Low siring success of females with an acquired male function illustrates the legacy of sexual dimorphism in constraining the breakdown of dioecy

Abstract

Dioecy has often broken down in flowering plants, yielding functional hermaphroditism. We reasoned that evolutionary transitions from dioecy to functional hermaphroditism must overcome an inertia of sexual dimorphism, because modified males or females will express the opposite sexual function for which their phenotypes have been optimised. We tested this prediction by assessing the siring success of monoecious individuals of the plant Mercurialis annua with an acquired male function but that are phenotypically still female‐like. We found that pollen dispersed by female‐like monoecious individuals was ~ 1/3 poorer at siring outcrossed offspring than pollen from monoecious individuals with an alternative male‐like inflorescence. We conclude that whereas dioecy might evolve from functional hermaphroditism by conferring upon individuals certain benefits of sexual specialisation, reversion from a strategy of separate sexes to one of combined sexes must overcome constraints imposed by the advantages of sexual dimorphism. The breakdown of dioecy must therefore often be limited to situations in which outcrossing cannot be maintained and where selection favours a capacity for inbreeding by functional hermaphrodites.

A new biological species in the Mercurialis annua polyploid complex: functional divergence in inflorescence morphology and hybrid sterility

“…We also found that F 1 progeny from crosses between the two phenotypes were substantially larger than the non-hybrid progeny. This result may point to heterosis or hybrid vigour, consistent with both parental lineages being inbred (Semel et al , 2006; Hochholdinger and Hoecker, 2007; Wang et al , 2015), and as suggested by the low genetic diversity observed in P+ populations (Santos del Blanco et al , 2019), but also in many P– populations (Obbard et al , 2006b; Pujol et al , 2009, 2010). Alternatively, it is possible that some of the vigour of hybrid individuals is attributable to trade-offs resulting from their lower reproductive effort.…”

“…The pedunculate phenotype (labelled ‘P+’), although broadly sympatric with the P– phenotype along the Spanish Mediterranean coastal areas and occupying very similar habitats, occurs rarely in mixed populations with the P– phenotype. A previous study found that the P+ phenotype is substantially better at dispersing pollen than the P– phenotype and enjoys much greater siring success in experimental populations, without any obvious phenotypic advantage to the P– phenotype (Santos del Blanco et al , 2019). One might expect such a superior strategy for pollen dispersal to spread quickly throughout the species range, particularly as it does not appear very costly in terms of other fitness components (Buggs and Pannell, 2006).…”

“…However, we recently documented the existence in some populations of apparently hexaploid monoecious individuals of M. annua that, like males, hold virtually all their male flowers on erect peduncles rather than in the sub-sessile axillary inflorescences that are more typical of hexaploid M. annua , whereas female flowers are found on short pedicels in the leaf axils or, occasionally, on the erect peduncles along with male flowers (Fig. 1C; Santos del Blanco et al , 2019). The non-pedunculate form of hexaploid monoecious M. annua (which we here label ‘P–‘) occurs widely around the Iberian Peninsula in disturbed ruderal habitats, often together with males in androdioecious populations (Pannell, 1997 a ; Buggs and Pannell, 2006; Obbard et al , 2006a).…”

“…The M. annua species complex displays remarkable variation in its sexual systems, including dioecy, monoecy and the rare sexual system androdioecy, where males co-occur with monoecious hermaphrodites (Pannell, 1997 a , 2008; Obbard et al , 2006a,b; Russell and Pannell, 2015). Against this background, variation in inflorescence architecture among monoecious populations allows valuable comparisons among divergent inflorescence strategies for outcross siring success (Santos del Blanco et al , 2019), but it also prompts questions concerning its origins.…”

Enhanced leaky sex expression is an adaptive plastic response to pollen limitation in the dioecious plantMercurialis annua

“…However, whereas the absence of males from a population in the dioecious diploid lineage would be reliably perceived by females in terms of an absence of pollen on their stigmas, or low rates of fertilization of their ovules, monoecious 'females' of the polyploid lineage would receive pollen from other monoecious individuals even when males are absent, which occurs frequently (Pannell et al 2014). Thus, although polyploid monoecious individuals would likely benefit from suppressing the production of male flowers when males are present, because males are so much better at dispersing pollen and outcross siring (Eppley and Pannell 2007a;Santos del Blanco et al 2018), this strategy might be inaccessible to them for want of a suitably reliable signal.…”