Macroevolutionary synthesis of flowering plant sexual systems

Abstract

Sexual system is a key determinant of genetic variation and reproductive success, affecting evolution within populations and within clades. Much research in plants has focused on evolutionary transitions away from the most common state of hermaphroditism and toward the rare state of dioecy (separate sexes). Rather than transitions predominantly toward greater sexual differentiation, however, evolution may proceed in the direction of lesser sexual differentiation. We analyzed the macroevolutionary dynamics of sexual system in angiosperm genera that contain both dioecious and nondioecious species. Our phylogenetic analyses encompass a total of 2145 species from 40 genera. Overall, we found little evidence that rates of sexual system transitions are greater in any direction. Counting the number of inferred state changes revealed a mild prevalence of transitions away from hermaphroditism and away from dioecy, toward states of intermediate sexual differentiation. We identify genera in which future studies of sexual system evolution might be especially productive, and we discuss how integrating genetic or population-level studies of sexual system could improve the power of phylogenetic comparative analyses. Our work adds to the evidence that different selective pressures and constraints act in different groups, helping maintain the variety of sexual systems observed among plants.

Drivers of large‐scale geographical variation in sexual systems of woody plants

“…In Costa Rica, Vamosi and Queenborough (2010) found a comparable reliance of dioecious and monoecious species on insect and wind pollination in a series of forest plots along a local transect. These results might indicate that monoecy adapts to specific ecological conditions flexibly or that monoecy is an intermediate stage between the other two sexual systems (Goldberg et al, 2017) and thus is not so clearly associated with particular environmental conditions. Here, we found that the proportions of dioecious and monoecious species consistently increased with the average plant height per grid cell.…”

“…(Goldberg et al, 2017). By combining these data with high-resolution species distribution maps, we have explored the geographical variation in the composition of sexual systems of woody plants in China and their potential abiotic (climatic) and biotic (plant traits and evolutionary age) drivers.…”

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

“…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 . ; Kafer et al . ).…”

“…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).…”

“…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). Within genera, Goldberg et al (2017) found that transitions towards combined sexes were no less common than those towards separate sexes. In many of these reversions, dioecy evolved from monoecy, not hermaphroditism with bisexual flowers, suggesting that the association between dioecy and monoecy (Renner & Ricklefs 1995) may be explained not only by the evolution of dioecy from hermaphroditism via monoecy, but also by the breakdown of dioecy to monoecy.…”