An angiosperm-wide analysis of the gynodioecy–dioecy pathway

Abstract

Aims About 6 % of an estimated total of 240 000 species of angiosperms are dioecious. The main precursors of this sexual system are thought to be monoecy and gynodioecy. A previous angiosperm-wide study revealed that many dioecious species have evolved through the monoecy pathway; some case studies and a large body of theoretical research also provide evidence in support of the gynodioecy pathway. If plants have evolved through the gynodioecy pathway, gynodioecious and dioecious species should co-occur in the same genera. However, to date, no large-scale analysis has been conducted to determine the prevalence of the gynodioecy pathway in angiosperms. In this study, this gap in knowledge was addressed by performing an angiosperm-wide survey in order to test for co-occurrence as evidence of the gynodioecy pathway. † Methods Data from different sources were compiled to obtain (to our knowledge) the largest dataset on gynodioecy available, with 275 genera that include at least one gynodioecious species. This dataset was combined with a dioecy dataset from the literature, and a study was made of how often dioecious and gynodioecious species could be found in the same genera using a contingency table framework. † Key Results It was found that, overall, angiosperm genera with both gynodioecious and dioecious species occur more frequently than expected, in agreement with the gynodioecy pathway. Importantly, this trend holds when studying different classes separately (or sub-classes, orders and families), suggesting that the gynodioecy pathway is not restricted to a few taxa but may instead be widespread in angiosperms. † Conclusions This work complements that previously carried out on the monoecy pathway and suggests that gynodioecy is also a common pathway in angiosperms. The results also identify angiosperm families where some (or all) dioecious species may have evolved from gynodioecious precursors. These families could be the targets of future small-scale studies on transitions to dioecy taking phylogeny explicitly into account.

On the rarity of dioecy in flowering plants

“…), and gynodioecy is associated with quite different traits than is dioecy, as gynodioecy is for example more frequent in herbaceous plants and temperate climates (Dufay et al . ; Caruso et al . ; Rivkin et al .…”

Male‐biased hermaphrodites in a gynodioecious shrub,Daphne jezoensis

“…Gynodioecy is a breeding system in which populations consist of hermaphrodite and female individuals that are derived from a male sterility mutation in hermaphrodite populations (Lewis 1941;Lloyd 1975). Gynodioecy is widely considered an intermediate stage in the evolutionary pathway from hermaphroditism to dioecy (Charlesworth & Charlesworth 1978;Delph & Wolf 2005;Ashman 2006;Dufay et al 2014) although there is some debate on the evolutionary significance of the gynodioecy-dioecy pathway (see Spigler & Ashman 2012;Dufay et al 2014). In the gynodioecy-dioecy pathway, the female frequency within populations and the extent of female reproductive advantage are key issues to evaluate the evolutionary status in the transition from hermaphroditism to dioecy.…”

The role of infectious disease in the evolution of females: Evidence from anther‐smut disease on a gynodioecious alpine carnation*

“…The evolution of females from hermaphroditic populations (gynodioecy) is widely hypothesized to be an important pathway for the evolution of separate males and females (dioecy: Charlesworth and Charlesworth ; Barrett ; Dufay et al. ). As females increase in frequency, hermaphrodites gradually gain more fitness through male function, setting the selective conditions necessary for the evolution of true males (Charlesworth and Charlesworth ).…”