TECHNICAL COMMENT
doi:10.1111/j.1558-5646.2007.00221.x
THE EVOLUTION OF DIOECY,
HETERODICHOGAMY, AND LABILE SEX
EXPRESSION IN ACER
S. S. Renner,1,2 L. Beenken,1 G. W. Grimm,3 A. Kocyan,1 and R. E. Ricklefs4
1 Department
2 E-mail:
3 Institute
of Biology, University of Munich, Menzinger Str. 67, D-80638 Munich, Germany
renner@lrz.uni-muenchen.de
of Geosciences, University of Tübingen, Sigwartstr. 10, D-72076 Tübingen, Germany;
4 Department
of Biology, University of Missouri-St. Louis, 8001 Natural Bridge Rd., St. Louis, MO 63121, USA
Received January 24, 2007
Accepted June 25, 2007
The northern hemisphere tree genus Acer comprises 124 species, most of them monoecious, but 13 dioecious. The monoecious
species flower dichogamously, duodichogamously (male, female, male), or in some species heterodichogamously (two morphs that
each produce male and female flowers but at reciprocal times). Dioecious species cannot engage in these temporal strategies. Using
a phylogeny for 66 species and subspecies obtained from 6600 nucleotides of chloroplast introns, spacers, and a protein-coding
gene, we address the hypothesis (Pannell and Verdú, Evolution 60: 660–673. 2006) that dioecy evolved from heterodichogamy.
This hypothesis was based on phylogenetic analyses (Gleiser and Verdú, New Phytol. 165: 633–640. 2005) that included 29–39
species of Acer coded for five sexual strategies (duodichogamous monoecy, heterodichogamous androdioecy, heterodichogamous
trioecy, dichogamous subdioecy, and dioecy) treated as ordered states or as a single continuous variable. When reviewing the
basis for these scorings, we found errors that together with the small taxon sample, cast doubt on the earlier inferences. Based on
published studies, we coded 56 species of Acer for four sexual strategies, dioecy, monoecy with dichogamous or duodichogamous
flowering, monoecy with heterodichogamous flowering, or labile sex expression, in which individuals reverse their sex allocation
depending on environment–phenotype interactions. Using Bayesian character mapping, we infer an average of 15 transformations,
a third of them involving changes from monoecy-cum-duodichogamy to dioecy; less frequent were changes from this strategy to
heterodichogamy; dioecy rarely reverts to other sexual systems. Contra the earlier inferences, we found no switches between
heterodichogamy and dioecy. Unexpectedly, most of the species with labile sex expression are grouped together, suggesting that
phenotypic plasticity in Acer may be a heritable sexual strategy. Because of the complex flowering phenologies, however, a concern
remains that monoecy in Acer might not always be distinguishable from labile sex expression, which needs to be addressed by
long-term monitoring of monoecious trees. The 13 dioecious species occur in phylogenetically disparate clades that date back to
the Late Eocene and Oligocene, judging from a fossil-calibrated relaxed molecular clock.
KEY WORDS:
Dioecy, heterodichogamy, inference of character evolution, labile sex, phenotypic plasticity, sexual systems, stochas-
tic mapping of characters.
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 Yam-
C 2007 The Society for the Study of Evolution.
2007 The Author(s). Journal compilation
Evolution 61-11: 2701–2719
C
2701
polsky 1922; Sakai and Weller 1999; Barrett 2002). “Sexual
system” here refers to the distribution and function of gameteproducing morphological structures (Sakai and Weller 1999), not
realized mating patterns. Although the terminology for realized
TECHNICAL COMMENT
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
2702
EVOLUTION NOVEMBER 2007
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
TECHNICAL COMMENT
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.
Materials and Methods
TAXON SAMPLING AND DNA SEQUENCING
Previous phylogenies of Acer, including the three used by Gleiser
and Verdú (2005), relied on relatively small amounts of data from
the internal transcribed spacer (ITS) region of nuclear ribosomal
DNA and the chloroplast trnL intron and spacer. To the extent that
these studies overlapped in species sampling, they yielded contradictory relationships, although not with statistical support. To
remedy this problem, our phylogeny is based on a larger amount
of data from five combined chloroplast loci. Online Supplementary Table S1 lists all species sequenced for this study with author
names, sources, geographic provenance, GenBank accession numbers, and assignments to sections and series in the classification
of van Gelderen et al. (1994). The sequenced species represent all
but one of the sections accepted by de Jong (1994), whose taxon
concepts we follow. The missing section is Wardiana, which contains only A. wardii W.W. Sm. A previous study (Grimm et al.
2006) found A. wardii embedded in the Palmata clade (section
Palmata sensu de Jong 1994), which is well represented in our
study. Sequences of A. fabri and A. kweilinense are from another
study (Renner et al., unpubl. ms.).
Sequences of the cp trnD-trnT and psbM-trnD spacers were
downloaded from GenBank (Li et al. 2006) and added to our
data, with a few taxa not sequenced for these loci coded as having unknown nucleotides. Trees were rooted with both species of
Dipteronia, two species of Aesculus, and Koelreuteria bipinnata
based on a phylogeny for Sapindaceae (Harrington et al. 2005).
Total genomic DNA was isolated from silica-dried leaves or
from herbarium specimens using commercial plant DNA extraction kits. The polymerase chain reactions (PCR) followed standard
protocols. Reaction products were purified with a commercial
clean-up kit, and cycle sequencing was performed with BigDye
Terminator cycle sequencing kits (Applied Biosystems, Norwalk,
CT), using 1/4- or 1/8-scale reaction mixtures. The dye terminators were removed with the help of commercial kits, according to
the manufacturers’ protocols. Purified sequencing reactions were
run on an ABI 3130 (Applied Biosystems, Darmstadt, Germany)
automated sequencer.
Primers used to amplify the rbcL gene were 1F of Fay et al.
