On the rarity of dioecy in flowering plants

Abstract

Dioecy, the coexistence of separate male and female individuals in a population, is a rare but phylogenetically widespread sexual system in flowering plants. While research has concentrated on why and how dioecy evolves from hermaphroditism, the question of why dioecy is rare, despite repeated transitions to it, has received much less attention. Previous phylogenetic and theoretical studies have suggested that dioecy might be an evolutionary dead end. However, recent research indicates that the phylogenetic support for this hypothesis is attributable to a methodological bias and that there is no evidence for reduced diversification in dioecious angiosperms. The relative rarity of dioecy thus remains a puzzle. Here, we review evidence for the hypothesis that dioecy might be rare not because it is an evolutionary dead end, but rather because it easily reverts to hermaphroditism. We review what is known about transitions between hermaphroditism and dioecy, and conclude that there is an important need to consider more widely the possibility of transitions away from dioecy, both from an empirical and a theoretical point of view, and by combining tools from molecular evolution and insights from ecology.

Transitions in sex determination and sex chromosomes across vertebrate species

“…Alternatively, if gonochorism is the ancestral state in fish (still to be formally tested), then the genetic and developmental mechanisms that underlie the evolution of hermaphroditism from a gonochoristic ancestor might preclude a reversion to separate sexes. Such a constraint does not appear to be present in flowering plants, as the evolution of separate sexes from a hermaphroditic ancestor has occurred many times, and there are no differences in the rates of transition between hermaphroditism and dioecy (Barrett, ; Goldberg et al., ; Käfer et al., , ; Renner, ). Future work is needed to identify the evolutionary and genetic mechanisms underlying transitions between hermaphroditism and separate sexes in plants and fish, as well as the potential ecological or life history conditions that might predispose these lineages to hermaphroditism.…”

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

“…; Kafer et al . ). For instance, dioecy was lost several times in the large and successful Cucurbitaceae family (Volz & Renner ; Schaefer & Renner ), as well as in the genera Bursera (Becerra & Venable ), Garcinia (Sweeney ), Gallium (Soza & Olmstead ) and Dodonaea (Harrington & Gadek ).…”

“…However, the dead‐end hypothesis has been challenged by analysis suggesting that the evolution of dioecy might actually increase lineage diversification, and that the scattered phylogenetic distribution of dioecious species might be explained by frequent reversions from dioecy to functional hermaphroditism, that is, to a state in which plants have either bisexual flowers or flowers of both sexes (‘monoecy’) (Käfer & Mousset ; Kafer et al . , ; Sabath et al . ).…”

“…This distribution might suggest that dioecy is an evolutionary dead end or 'failure' (Westergaard 1958;Bull & Charnov 1985;Heilbuth 2000), such that lineages with separate sexes diversify less and are more prone to extinction than their hermaphroditic counterparts. However, the dead-end hypothesis has been challenged by analysis suggesting that the evolution of dioecy might actually increase lineage diversification, and that the scattered phylogenetic distribution of dioecious species might be explained by frequent reversions from dioecy to functional hermaphroditism, that is, to a state in which plants have either bisexual flowers or flowers of both sexes ('monoecy') (K€ afer & Mousset 2014;Kafer et al 2014Kafer et al , 2017Sabath et al 2015).…”

“…Evidence for reversions from dioecy to hermaphroditism or monoecy has been accumulating for some time. Phylogenetic analysis of clades in which both dioecy and functional hermaphroditism occur indicates that dioecy has not always been derived from, but may also be ancestral to, hermaphroditism or monoecy (Goldberg et al 2017;Kafer et al 2017). For instance, dioecy was lost several times in the large and successful Cucurbitaceae family (Volz & Renner 2008;Schaefer & Renner 2010), as well as in the genera Bursera (Becerra & Venable 1999), Garcinia (Sweeney 2008), Gallium (Soza & Olmstead 2010) and Dodonaea (Harrington & Gadek 2010).…”