The open architecture, modular growth, and seemingly endless modifications of the timing of anther and stigma function of flowering plants have led to a large number of sexual systems (Darwin 1877; Errera and Gevaert 1878; Yampolsky and Yampolsky 1922; Sakai and Weller 1999; Barrett 2002). “Sexual system” here refers to the distribution and function of gamete-producing morphological structures (Sakai and Weller 1999), not realized mating patterns. Although the terminology for realized mating patterns (outcrossing, selfing, mixed mating) and genetic mechanisms (self-compatibility, self-incompatibility) is straightforward, that for the sexual systems can appear daunting, with names such as monoecy, andromonoecy, gynomonoecy, heterostyly, enantiostyly, dioecy, androdioecy, gynodioecy, trioecy, or polygamodioecy, in addition to the overlaid phenological strategies dichogamy, duodichogamy, and heterodichogamy (Delpino 1874; Darwin 1877; Todd 1882; Stout 1928; Gleeson 1982; Ross 1982; Lloyd and Webb 1986; Barrett 1992; McArthur et al. 1992; Bertin and Newmann 1993; Renner and Ricklefs 1995; Renner 2001; Jesson and Barrett 2002; Pannell 2002; Dorken and Barrett 2003; Gross 2005; Vamosi et al. 2006). Different uses of some of these terms by different authors have repeatedly caused misunderstandings, a recent example being the different meaning given the term heterodichogamy by de Jong (1976), Gleiser and Verdú (2005), and Pannell and Verdú (2006), as will become apparent below.
Pathways between plant sexual systems can be inferred in three ways, by population-level studies, sometimes in combination with phylogeographic approaches (e.g., Pendleton et al. 2000; Dorken and Barrett 2004a; Stehlik and Barrett 2006), by species-level studies that rely on the comparative method (e.g., Weller and Sakai 1999; Renner and Won 2001; Graham and Barrett 2004; Levin and Miller 2005; Navajas-Pérez et al. 2005), and by modeling (e.g., Charlesworth and Charlesworth 1978; Pannell and Verdú 2006; Ehlers and Bataillon 2007; Gleiser et al., unpubl. ms.). These approaches address different ways in which a system can be considered a “pathway,” all of them valid. The phylogenetic approach reveals whether the sexual system of a species is similar to that of its relatives, the assumption being that all may share a common ancestral system. The population-genetic approach may reveal directional selection, and prospective modeling points to likely outcomes resulting from evolutionary stable strategies. The present study uses the phylogenetic approach to address a hypothesis about the likely evolutionary pathway to dioecy in Acer that was put forward by Gleiser and Verdú (2005), based on phylogenetic inference, and which subsequently led to a new model for the evolution of dioecy (Pannell and Verdú 2006).
The long-standing focus on pathways between flowering plant sexual systems (Ross 1982; Pannell and Verdú 2006), with the accompanying need to assign species to clear categories (e.g., Gleiser and Verdú 2005; this study), may have contributed to plastic sex expression receiving relatively little attention (but see Dorken and Barrett 2003, 2004; Miller and Diggle 2003; Delph and Wolfe 2005; Ehlers and Bataillon 2007). Plasticity in sex expression means that sex is determined or modulated by the environment and changes adaptively during each individual's lifetime (Charnov and Bull 1977). It is common throughout land plants (Korpelainen 1998; Taylor et al. 2005), and ranges from switches between male and female phases over the life of an individual (as in Arisaema and Catasetum) to shorter-term changes in resource allocation to male and female function.
A clade with particularly well-documented sexual liability is Acer (Wittrock 1886; Haas 1933; de Jong 1976; Hibbs and Fischer 1979; Freeman et al. 1980; Barker et al. 1982; Sakai and Oden 1983; Primack and McCall 1986; Sakai 1990; Matsui 1995; Bendixen 2001; Sato 2002; Tal 2006). Acer comprises 124 species in the Northern Hemisphere (van Gelderen et al. 1994), most of them in China, Korea, and Japan (81%); Europe and Western Asia have 12% of the species, Eastern North America 5%, and Western North America 4%. Morphologically, maple flowers can be bisexual or unisexual. Functionally, however, they are unisexual (exceptions are exceedingly rare; de Jong 1976: 17), with most species being monoecious (flowers of both sexes on each tree), but a few dioecious (male and female trees), polygamodioecious (male trees, female trees, and monoecious trees), or androdioecious (male trees and monoecious trees). All monoecious Acer flower dichogamously (male and female flowering separated in time), and those with large inflorescences often put out three synchronized batches of flowers in the sequence male → female → male, a system called duodichogamy (Stout 1928; de Jong 1976; Luo et al. 2007). Protandrous trees or duodichogamous trees often are inconstant, failing to produce female flowers in some years, but not others. Lastly, some species include a certain percentage of individuals that flower in the sequence male → female (protandrous) and others with the opposite sequence (protogynous). If most trees in a population specialize in this manner, being either protogynous or protandrous, this constitutes heterodichogamy (Delpino 1874; Gleeson 1982; Renner 2001; Endress and Lorence 2004; Pannell and Verdú 2006). Unfortunately, heterodichogamy has also been used without regard to the occurrence of two genetic morphs (e.g., de Jong 1976; Gleiser and Verdú 2005).
With its rich mix of morphological and temporal sexual strategies, Acer presents a remarkable opportunity to study the evolution of sexual systems. The first such study was that of Gleiser and Verdú (2005) who relied on de Jong's (1976) biosystematic monograph to score the sexual system of 44 species, from which they inferred character transformations in the context of three published phylogenies that included 29, 37, or 39 species (with partial taxon overlap between studies). For trait change inference, Gleiser and Verdú created five categories loosely based on de Jong (Materials and Methods, below). Following phylogenetic inference of trait change, using either models that involved ordered states and one or two rate parameters or a model that treated the five systems as a continuous variable, they concluded (l.c., p. 633), “Three different paths to dioecy have been followed in the genus Acer: from heterodichogamous androdioecy; from heterodichogamous trioecy; and from dichogamous subdioecy.”
We here use a new molecular phylogeny that includes almost all dioecious species of Acer and a compilation of all data on Acer reproductive biology to test Gleiser and Verdú's (2005) hypotheses and to infer sexual system evolution in Acer. Based on a molecular clock, we also place sexual system changes in a temporal framework, focusing on transitions involving dioecy.