(1997) and 1460R of Olmstead et al. (1992). For cycle sequencing, they were supplemented by the internal primers 600F (ATTTATGCGTTGGAGAGACCG) and 800R (CAATAACRGCATGCATYGCACGRT) (Kocyan et al. 2007). For the trnL intron and
adjacent trnL-F spacer, primers c, d, e, and f of Taberlet et al.
(1991) were used for amplification and sequencing. For the rpl16
intron, we used primers 71F of Jordan et al. (1996) and 1067F of
Asmussen (1999); and for the psbA-trnH region, we used primers
psbA of Sang et al. (1997) and trnH2 of Tate and Simpson (2003).
DNAs from herbarium material were amplified with low annealing
temperatures and/or with internal primers. Forward and reverse
reads were obtained for most samples. Sequences were edited
with Sequencher (4.6; Gene Codes, Ann Arbor, MI) and aligned
by eye, using MacClade 4.06 (Maddison and Maddison 2003).
PHYLOGENETIC ANALYSES
Maximum likelihood (ML) analyses were performed with
RAxML version 2.2.1 (Stamatakis 2006, http://icwww.epfl.
ch/∼stamatak/index-Dateien/Page443.htm) and Bayesian analyses with MrBayes version 3.1.2 (Huelsenbeck and Ronquist 2001;
Ronquist and Huelsenbeck 2003). The best-fitting evolutionary
model for the concatenated data (6855 nucleotides including gaps)
selected by MrModeltest version 2.2 (Nylander 2004), employing
the Akaike information criterion, was the general time-reversible
(GTR) model plus a gamma-shape parameter (Ŵ) and proportion of invariable sites (I). For Bayesian analyses we used a twopartition model, with separate estimation of substitution rates under the GTR + Ŵ + I model for the coding (rbcL) and noncoding
regions. Evolutionary rates were allowed to differ across partitions
by unlinking the sets of parameters. Some runs were started from
an independent random starting tree, others from the last tree found
in the previous run. Markov chain Monte Carlo (MCMC) runs extended for two million generations, with trees sampled every 100
generations. Each run employed Metropolis-coupled MCMC, using three heated chains in addition to the sampled (cold) chain
(the default settings in MrBayes). We used a flat Dirichlet prior
for the relative nucleotide frequencies and rate parameters, a discrete uniform prior for topologies, and an exponential distribution
(mean 1.0) for the gamma-shape parameter and all branch lengths.
Convergence was assessed by checking that final likelihoods and
majority rule topologies in different runs were similar; that the
standard deviations (SD) of split frequencies were <0.01; that the
log probabilities of the data given the parameter values fluctuated
within narrow limits; that the convergence diagnostic given by
MrBayes approached 1; and by examining the plot provided by
MrBayes of the generation number versus the log probability of
the data.
For ML searches with RAxML, we used a 6664-character matrix that excluded most large gaps and employed the GTR + CAT
approximation of the GTR + Ŵ model, using 25 rate categories
to approximate the gamma-shape parameter. Model parameters
were estimated in RAxML over the duration of specified runs,
and searches started from complete random trees.
Statistical support was measured by ML bootstrapping and
Bayesian posterior probabilities.
EVOLUTION NOVEMBER 2007
2703
TECHNICAL COMMENT
CODING OF SEXUAL SYSTEMS AND INFERENCE
OF TRAIT CHANGE
Many species of Acer have been the subject of multiyear reproductive biology studies, sometimes with large sample cohorts; Table 1
is a compilation of all studies on Acer sexual systems that we could
find. To infer sexual system evolution in the genus, we scored as
many of the 66 species and subspecies in the molecular tree as possible for the following four states: dioecious, monoecious with dichogamous or duodichogamous flowering, monoecious with heterodichogamous flowering, or sexually labile. This resulted in the
scoring of 52 species/subspecies (Table 1). As mentioned (Introduction), all monoecious species of Acer flower dichogamously
and/or duodichogamously, with smaller inflorescences doing the
former, larger ones the latter. Dioecious species cannot engage in
dichogamous, duodichogamous, or heterodichogamous flowering
because these strategies depend on each individual producing male
and female flowers.
At least five species, A. campestre, A. japonicum, A. opalus,
A. platanoides, and A. pseudoplatanus, appear to have consistently protogynous and protandrous individuals; that is, these
species are at least partially heterodichogamous (references see
Table 1). In addition, their populations contain inconsistent protandrous trees and/or duodichogamous trees. Unfortunately, the percentage of individuals that are protandrous or protogynous specialists or exhibit labile sex is only known for a few species.
In A. japonicum, for example, 3.4–5.6% of 95 trees changed
sex expression every year (over four years of observation; Asai
2000), although most trees were either protandrous or protogynous. We did two runs, one with A. japonicum as heterodichogamous (following Asai 2000 and Sato 2002), the other with
A. japonicum coded as sexually labile. This had very little effect on
the estimated transition rates, and we therefore report only results
from the first run. In total, seven or eight species (Table 1) were
scored as sexually labile because multiyear studies have shown
that some proportion of their individuals change sex expression
depending on phenotype–environment interactions.
Of the outgroups, Dipteronia is monoecious and duodichogamous (de Jong 1976), whereas Aesculus and Koelreuteria are andromonoecious and dichogamous (Bertin 1982; Ronse Decraene
et al. 2000; L. Beenken, pers. obs. in the Munich Botanical Garden). The distant outgroup Koelreuteria was excluded from trait
change analyses.
