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

Abstract

Summary• 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.

Sex determination in dioecious Mercurialis annua and its close diploid and polyploid relatives

“…Indeed, females of dioecious M. annua occasionally produce small numbers of staminate flowers with fully viable pollen (Yampolsky, 1919), suggesting incomplete suppression of a male function in XX individuals, and this tendency also seems to be a quantitative trait (G. Cossard and J.R. Pannell, unpublished data). Such leakiness in the expression of gender is very common in dioecious species, especially those derived from monoecy where male and female functions can be leaky (Lloyd, 1980;Lloyd and Bawa, 1984;Delph, 2003;Ehlers and Bataillon, 2007). Determining whether the genetic architecture of s.d.…”

Ecological genetics of sex ratios in plant populations

“…Darwin (1877) identified several species in which populations were composed of females, males and hermaphrodites. Sexual diversity of this type is now reported from numerous species, raising the question of how it originates and whether it represents a stable sexual system, or is simply a transient condition associated with the evolution of dioecy, as Darwin surmised (Lloyd 1976;Charlesworth & Charlesworth 1978;Ehlers & Bataillon 2007). Theoretical investigations of the evolutionary maintenance of subdioecy indicate that coexistence of three sexes can occur as a stable polymorphism, although under restrictive conditions (Maurice & Fleming 1995;Ehlers & Bataillon 2007), or simply cannot be maintained All plants in each sample were recorded as female (grey bar), male (black bar) or non-reproductive (vegetative; white bar).…”

“…Several hypotheses may account for the discrepancy between these theoretical expectations and empirical observations. First, resource-dependent gender plasticity may lessen the trade-off between female and male fitness and help maintain subdioecy (Ehlers & Bataillon 2007). Second, subdioecy may persist at the metapopulation level as a result of selection for hermaphrodites during colonization, and unisexuals in established colonies due to inbreeding avoidance and optimal resource allocation (Pannell 2006).…”

Darwin's legacy: the forms, function and sexual diversity of flowers

“…These populations are genuinely androdioecious. Second, a common feature of dioecious populations, especially those that have originated via the gynodioecious pathway, is the occurrence of genetically based sex inconstancy in male plants (Lloyd 1976;Dorken & Barrett 2004a;Ehlers & Bataillon 2007). In populations of most dioecious species male sex inconstancy is expressed at a relatively low level (approx.…”