymous reviewer, Pamela Diggle, Niels Müller, Bohuslav Janousek, Deborah Charlesworth, and Aaron Liston for their comments on various versions of this manuscript. 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