Table 1 includes the sexual strategy scorings of all species
in Gleiser and Verdú (2005) and de Jong (1976) whom they cite
as their source. de Jong’s results are based on up to 10 years of
monitoring of cultivated trees, observations on wild trees of European species, and indirect evidence from mode of inflorescence
branching and old fruit stalks on herbarium specimens; he listed
all studied herbarium specimens in an appendix. de Jong assigned
113 species to 10 sexual expression types plus flowering modes,
2704
EVOLUTION NOVEMBER 2007
designated with the letters A through G, plus three letter combinations (de Jong 1976: table 2; de Jong 1994: figure 6.3). Unfortunately, de Jong called species heterodichogamous whenever
he found protandrous and protogynous inflorescences, whether
on one tree, on different trees, or only on herbarium sheets. A
few examples of his application of the term to species producing protandrous and protogynous inflorescences on the same tree
are A. griseum (p. 77), A. japonicum (p. 59), A. pseudoplatanus
(p. 35), and A. platanoides (p. 51). This use of heterodichogamy is
fundamentally different from the genetic system of two temporal
(genetic) morphs that other authors call heterodichogamy (Renner
2001 for a review; Pannel and Verdú 2006). Gleiser and Verdú’s
(2005) scorings of numerous species as heterodichogamous for
which there is no information on morph frequencies suggest that
they may have been misled by de Jong’s use of heterodichogamy.
These scoring problems affect two-thirds of the species included
in their study (cf. our Table 1).
We modeled changes in sexual system by means of the
stochastic character mapping technique described by Huelsenbeck
et al. (2003) and implemented in the program SIMMAP (Bollback 2006; version 1.0 Beta 2.3 available at http://www.simmap.
com/simmap/simmap.html). The Markov approach estimates the
rates at which a discrete character undergoes state changes as it
evolves through time (Pagel 1994; Lewis 2001; Huelsenbeck et al.
2003). We opted for Bayesian estimation of state transformations
because this approach allows one to average over equally likely
topologies, which is relevant because the Acer phylogenetic tree
has a poorly resolved backbone.
The rate and number of state transformations were estimated
on the 7501 post burn-in trees (with branch lengths) from a
Bayesian analysis (that used the search strategies described under
Phylogenetic analyses) of the chloroplast dataset after the exclusion of the taxa with unknown sexual systems and the distant
outgroup Koelreuteria. This left 56 taxa and four states. For a
four-state character, 12 rates must be estimated, as each sexual
system can change into any other. A rule of thumb is that for each
rate parameter to be estimated, there should be 10 species with
known character states in the phylogenetic tree; clearly, our dataset
does not approach that ratio, resulting in large confidence intervals
(CIs). As recommended, branch lengths were rescaled so that the
total tree length was 1, with branch length proportions maintained.
We assigned no prior value on the rate parameters and instead let
branch lengths define rates. The prior on the bias parameter was
fixed at 1/k, where k is the number of states, this being the recommended approach in SIMMAP for characters with more than two
states.
MOLECULAR CLOCK TIME ESTIMATION
The matrix used for dating excluded the trnD-trnT and psbM-trnD
spacers because of missing sequences, as well as taxa for which
Table 1.
Sexual systems recorded in Acer, and their scoring in this study and in Gleiser and Verdú (2005). Gleiser and Verdú assigned species to five “sexual systems,” namely
duodichogamous monoecy, heterodichogamous androdioecy, heterodichogamous trioecy, dichogamous subdioecy, and dioecy, listing de Jong (1976) as their basis. For comparison,
we include de Jong’s original assignments. Note that de Jong’s (1976) usage of heterodichogamy differs from that of other authors in that he used the term whenever a species has
protandrous and protogynous inflorescences, without considering whether these inflorescences occur on different trees or on the same tree (see text for details). Based on the studies
cited in column 3, we scored species for the following sexual systems: (1) dioecious = individuals genetically male or female; (2) monoecious with duodichogamous flowering; (3)
monoecious with heterodichogamous phenology; (4) labile sex expression. Monoecious Acer species flower dichogamously, duodichogamously, or heterodichogamously; dioecious
species cannot engage in these phenological strategies. A species was scored as having labile sex expression if individuals change their sex expression during ontogeny (often
drastically between years). Chromosome numbers in column 2 are from Gelderen et al. (1994). Note: Because most female flowers morphologically look bisexual, herbarium-based
studies, such as Xu et al.’s treatment of Aceraceae for the Flora of China, often describe Acer species as andromonoecious (i.e., with male and bisexual flowers).
Species
#
A. acuminatum Wall. ex D. Don
A. argutum Maxim.
A. barbinerve Maxim.
A. buergerianum Miq.
–
–
–
26
A. caesium Wall. ex Brand.
A. campbellii subsp. flabellatum
(Rehder) A.E. Murray
A. cappadocicum Gled.
A. carpinifolium Sieb. & Zucc.
2705
A. caudatum subsp.
ukurunduense (Trautv. & C.A.
Mey.) A. E. Murray
A. circinatum Pursh
Scoring in this
study based on
the cited sources
Scoring in
Gleiser and
Verdú (2005)
P. 94: Dioecious Xu et al., unpubl. ms.: Dioecious
P. 94: Dioecious Semm 1966: Dioecious
P. 94: Dioecious Xu et al., unpubl. ms.: Dioecious
de Jong 1976: No information on sexual system
for this species
26 (52?) de Jong 1976: No information on sexual system
for this species; van Gelderen et al. 1994:
Monoecious but “poorly known”
26
de Jong 1976: No information on sexual system
for this species; van Gelderen et al. 1994:
Monoecious
–
P. 102: Duodichogamous Xu et al., unpubl. ms.:
Andromonoecious
26
P. 51: five trees over six years, two protogynous,
one male or protandrous, two
duodichogamous Semm 1966:
Duodichogamous, protandrous and
protogynous, rarely unisexual; Bendixen 2001:
Duodichogamous and heterodichogamous
26
P. 51: two trees over six years; protandrous or
duodichogamous
52
P. 94: Dioecious; tendency to wind pollination
Ohwi 1965
26
van Gelderen et al. 1994: Monoecious Xu et al.,
unpubl. ms.: Andromonoecious
Dioecious
Dioecious
Dioecious
Not included because no
information
Not included because too little
information
Not included in phylogenies
Dioecious
Not included in phylogenies
Heterodichogamous androdioecious
Monoecious; no information on
phenology
Heterodichogamous androdioecious
Monoecious; insufficient
information on phenology
Monoecious with
heterodichogamous flowering
Not included in phylogenies
Not available for sequencing
Heterodichogamous androdioecious
Dioecious
Dioecious
Monoecious; no information on
phenology
Not included in phylogenies
26
Monoecious; insufficient
information on phenology
Heterodichogamous androdioecious
P. 58–61: one tree over six years,
duodichogamous
Heterodichogamous androdioecious
Heterodichogamous androdioecious
Continued
TECHNICAL COMMENT
EVOLUTION NOVEMBER 2007
A. campbellii subsp. sinense
(Pax) P.C. de Jong
A. campestre L.
Sources of information
P. = page number
in de Jong (1976)
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EVOLUTION NOVEMBER 2007
TECHNICAL COMMENT
Table 1.
