Sexual conflict in protandrous flowers and the evolution of gynodioecy*

Abstract

Sexual interference between male and female function in hermaphrodite plants is reduced by protandry. In environments with insufficient pollinator service, prolongation of male function owing to limited pollen removal could restrict the duration of female function and lower seed production. We provide evidence that this form of sexual conflict has played a role in the spread of females in gynodioecious populations of Cyananthus delavayi in the pollen‐limited environments in which this subalpine species occurs. Using field experiments involving artificial pollen removal from the strongly protandrous flowers of hermaphrodites, we demonstrated a trade‐off between male‐ and female‐phase duration with no influence on overall floral longevity. Pollen removal at the beginning of anthesis resulted in hermaphrodite seed production matching that of females. In contrast, restricted pollen removal increased the duration of male function at the expense of female function lowering maternal fertility compared to females. This pattern was evident in five populations with females experiencing a twofold average seed fertility advantage compared to hermaphrodites. Gynodioecy often appears to evolve from protandrous ancestors and pollen limitation is widespread in flowering plants suggesting that sexual conflict may play an unappreciated role in the evolution of this form of sexual dimorphism.

Digest: Sexual conflict as a novel hypothesis for the evolution of gynodioecy*

“…1), Wang et al. (2020) confirm that a sexual conflict over the duration of male and female phases may promote the evolution of gynodioecy. The artificial removal of pollen from anthers in hermaphroditic flowers shortened the male phase at the benefit of the female phase, which fostered seed production up to the level of female plant's fertility.…”

“…Many hermaphroditic plants have evolved a withinflower temporal separation of the maturity of anthers and pistils, named dichogamy, attributed to self-fertilization avoidance and reduction of sexual interference (Lloyd and Webb 1986). Wang et al (2020) propose that a failure in pollen removal due to pollinator scarcity may trigger a plastic prolongation of the male phase at the expense of the duration of the female phase ( Fig. 1).…”

The demographic costs of sexually antagonistic selection in partially selfing populations

“…Yet, other factors, such as genetic linkage to other SA loci or a sex-determining region (Jordan and Charlesworth, 2012; Olito, 2017; Olito and Connallon, 2019; Otto et al, 2011), antagonism between viability and fecundity selection (Glémin, 2021), or spatial heterogeneity and complexity of the life-cycle can expand the parameter space for SA polymorphism (Connallon et al, 2019; Glémin, 2021; Olito et al, 2018). Overall, both theoretical predictions and current empirical data suggest that there is ample scope for SA trade-offs and the maintenance of SA polymorphisms in both dioecious and hermaphrodite populations (Abbott, 2011; Wang et al, 2020), although identifying specific SA loci from genome sequence data remains challenging (Ruzicka et al, 2020).…”

“…That is, each individual’s genotype determines both the number of ovules produced and the paternal mating success, broadly defined. For hermaphroditic flowering plants, for example, paternal mating success could reflect pollen production, export efficiency, pollen-tube germination and growth rates, among other things (Harder et al, 2016; Lloyd and Webb, 1986; Wang et al, 2020). Note, however, that by modeling paternal relative mating success rather than pollen/sperm production, we implicitly assume female demographic dominance (i.e., production/transport of male gametes does not limit ovule fertilization and hence population growth), a point we return to in the Discussion.…”

Testing a behavioral model for the maintenance of androdioecy as a result of sexual conflict in the clam shrimp Eulimnadia dahli

“…Breeding systems other than dioecy are also susceptible to conflicts of interest between sexual types. Sexual conflicts have been noted in androdioecious (male and hermaphrodite) systems (Benvenuto & Weeks, 2011, 2012Chasnov, 2010), gynodioecious (female and hermaphrodite) systems (Wang et al, 2021), and even in simultaneously hermaphroditic systems (Anthes & Michiels, 2007;Bedhomme et al, 2009).…”