Causes and consequences of sex ratio variation in plants. A commentary on: ‘Life history characteristics and historical factors are important to explain regional variation in reproductive traits and genetic diversity in perennial mosses’

Abstract

This article comments on:

Irene Bisang, Johan Ehrlén, and Lars Hedenäs. Life-history characteristics and historical factors are important to explain regional variation in reproductive traits and genetic diversity in perennial mosses, Annals of Botany, Volume 132, Issue 1, 1 July 2023, Pages 29–42, https://doi.org/10.1093/aob/mcad045

Separate sexes (females and males) have evolved independently across anisogamous lineages, with multiple origins of separate sexes in animals (Sasson and Ryan, 2017) and land plants (Renner and Müller, 2021). Indeed, although land plants, and the flowering plants in particular, are predominantly hermaphroditic, separate sexes have evolved more often within this group than in any other, with hundreds of origins of dioecy (i.e. populations with separate female and male sporophyte plants) in flowering plants (Renner, 2014) and dozens of origins of dioicy (i.e. populations with separate female and male gametophyte plants) in mosses (McDaniel et al., 2013). Evolutionary transitions from hermaphroditism to separate sexes are associated with, and may be driven by, the enforcement of outcrossing (Charlesworth and Charlesworth, 1978), and in large, well-mixed populations of outcrossing individuals balanced ratios of females and males are generally expected (Fisher, 1930). Yet strongly biased sex ratios can be found across groups with separate sexes (Field et al., 2013; Schacht et al., 2022), including mosses, a recent example of which is highlighted in a new study in this issue of Annals of Botany by Bisang et al. (2023), which found pervasive female bias in two species of wetland mosses, Drepanocladus trifarius and D. turgescens, across a range of ecological conditions and a large geographical area. Pervasive female-biased sex ratios, a widespread feature of dioicous mosses (de Jong et al., 2018), beg for an explanation, and a consideration of their consequences.

A variety of ecological and evolutionary processes can drive female-biased sex ratios in plants. A full discussion of the causes of biased sex ratios in plants is beyond the scope of this comment and have recently been reviewed (de Jong et al., 2018). Briefly, differences in the growth and/or survival of female plants can yield female-biased sex ratios even if the offspring sex ratio is balanced. Such differences in growth or survival between the sexes might arise from differences in their respective allocations of resources to reproduction (Obeso, 2002). These differences might also be exacerbated by nuclear–cytoplasmic interactions that favour females. Cytoplasmic genomes are typically maternally inherited in plants and so whenever they are transmitted to male offspring they are at an evolutionary dead end (Fig. 1). As a result, there is no selection on these genomic elements to function well in males (de Jong et al., 2018). Indeed, if males compete with female siblings during establishment, as could occur whenever spores (or seeds) are co-dispersed over short distances, cytoplasmic genomes have enhanced transmission if they suppress the growth of males (Cosmides and Tooby, 1981).

Fig. 1.

All land plants have life cycles that alternate between two multicellular phases: a haploid gamete-producing phase, and a diploid spore-producing phase (middle, brown circle in each life-cycle diagram). Sexual expression: For dioicous mosses, sex is expressed in the haploid phase and therefore is determined by the segregation of sex chromosomes following meiosis. For dioecious angiosperms, sex is expressed in the diploid phase and is therefore determined following syngamy. Sexual selection: In mosses sexual selection can only occur during the brief part of the life cycle between sperm release and fertilization. By contrast, in angiosperms sexual selection can extend across both phases of the life cycle, affecting sporophytes (e.g. competition among plants for the attraction of pollinators) and gametophytes (e.g. when pollen grains from different plants compete to fertilize an ovule). Nuclear–cytoplasmic interactions: Cytoplasmic genomes are typically maternally inherited, as depicted in the central green circle in each life-cycle diagram, with subscripts denoting whether cytoplasmic genomes (C) occur in female or male plants. Because of biased transmission, selection that maintains proper function of cytoplasmic genomes in males is weaker than in females, with potential consequences for the growth and survival of males. Representative images are shown below each life-cycle diagram: a dioicous moss (Polytrichum juniperinum) with intermingled male (plants with red tips) and female moss plants (with leafy green tips, some of which bear immature sporophytes); and a dioecious angiosperm (Sagittaria latifolia) with a flower from a female plant on the right and a flower from a male plant on the left. (Photographs: Marcel Dorken.).

Whatever the cause, females often outperform males and this could explain female-biased sex ratios, particularly for herbaceous angiosperms with abiotic pollen and seed dispersal (Obeso, 2002; Field et al., 2013). Reproductive costs for mosses are less well studied than for angiosperms and the few results are contradictory; differences in survival or reproductive effort between the sexes can help explain female-biased sex ratios in one species (Ekwealor et al., 2017) but not in another (Bisang et al., 2006).

The study by Bisang et al. (2023) brings the causes of female-biased sex ratios into sharper focus. They studied two species of mosses that differ in terms of their frequency of sexual reproduction across geographical regions, with regular sporophyte production in southern Scandinavia but very rare or absent sporophyte production in northern Scandinavia. They examined patterns of genetic variation across regions for both species and measured the sex ratios of plants within regions using a combination of direct observation and the use of molecular-genetic techniques to identify the sex of plants without observable reproductive tissues. A clear takeaway from their study is that female-biased sex ratios largely characterize both species, regardless of the frequency of sexual reproduction across regions. As noted by Bisang et al. (2023), these findings, combined with the observation from a related species that spore sex ratios are unbiased (Bisang et al., 2017), implicate processes operating after meiosis (i.e. the lower left quadrant of the circles in Fig. 1) in driving female-biased sex ratios across regions. For the two species studied by Bisang et al. (2023), differential growth – and the vegetative expansion of females via clonal growth in particular – was argued to be a major driver of female-biased sex ratios. This study therefore brings us one step closer to understanding the causes of female-biased sex ratios in mosses.

However, the story likely does not end there. Female-biased sex ratios are expected to have important consequences for patterns of mate acquisition and therefore fitness through sexual reproduction. Typically, anisogamy (i.e. the production of many small spermatozoa versus relatively few large eggs) results in sexual selection in males (Bateman, 1948; Lehtonen, 2022). However, severe mate limitation in female-biased populations combined with inefficient sperm transfer is expected to reduce the magnitude of sexual selection in males, and could even result in stronger sexual selection in females than in males (Lehtonen, 2022). Indeed, there is evidence that female mosses are the more ‘attractive’ sex for arthropods that can enact sperm transfer (Rosenstiel et al., 2012) in a way that might be expected if sexual selection were driven by variation in female mating success. The intriguing possibility that sexual selection might operate in a much different manner in mosses than it does in other groups indicates that there is still much to be learned about fundamental ecological and evolutionary processes from this group of plants.