Continued
Species
#
Sources of information
P. = page number
in de Jong (1976)
Scoring in this
study based on
the cited sources
Scoring in
Gleiser and
Verdú (2005)
A. cissifolium (Sieb. & Zucc.)
K. Koch
A. crataegifolium Sieb. & Zucc.
26
Dioecious
Dioecious
26
Labile sex expression; insufficient
information on phenology
Dichogamous subdioecious
A. davidii subsp. davidii
26
P. 90: Dioecious; also L. Beenken, pers. obs. in
Munich Bot. Garden
P. 61, 71, 102: Depending on the individual
and/or surrounding conditions or age, some
male or female trees are monoecious in other
years (J. Murata, pers. comm., Botanical
Gardens, The University of Tokyo, Feb. 2007)
P. 61, 67, 71: Monoecious, but very variable
A. davidii subsp. grosseri (Pax)
P.C. de Jong
26
Monoecious; insufficient
information on phenology
Labile sex expression
A. diabolicum Blume ex K. Koch
A. distylum Sieb. & Zucc.
26
–
Unclear which subspecies included
in phylogenies
Dichogamous subdioecious (unclear
which subspecies included in
phylogenies)
Dioecious
Heterodichogamous trioecy
A. erianthum Schwer.
–
A. fabri Hance
–
A. glabrum Torr.
–
A. griseum (Franch.) Pax
26
A. heldreichii Boiss.
26
A. henryi Pax
–
P. 61, 66, 71: five trees over six years, male,
female, and protandrous inflorescences all on
one tree; change of sex expression
P. 88: Dioecious Gelderen et al. 1994: Dioecious
P. 74: Duodichogamous, protandrous,
protogynous; only studied from herbarium
specimens
P. 61, 102: Duodichogamous Xu et al., unpubl.
ms.: Andromonoecious
Xu et al., unpubl. ms.: Andromonoecious
P. 93: Unisexual and protogynous; sex change
observed in one cultivated tree studied
between 1963 and 1972
P. 75, 77: six trees studied over three years,
protogynous and protandrous inflorescence
borne on same tree
P. 35: one protogynous tree observed over six
years
P. 90, 93: Dioecious Xu et al., unpubl. ms.:
Dioecious
Dioecious
Monoecious; no information on
phenology
Monoecious; insufficient
information on phenology
Monoecious; no information on
phenology
Monoecious; insufficient
information on phenology
Not included in phylogenies
Not included in phylogenies
Heterodichogamous trioecy
Monoecious; insufficient
information on phenology
Heterodichogamous trioecy
Monoecious; insufficient
information on phenology
Dioecious
Not included in phylogenies
Dioecious
Continued
Table 1.
Continued
#
Sources of information
P. = page number
in de Jong (1976)
Scoring in this
study based on
the cited sources
Scoring in
Gleiser and
Verdú (2005)
A. japonicum Thunb.
26
Monoecious with
heterodichogamous flowering
Heterodichogamous androdioecious
A. kweilinense W. P. Fang
& M. Y. Fang
A. laevigatum Wall.
–
P. 59, 102: Duodichogamous,
heterodichogamous Asai 2000: 95 trees, four
years, eight trees changed their sex expression
over the four years, 3.4–5.6% of trees changed
sex expression every year; Sato 2002: 109
trees, two years, 45 protogynous, 54
protandrous (22 of the latter
duodichogamous), six trees male in both years,
four males in one year but m>f next year
Xu et al., unpubl. ms.: Andromonoecious.
Not included in phylogenies
26
A. laurinum Hassk.
26
Monoecious; no information on
phenology
Monoecious; insufficient
information on phenology
Dioecious
A. macrophyllum Pursh
26
A. mandshuricum Maxim.
26
A. maximowiczianum Miq. (incl.
A. nikoense Maxim.)
–
A. miyabei Maxim.
–
A. mono Maxim.
26
P. 61, 102: Duodichogamous Xu et al., unpubl.
ms.: Andromonoecious
P. 96: Probably dioecious Xu et al., unpubl. ms.:
Androdioecious or dioecious
P. 89: Duodichogamous with occasional loss of
one phase
P. 78: “Few studied specimens” only herbarium
material Xu et al., unpubl. ms.: “Dioecious?”
P. 74–78, Table 12: 10 trees studied over up to six
years. All-male trees changed to producing
bisexual inflorescence and unisexual
inflorescence in subsequent years
P. 51, 55: one tree studied over six years
switched between protandrous to
duodichogamous inflorescences
P. 51: one tree studied over six years,
protogynous Semm 1966: Dichogamous
Not included in phylogenies
Heterodichogamous trioecy
Monoecious; insufficient
information on phenology
Not included because too little
information
Labile sex expression
Heterodichogamous androdioecious
Monoecious; insufficient
information on phenology
Not included in phylogenies
Monoecious; insufficient
information on phenology
Heterodichogamous androdioecious
Heterodichogamous trioecy
Not included in phylogenies
2707
Continued
TECHNICAL COMMENT
EVOLUTION NOVEMBER 2007
Species
2708
EVOLUTION NOVEMBER 2007
TECHNICAL COMMENT
Table 1.
