Temporal dynamics of sexual dimorphism in a dioecious species.

BACKGROUND AND AIMS: Sexual dimorphism for floral traits is common in dioecious plant species. Beyond its significance for understanding how selection acts on plant traits through male vs. female reproductive function, sexual dimorphism has also been proposed as a possible risky characteristic for insect-pollinated plants, as it could drive pollinators to forage mostly on male plants. However, even though most flowering plant species spread their flowering across several weeks or months, the temporal variation of floral phenotypes and sexual dimorphism have rarely been investigated. METHODS: We performed a survey of male and female plants from the dioecious generalist-pollinated Silene dioica (Caryophyllaceae) in a common garden experiment, over two consecutive flowering seasons. Flower number and floral size were measured each week, as well as pollen quantity and viability in male plants. KEY RESULTS: Sexual dimorphism was found for all investigated floral traits, with males showing an overall higher investment in flower production and flower size. Males and females showed a similar temporal decline in flower size. The temporal dynamics of daily flower number differed between sexes, with males showing a peak in the middle of their flowering season, whereas flower production by females was quite stable over time. At the scale of the experimental population, both individual and floral sex ratios appeared to vary across the flowering season. Moreover, because the onset of flowering varied among plants, the magnitude of sexual dimorphism in floral size also fluctuated strongly through time. CONCLUSIONS: Capturing male/female differences with only one temporal measurement per population may not be informative. This opens stimulating questions about how pollinator behaviour and resulting pollination efficiency may vary across the flowering season.

Disentangling the causes of heterogeneity in male fecundity in gynodioecious Beta vulgaris ssp. maritima.

Variation among individuals in reproductive success is advocated as a major process driving evolution of sexual polymorphisms in plants, such as gynodioecy where females and hermaphrodites coexist. In gynodioecious Beta vulgaris ssp. maritima, sex determination involves cytoplasmic male sterility (CMS) genes and nuclear restorers of male fertility. Both restored CMS and non-CMS hermaphrodites co-occur. Genotype-specific differences in male fitness are theoretically expected to explain the maintenance of cytonuclear polymorphism. Using genotypic information on seedlings and flowering plants within two metapopulations, we investigated whether male fecundity was influenced by ecological, phenotypic and genetic factors, while taking into account the shape and scale of pollen dispersal. Along with spatially restricted pollen flow, we showed that male fecundity was affected by flowering synchrony, investment in reproduction, pollen production and cytoplasmic identity of potential fathers. Siring success of non-CMS hermaphrodites was higher than that of restored CMS hermaphrodites. However, the magnitude of the difference in fecundity depended on the likelihood of carrying restorer alleles for non-CMS hermaphrodites. Our results suggest the occurrence of a cost of silent restorers, a condition supported by scarce empirical evidence, but theoretically required to maintain a stable sexual polymorphism in gynodioecious species.

Gynodioecy in structured populations: understanding fine-scale sex ratio variation in Beta vulgaris ssp. maritima.

Natural selection, random processes and gene flow are known to generate sex ratio variations among sexually polymorphic plant populations. In gynodioecious species, in which hermaphrodites and females coexist, the relative effect of these processes on the maintenance of sex polymorphism is still up for debate. The aim of this study was to document sex ratio and cytonuclear genetic variation at a very local scale in wind-pollinated gynodioecious Beta vulgaris ssp. maritima and attempt to elucidate which processes explained the observed variation. The study sites were characterized by geographically distinct patches of individuals and appeared to be dynamic entities, with recurrent establishment of distinct haplotypes through independent founder events. Along with substantial variation in sex ratio and unexpectedly low gene flow within study sites, our results showed a high genetic differentiation among a mosaic of genetically distinct demes, with isolation by distance or abrupt genetic discontinuities taking place within a few tens of metres. Overall, random founder events with restricted gene flow could be primary determinants of sex structure, by promoting the clumping of sex-determining genes. Such high levels of sex structure provide a landscape for differential selection acting on sex-determining genes, which could modify the conditions of maintenance of gynodioecy in structured populations.

Sex-specific fitness variation in gynodioecious Beta vulgaris ssp. maritima: do empirical observations fit theoretical predictions?

In gynodioecious species, in which hermaphroditic and female plants co-occur, the maintenance of sexual polymorphism relies on the genetic determination of sex and on the relative fitness of the different phenotypes. Flower production, components of male fitness (pollen quantity and pollen quality) and female fitness (fruit and seed set) were measured in gynodioecious Beta vulgaris spp. maritima, in which sex is determined by interactions between cytoplasmic male sterility (CMS) genes and nuclear restorers of male fertility. The results suggested that (i) female had a marginal advantage over hermaphrodites in terms of flower production only, (ii) restored CMS hermaphrodites (carrying both CMS genes and nuclear restorers) suffered a slight decrease in fruit production compared to non-CMS hermaphrodites and (iii) restored CMS hermaphrodites were poor pollen producers compared to non-CMS hermaphrodites, probably as a consequence of complex determination of restoration. These observations potentially have important consequences for the conditions of maintenance of sexual polymorphism in B. vulgaris and are discussed in the light of existing theory on evolutionary dynamics of gynodioecy.

Pollen limitation of female reproductive success at fine spatial scale in a gynodioecious and wind-pollinated species, Beta vulgaris ssp. maritima.

In sexually polymorphic plants, the spatial distribution of sexes is usually not random. Local variation in phenotype frequencies is expected to affect individual fitness of the different phenotypes. For gynodioecious species, with co-occurrence of hermaphrodites and females, if sexual phenotypes are structured in space and pollen flow is spatially restricted, local pollen availability should vary among patches. Female fitness may thus be low when hermaphrodites are locally rare. To test this hypothesis, we analysed how the reproductive output of females varied among patches within two natural study sites of the gynodioecious wind-pollinated Beta vulgaris ssp. maritima. Plants growing in female-biased areas and experiencing pollen limitation were found to have low fruit and seed sets but did not reallocate resources towards better offspring. Our results show that fine-scale processes influence individual fitness and the evolution of sex ratio in sexually polymorphic plants.

Variation in pollen production and pollen viability in natural populations of gynodioecious Beta vulgaris ssp. maritima: evidence for a cost of restoration of male function?

Gynodioecious species are defined by the co-occurrence of two clearly separated categories of plants: females and hermaphrodites. The hermaphroditic category may, however, not be homogeneous, as male fitness may vary among hermaphrodites as a result of many biological factors. In this study, we analysed estimates of pollen quantity and viability in the gynodioecious Beta vulgaris ssp. maritima, comparing hermaphrodites bearing a male-fertile cytotype and hermaphrodites bearing cytoplasmic male sterility (CMS) genes, which are counteracted by nuclear restoration factors. We show that: (i) pollen quantity continuously varies among restored hermaphrodites, suggesting a complex genetic determination of nuclear restoration; (ii) pollen viability was lower in restored (CMS) hermaphrodites than in non-CMS hermaphrodites, probably because of incomplete restoration in some of these plants; and (iii) pollen quantity and viability also varied among hermaphrodites with male-fertile cytotypes, possibly a result of a silent cost of restoration. Finally, we discuss the consequences of these results for pollen flow and the dynamics of gynodioecy.