Gynodioecy to dioecy: are we there yet?

Background

The ‘gynodioecy–dioecy pathway’ is considered to be one of the most important evolutionary routes from hermaphroditism to separate sexes (dioecy). Despite a large accumulation of evidence for female seed fertility advantages in gynodioecious species (females and hermaphrodites coexist) in support of the first step in the gynodioecy–dioecy pathway, we still have very little evidence for the second step, i.e. the transition from gynodioecy to dioecy.

Scope

We review the literature to evaluate whether basic predictions by theory are supported. To establish whether females'' seed fertility advantage and frequencies are sufficient to favour the invasion of males, we review these for species along the gynodioecy–dioecy pathway published in the last 5 years. We then review the empirical evidence for predictions deriving from the second step, i.e. hermaphrodites'' male fertility increases with female frequency, selection favours greater male fertility in hermaphrodites in gynodioecious species, and, where males and hermaphrodites coexist with females (subdioecy), males have greater male fertility than hermaphrodites. We review how genetic control and certain ecological features (pollen limitation, selfing, plasticity in sex expression and antagonists) influence the trajectory of a population along the gynodioecy–dioecy pathway.

Conclusions

Females tend to have greater seed fertility advantages over hermaphrodites where the two coexist, and this advantage is positively correlated with female frequency across species, as predicted by theory. A limited number of studies in subdioecious species have demonstrated that males have an advantage over hermaphrodites, as also predicted by theory. However, less evidence exists for phenotypic selection to increase male traits of hermaphrodites or for increasing male function of hermaphrodites in populations with high female frequency. A few key case studies underline the importance of examining multiple components of male fertility and the roles of pollen limitation, selfing and plasticity, when evaluating advantages. We conclude that we do not yet have a full understanding of the transition from gynodioecy to dioecy.     

Seedling performance in a trioecious cactus,Pachycereus pringlei: Effects of maternity and paternity

We studied seed germination and the growth and survivorship of seedlings of females and hermaphrodites ofPachycereus pringlei (cardon), a Mexican columnar cactus whose geographically variable breeding system includes trioecy and gynodioecy. Results of a two-year field experiment conducted near Bahia Kino, Sonora, Mexico and a ten-month laboratory experiment were similar and did not support the hypothesis that seedlings of females outperform those of hermaphrodites. In the field, percent seed germination and 2-yr seedling survivorship averaged 66% and 95%, respectively and did not differ among six treatment classes. Seedlings of hermaphrodites generally were larger than those of females at the end of both experiments. Selfed seedlings of hermaphrodites did not grow more slowly than outcrossed seedlings of hermaphrodites or females. Hermaphrodite seedlings performed best when pollinated with hermaphrodite pollen; female seedlings performed best with male pollen. We conclude that superior seedling performance cannot explain why females are able to coexist with hermaphrodites in populations of this cactus. Instead, we postulate that greater annual seed production, which averaged 1.6 times higher in females than in hermaphrodites in two years, may be sufficient to allow females to co-occur with hermaphrodites in this large, longlived plant, especially if sex determination involves cytoplasmic-nuclear inheritance.     

Environmental stressors affect sex ratios in sexually dimorphic plant sexual systems

• Revealing the environmental pressures determining the frequency of females amongst populations of sexually dimorphic plants is a key research question. Analyses of sex ratio variation have been mainly done in dioecious plants, which misses key plant sexual systems that might represent intermediate stages in the evolution of dioecy from hermaphroditism.
• We investigated female frequency across populations of sexually dimorphic plant species in relation to environmental stressors (temperature, precipitation), totaling 342 species, 2011 populations, representing 40 orders and three different sexual systems (dioecy, gynodioecy and subdioecy). We also included the biome where the population was located to test how female frequency may vary more broadly with climate conditions.
• After correcting for phylogeny, our results for gynodioecious systems showed a positive relationship between female frequency and increased environmental stress, with the main effects being temperature‐related. Subdioecious systems also showed strong positive relationships with temperature, and positive and negative relationships related to precipitation, while no significant effects on sex ratio in dioecious plants were detected.
• Combined, we show that female frequencies in an intermediate sexual system on the pathway from hermaphroditism to dioecy respond strongly to environmental stressors and have different selective agents driving female frequency.

     

'Inconstant males' and the maintenance of labile sex expression in subdioecious plants

* Here, we evaluate the role of pollen limitation and selfing in the maintenance of labile sex expression in subdioecious plant species. * We used a literature survey to explore which factors correlated with a significant occurrence of hermaphrodites in dioecious species. We developed models to explore the selective maintenance of labile sex expression. The models had similar ecological assumptions but differed in the genetic basis of sex lability. * We found that a significant frequency of hermaphrodites was associated with animal pollination, and that hermaphrodites were 'inconstant' males with perfect flowers, suggesting evolution through the gynodioecious pathway. Models showed that a modifier converting pure males into inconstant males could be maintained under a wide range of reduction in both male and female fitness. Pollen limitation and self-fertilization facilitated invasion of the modifier. Depending on the genetics of sex determination, we found pure dioecy, stable subdioecy (trioecy), and situations where inconstant males coexisted with either pure females or pure males. Under selfing and pollen limitation, certain conditions selected for inconstant males which will drive populations to extinction. * We discuss our results in relation to the evolution towards, and the breakdown of, dioecy, and the ecological and evolutionary implications of labile sex expression.     

ARE TRIOECY AND SEXUAL LABILITY IN ATRIPLEX CANESCENS GENETICALLY BASED?: EVIDENCE FROM CLONAL STUDIES

Prior studies have alternatively considered floral phenotypes in Atriplex canescens as trioecious (having three sexual genders) and/or dioecious and having a “leaky genetical switch.” Clones transplanted from three populations and grown in common gardens reveal the existence of two distinctly different genetic controls regulating gender expression. In some clones gender is fixed as male (staminate) or female (pistillate), while in other clones gender varies, ranging from a mixture of male and female ramets to simultaneous hermaphrodites with various proportions of male and female flowers. For clones which vary their sex expression, variation occurs within irrigation treatments, between treatments and over time, as a consequence of the combined effects of genotype plus environment. The magnitude of sex change is also a product of the interaction of genetics and environment. Some clones have been repeatedly examined for 20 years.     

Geographic variation in the breeding system and the evolutionary stability of trioecy in Pachycereus pringlei (Cactaceae)

The Sonoran Desert columnar cactus Pachycereus pringlei has a geographically variable, non-hermaphroditic breeding system. It is trioecious (separate males, females and hermaphrodites) in the northern two-thirds of its range in Sonora, Mexico, and in the southern three-quarters of its range in Baja California, Mexico, and is gynodioecious (separate females and hermaphrodites) elsewhere. Trioecy occurs near known maternity roosts of its major pollinator, the nectar-feeding bat Leptonycteris curasoae; gynodioecy occurs>50km from known bat roosts. The observed geographic patterns cannot be explained by limited gene flow or by the geographic distributions of diurnal avian pollinators. Our field observations plus a theoretical analysis suggest that the abundance of chiropteran pollinators plays an important role in the maintenance of trioecy in this plant. Under pollinator limitation, trioecy can be a stable breeding system in this species. This revised version was published online in July 2006 with corrections to the Cover Date.