Continued
Species
#
A. monspessulanum L.
26
A. negundo L.
A. nipponicum H. Hara
A. oblongum DC. (A.
albopurpurascens Hayata)
A. opalus Mill.
A. palmatum Thunb.
A. pensylvanicum L.
A. pentaphyllum Diels
A. pilosum Maxim.
A. platanoides L.
Sources of information
P. = page number
in de Jong (1976)
P. 44, 102: Varying between protandrous,
protogynous, and unisexual; Haas 1933:
Protandrous; Semm 1966: Dichogamous,
no sex change
26
P. 90: Dioecious Dawson and Geber 1999:
Dioecious
–
P. 72: Duodichogamous, but some inflorescences
just protandrous or male
26
de Jong 1976: No information on sexual system;
Khushalani 1963: Monoecious
26
P. 44, 102: Individuals protogynous or unisexual
Gleiser et al., unpbl.: 100 trees studied over six
years; 48% protogynous; 38% pure-males;
14% protandrous
26
P. 58, 59: Duodichogamous, protogynous,
occasional pure males; Xu et al., unpubl. ms.:
Andromonoecious
26
P. 61–67: Male, female, and protandrous
inflorescences all on one tree; change of sex
expression; Hibbs and Fisher 1979: Labile sex
expression
–
P. 94: Only one herbarium specimen (the type
collection) studied
–
de Jong 1976: No information on sexual system;
Xu et al., unpubl. ms.: Andromonoecious
26, 39 P. 45–55: Duodichogamous, rarely flowering
purely male Wittrock 1886: 100 trees, 47–50
protogynous, 31–30 protandrous; 7–18 pure
males; 3–8 duodichogamous. Haas 1933;
Svobodavá 1967: Of 152 trees, 110
protandrous, 36 protogynous; Tal 2006: two
years, three trees protandrous, seven
protogynous
Scoring in this
study based on
the cited sources
Scoring in
Gleiser and
Verdú (2005)
Monoecious; insufficient
information on phenology
Heterodichogamous trioecy
Dioecious
Dioecious
Monoecious; insufficient
information on phenology
Monoecious; no information on
phenology
Monoecious with
heterodichogamous flowering
Duodichogamous monoecy
Heterodichogamous androdioecious
Heterodichogamous trioecy
Monoecious; insufficient
information on phenology
Heterodichogamous androdioecious
Labile sex expression
Dichogamous subdioecious
Not included because too little
information
Monoecious
Heterodichogamous androdioecious
Monoecious with
heterodichogamous flowering
Heterodichogamous androdioecious
Not included in phylogenies
Continued
Table 1.
Continued
Species
#
A. pseudoplatanus L.
52
A. rubrum L.
A. rufinerve Sieb. & Zucc.
Scoring in this
study based on
the cited sources
2709
P. 35, 40: Duodichogamous, protandrous,
Monoecious with
protogynous, all three types of inflorescences
heterodichogamous flowering
on the same tree; Scholz 1960: Some trees
consistently protandrous or protogynous,
whereas others switched their sequence of
flowering; Semm 1966: Duodichogamous,
protandrous, protogynous, rarely unisexual;
Binggeli 1992: “In most cases, all
inflorescences of a tree always start flowering
with a male or female sequence and switch to
the other sex one or more times.” (i.e., were
duodichogamous). Proportion of protandrous
and protogynous individuals varying widely
between studies. Tal 2006: Over two years, 55
trees duodichogamous (seven of them lacking
second male phase), 18 protogynous, one pure
male; no tree found to switch sex expression
26
de Jong 1976: No information on sexual system Not included because too
little information
Dioecious
78
Saeki 2005: Dioecious; sex ratio for several
natural populations 35% male, 32% female,
and 33% nonflowering
78, 91, or 108 P. 78–86: Purely female trees, purely male trees, Labile sex expression
bisexual trees, with changing sex expression
over time: “Inconstant females”, “inconstant
males”, “variable plants” Haas 1933; Primack
and McCall 1986: 79 trees, seven years, Sakai
1990: Polygamodioecious
26
P. 61–71: Male, female, and protandrous
Labile sex expression
inflorescences all on one tree; change of sex
expression; Matsui 1995: Labile sex
expression
Scoring in
Gleiser and
Verdú (2005)
Heterodichogamous
androdioecious
Heterodichogamous
androdioecious
Not included in phylogenies
Heterodichogamous trioecy
Dichogamous subdioecious
Continued
TECHNICAL COMMENT
EVOLUTION NOVEMBER 2007
A. pseudosieboldianum
(Pax) Kom.
A. pycnanthum Koch
Sources of information
P. = page number
in de Jong (1976)
Continued
EVOLUTION NOVEMBER 2007
Species
#
Sources of information
P. = page number
in de Jong (1976)
Scoring in this
study based on
the cited sources
Scoring in
Gleiser and
Verdú (2005)
A. saccharinum L.
52
Labile sex expression
Heterodichogamous trioecy
A. saccharum subsp.
grandidentatum (Torr. &
A. Gray) Desm.
A. saccharum Marsh. subsp.
saccharum
–
P. 78–86: Functionally male trees, functionally
female trees, and bisexual trees; Semm 1966:
Bisexual trees, rarely unisexual trees; Sakai
1978: 700 trees, five years, Sakai and Oden
1983: Inconstant females, inconstant males,
variable sex expression
Baker et al. 1982: Labile sex expression
Labile sex expression
Not included in phylogenies
Monoecious; insufficient
information on phenology
Heterodichogamous
androdioecious
A. sieboldianum Miq.
26, 52, 53, 78 P. 44: two cultivated trees studied over three
years, both protogynous; Gabriel 1968: six
trees over three years, protandrous or
protogynous inflorescence, sometimes on
same tree
26
de Jong 1976: No information on sexual system
A. spicatum Lam.
26
A. stachyophyllum Hiern.
A. sterculiaceum subsp.
franchetii (Pax) A.E. Murray
A. takesimense Nakai = A.
pseudosieboldianum subsp.
takemiense (Nakai) de Jong
A. tataricum subsp. ginnala
(Maxim.) Wesm.
26
26
Not included because too little
information
P. 72, 74: Duodichogamous, once protogynous
Monoecious; insufficient
information on phenology
P. 94: Dioecious Xu et al., unpubl. ms.: Dioecious Dioecious
P. 88: Dioecious Xu et al., unpubl. ms.: Dioecious Dioecious
–
de Jong 1976: No information on sexual system
Not included because no
information
Heterodichogamous
androdioecious
26
P. 86, under A. ginnala: four trees studied, one
protogynous, three duodichogamous mixed
with protandrous inflorescence Semm 1966:
Duodichogamous
Monoecious; insufficient
information on phenology
Heterodichogamous
androdioecious
Heterodichogamous
androdioecious
Duodichogamous monoecy
Not included in phylogenies
Not included in phylogenies
Continued
TECHNICAL COMMENT
2710
Table 1.
Table 1.
Continued
#
Sources of information
P. = page number
in de Jong (1976)
Scoring in this
study based on
the cited sources
Scoring in
Gleiser and
Verdú (2005)
A. tataricum subsp. semenovii
(Regel & Herder) A. E. Murray
–
Monoecious; insufficient
information on phenology
Heterodichogamous androdioecious
A. tegmentosum Maxim.
–
P. 86, under A. tataricum: two trees studied, one
protogynous, one duodichogamous mixed
with protandrous inflorescence Semm 1966:
Duodichogamous
de Jong 1976: No information on sexual system
Dichogamous subdioecious
A. trautvetteri Medw.
26
Not included because no
information
Monoecious; insufficient
information on phenology
A. triflorum Kom.
–
Not included because too little
information
Heterodichogamous trioecious
A. truncatum Bunge
26
Monoecious; insufficient
information on phenology
Heterodichogamous androdioecious
A. tschonoskii Maxim.
26
Monoecious; insufficient
information on phenology
Dichogamous subdioecious
A. wardii W.W. Smith
–
Not available for sequencing
Dichogamous subdioecious
Monoecious
Not included in trait inference
Monoecious
Monoecious
Monoecious
Only included to root phylogenies
Not included in trait inference
Duodichogamous monoecy
Duodichogamous monoecy
Not included
Aesculus flava Sol. (A. octandra
Marshall)
Aesculus parviflora Walter
Dipteronia dyeriana Henry
Dipteronia sinensis Oliver
Koelreuteria bipinnata Franch.
P. 35: Duodichogamous, protogynous, two trees
over three years, one tree protogynous, one
duodichogamous
de Jong 1976: No information on sexual system
for this species; Xu et al., unpubl. ms.:
Androdioecious
P. 45: “some living specimens” studied but no
further information for this species given Xu
et al., unpubl. ms.: Andromonoecious
P. 61, 66: Monoecious (citing other authors);
observation on one cultivated tree; Xu et al.,
unpubl. ms.: Andromonoecious
P. 72: “limited number of herbarium specimens
. . . flowers of one sex only”; Xu et al., unpubl.
ms.: Andromonoecious
P. 102: Duodichogamous, protandrous
P. 102: Duodichogamous and protandrous
P. 102: Duodichogamous, but data scarce
P. 102: Herbarium and living tree
P. 102: Duodichogamous (but only one cultivated
tree)
Heterodichogamous androdioecious
2711
TECHNICAL COMMENT
EVOLUTION NOVEMBER 2007
Species
TECHNICAL COMMENT
we did not sequence rbcL (Online Supplementary Table S1).
It consisted of 52 taxa and 4521 nucleotides. The relaxed-clock
approach used was that of Thorne and Kishino (2002; freely
available at http://statgen.ncsu.edu/thorne/). Parameter values under the F84 + G model with five rate categories were estimated with PAML’s baseml (Yang 1997; freely available at
http://abacus.gene.ucl.ac.uk/software/paml.html), this being the
only model implemented in Thorne’s software. We then used
Thorne’s estbranches to calculate branch lengths and their variance, given the sequence data, PAML’s model parameter file, and
a specified rooted topology. The topology used as input was the
highest likelihood tree obtained for the same data with RAxML.
The estbranches output became the prior for MCMC searches
in multidivtime that sought to find the most likely model of rate
change (with rate change assumed to be log-normally distributed),
given the tree topology, fossil constraints, and a Brownian motion
parameter (n) that controls the magnitude of autocorrelation per
million years (MY) along the descending branches of the tree.
Prior gamma distributions on parameters of the relaxed-clock
model were as follows: the mean of the prior distribution for the
root age was set to 63 MY, based on the earliest known fruits of
Dipteronia brownii from the Late Paleocene of Wyoming (McClain and Manchester 2001); the SD of this prior was also set
to 63. The mean and SD of the prior distribution for the ingroup
root rate were set to 0.0001 substitutions/site/MY by dividing the
median of the distances between the ingroup root and the tips
by 63 MY. The prior and SD for n were set to 0.02, following
the manual’s recommendation that the time between root and tips
multiplied by n be about 1. Markov chains in multidivtime were
run for one million generations, sampling every 100th generation
for a total of 10,000 trees, with a burn-in of 1000 trees before
the first sampling of the Markov chain. Like Dipteronia, Acer is
known from Paleocene fruits from North America and Eurasia
(Wolfe and Tanai 1987; Crane et al. 1990; Kittle et al. 2005), but
because they cannot be associated with particular nodes in the
phylogeny, we decided not to employ them as age constraints.
Results
PHYLOGENETIC RELATIONSHIPS
The final dataset used for phylogenetic inference included 6664
characters, following the elimination of 191 positions because of
ambiguous alignment. The data comprised 1142 aligned positions
from the trnL region, 1287 from the rpl16 intron, 783 from the
psbA-trnH spacer, 1524 from the trnD-trnT spacer, 679 from the
psbM-trnD spacer, and 1440 from the rbcL gene. Topologies resulting from individual analyses of these six loci contained no
well-supported conflicting nodes, and we therefore concatenated
the data. The mean gamma-shape parameter estimated by MrBayes for the rbcL gene was ␣ = 0.10, indicating little rate het-
2712
EVOLUTION NOVEMBER 2007
erogeneity, that for the noncoding regions was ␣ = 1.09, indicating
moderate rate heterogeneity. Figure 1 shows a ML tree obtained
from the combined data. Although the backbone of the phylogeny
is poorly resolved, many of the traditionally recognized series and
sections (marked in Fig. 1) are recovered, sometimes with high
statistical support. Section Acer, however, is polyphyletic, because
A. caesium and A. pseudoplatanus do not group with the remaining
species of that section, nor do A. caudatum and A. spicatum of
series Caudata group together.
EVOLUTION OF DIOECY IN ACER
Dioecy evolved in three clades and two isolated species (circled
in Fig. 1). With the divergence between Dipteronia and Acer constrained to minimally 63 MY based on the fossil D. brownii,
the initial radiation of the largest dioecious clade (consisting of
A. acuminatum, A. argutum, A. barbinerve, A. cissifolium,
A. henryi, and A. stachyophyllum; Figs. 1, 2) took place about
37 MY ago, with a 95% CI of 22 to 56 MY. The split between the
dioecious A. diabolicum and A. sterculiaceum is estimated as having occurred 26 MY ago (CI: 12–44 MY), and that of A. laurinum
from A. pycnanthum at 29 (16–46) MY. Divergence times of
A. negundo, A. carpinifolium, and A. craetaegifolium cannot be
estimated because of their statistically unsupported placements
(Fig. 1). The estimated age of the clade comprising four of the
nine species with sexual plasticity is 28 (16–46) MY (Fig. 2).
The rate and frequency distribution of the 12 possible sexual system transformations including those leading to dioecy are
shown in Table 2, and Figure 2 shows a randomly chosen character
history of the 75,010 replicates (10 replicates of character transformations on each of 7501 post burn-in Bayesian trees). The
mean total number of transformations (sexual system changes)
was 15.2, with the most frequent transitions those from monoecy with (duo)dichogamous flowering to dioecy (4.5) and from
monoecy with (duo)dichogamous flower to monoecy with heterodichogamous flowering (3.7). The relative transformation rates
(Table 2) suggest that returns from dioecy to most of the other systems are unlikely, with the exception of a switch to labile sex expression. The switch from heterodichogamous flowering to dioecy
was among the lowest of all observed transition rates (Table 2).
However, given the small overall number of transitions, the 95%
CIs around all estimates are large (or cannot be calculated), and
partly overlap (Table 2).
Discussion
THE DISTRIBUTION OF DIOECY AND
HETERODICHOGAMY IN ACER
Of the 124 species of Acer, 13 are dioecious (van Gelderen
et al. 1994; our Table 1). This may be a slight underestimate
because there are three Chinese entities that are closely related
TECHNICAL COMMENT
Figure 1.
Maximum-likelihood phylogram for 66 species/subspecies of Acer plus four outgroups, based on 6664 nucleotides from four
chloroplast DNA loci. Values above nodes indicate ML bootstrap support > 70%. Dioecious species are shown in bold. The remaining
species are monoecious with duodichogamous or heterodichogamous flowering (marked by arrows) or sexually labile (compare Fig. 2
for sexual systems).
EVOLUTION NOVEMBER 2007
2713
TECHNICAL COMMENT
One of 75,010 character histories inferred on a sample of Bayesian trees obtained with the same chloroplast data as used
for Figure 1 except that taxa with insufficient information on sexual system were excluded (see Materials and Methods). Black lines
Figure 2.
designate dioecy, gray lines monoecy with duodichogamous flowering, thick gray lines monoecy with heterodichogamous flowering,
and hatched lines a plastic sexual system. Table 1 lists the references for each species’ sexual system. Character histories were mapped
under a four-state continuous time Markov process, with trees and branch lengths sampled by the Markov chain. Compare Table 2 for
mean total numbers of transformations and transformation frequency distributions among the 75,010 replicates. The ages in millions of
years (with confidence intervals) are from a Bayesian relaxed molecular clock (see Materials and Methods).
2714
EVOLUTION NOVEMBER 2007
TECHNICAL COMMENT
Table 2. Estimated character transformations and their confidence limits for the sexual strategies monoecy with dichogamous flowering,
monoecy with heterodichogamous flowering, dioecy, and labile sex expression scored for the species of Acer listed in Table 1. Compare
Fig. 2 for a randomly selected character history out of the 75,010 replicates simulated on a post burn-in sample of Bayesian phylograms
obtained from 6674 nucleotides of combined chloroplast loci. Dwell time is the proportion of the total branch length in a particular
character state, averaged over all sampled histories. By dividing the estimated total transformations by the dwell time, the transition
rate can be determined (i.e., the likelihood of a branch having a particular state changing to another state).
Transformations
Total 15.21
Dwell time
Rate
Confidence limits
Dioecy>monoecy-dichogamy
Dioecy>monoecy-heterodichogamy
Dioecy>labile sex expression
Monoecy-dichogamy>monoecy-heterodichogamy
Monoecy-dichogamy>dioecy
Monoecy-dichogamy>labile sex expression
Monoecy-heterodichogamy>monoecy-heterodichogamy
Monoecy-heterodichogamy>dioecy
Monoecy-heterodichogamy>labile sex expression
Labile sex expression>monoecy-dichogamy
Labile sex expression>monoecy-heterodichogamy
Labile sex expression>dioecy
Monoecy-dichogamy
Monoecy-heterodichogamy
Dioecy
Labile sex expression
0.38
0.05
1.56
3.65
4.53
2.41
0.34
0.02
0.05
1.57
0.31
0.31
0.19
0.19
0.19
0.66
0.66
0.66
0.04
0.04
0.04
0.12
0.12
0.12
0.66
0.04
0.19
0.12
2.00
0.26
8.21
5.53
6.86
3.65
8.50
0.50
1.25
13.08
2.58
2.58
0–9.10
0–5.22
4.45–12.52
4.42–6.53
4.74–8.07
2.87–4.92
0–33.90
0–0
0–16
7.30–21.41
0–9.87
0–9.72
or synonymous with the dioecious species A. diabolicum and A.
sterculiaceum and that are also dioecious (Acer leipoense W. P.
Fang & T. P. Soong from Southwest Sichuan, A. yangbiense Y. S.
Chen & Q. E. Yang from Yunnan, and A. sinopurpurascens Cheng
from Central China). If these three are biological species and were
to group with A. diabolicum and A. sterculiaceum as expected
from their morphology, dioecy in Acer would have evolved five
times (Fig. 2). None of the dioecious species are phylogenetically
close to the five (partly) heterodichogamous species, A. campestre,
A. japonicum, A. opalus, A. platanoides, and A. pseudoplatanus
(Fig. 1), and switches from heterodichogamous flowering to
dioecy were among the lowest of all transition rates (Table 2).
This does not fit with the hypothesis that dioecy in Acer evolved
from heterodichogamous ancestors or relatives (Gleiser and Verdú
2005), although see below.
From inspection of the tree (Fig. 1) it appears that dioecy
in maples is not associated with species proliferation and that
the dioecious clades all originated relatively early, with no additional transitions to separate sexes later on. However, current
methods cannot distinguish between infrequent trait evolution and
a trait’s infrequency due to its occurrence in species-poor clades
(Maddison 2006). Morphological traits known to be associated
with dioecy, such as wind pollination and fleshy fruits (Renner
and Ricklefs 1995), do not appear to play a large role in Acer,
with only one of the dioecious species, A. negundo, being windpollinated (Freeman et al. 1976) and some nondioecious species,
for example A. saccharinum, also being wind-pollinated (Sakai
and Oden 1983). All Acer have wind-dispersed fruits. There is
also no obvious association of dioecy and ploidy level (Table 1,
column 2).
Gleiser and Verdú (2005, p. 635) inferred that heterodichogamy was the most likely ancestral condition in the genus.
However, the scoring problems (cf. our Table 1), small taxon
sample (only six dioecious species were included), and weak phylogenies available at the time cast doubt on these inferences. de
Jong (1976) hypothesized that the ancestral sexual system of Acer
was monoecy with dichogamous or duodichogamous flowering
and that heterodichogamous flowering evolved later. His arguments for this were that duodichogamy is the sexual strategy of
Dipteronia, the closest relative of Acer; that andromonoecy is
the sexual system in Aesculus and other Sapindaceae close to
Acer/Dipteronia; and that monoecious duodichogamous flowering is the most common phenological strategy in Acer. Although
our data fit with de Jong’s hypothesis, more solid inference of the
ancestral phenological strategy in Acer will require more data on
the flowering patterns in the basal-most species (compare Fig. 1
and Table 1).
Based on the results of Gleiser and Verdú (2005), Acer became the prime example of the path from heterodichogamy via
androdioecy to dioecy modeled by Pannell and Verdú (2006), because “dioecy appears to have evolved repeatedly via androdioecy
from a heterodichogamous ancestral state in the maple genus,
Acer” (l.c., p. 670). Although our data do not address the theoretical model, Acer should probably no longer be considered a
EVOLUTION NOVEMBER 2007
2715
TECHNICAL COMMENT
strong example of the proposed pathway. This is because heterodichogamy as modeled (Pannell and Verdú 2006) involves reciprocal mating types that occur at a 1:1 ratio as in walnut and pecan
(Gleeson 1982; Thompson and Romberg 1985). In Acer, there is
little evidence of such classic heterodichogamy. Instead, heterodichogamous trees coexist with males and inconstant protandrous
and duodichogamous individuals (e.g., Wittrock 1886; Svobodavá
1967; Asai 2000; Sato 2002; Tal 2006; additional studies are cited
in Table 1). Fluctuations in flowering apparently can stabilize monoecy with heterodichogamous flowering, rather than leading to
dioecy (Gleiser et al., unpubl. ms.).
INCONSTANT MALES, GENETIC MALES
(ANDRODIOECY), AND LABILE SEX
That inconstant individuals are very common in Acer has long
been noted (de Jong 1976; Gleiser et al., unpubl. ms.; Table 1
for additional references). de Jong suggested that occasional allmale flowering, rarely all-female flowering, in normally dichogamous or duodichogamous trees is stress-induced, because the
same trees usually are duodichogamous or protandrous in other
years. In some species, however, the phenotypic sex of all individuals appears to be ontogenetically labile (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; Asai 2000; Sato
2002). As is true of phenotypic plasticity in general, labile sex is
likely to evolve when stress periods occur at appropriate frequency
(Gabriel 2005), such that individuals fare better by constantly adjusting their sex allocation than by adopting a fixed sexual strategy.
From the phylogeny (Figs. 1, 2), it appears that species with labile sex determination are concentrated in section Macrantha (the
A. davidii-A. pensylvanicum clade), a North American/Asian clade
that may be 28 MY (16–46) old (Figs. 1, 2). This clustered occurrence of sexual phenotypic plasticity indicates that it is a heritable
sexual strategy.
In well-studied sexually plastic species, such as A. saccharum
subsp. grandidentatum and A. rufinerve, links between precipitation, water access, and sex expression have been demonstrated
(Barker et al. 1982; Matusi 1995; Ushimaru and Matsui 2001;
Nanami et al. 2004; also for A. pensylvanicum: Hibbs and Fischer 1979, A. pseudoplatanus: Jones 1945a; Scholz 1960; Semm
1966; Binggeli 1992, A. rubrum: Primack and McCall 1986; Sakai
1990, and A. saccharinum: Sakai 1978; Sakai and Oden 1983).
These and other studies (Jones 1945b; Wittrock 1886; Haas 1933;
Asai 2000; Bendixen 2001) suggest that at least in some species
of Acer, male and female reproductive outputs are differentially
affected by habitat quality as envisioned by theories of plant sex
choice (Charnov and Bull 1977; Freeman et al. 1980; Korpelainen
1998; Guillon et al. 2006).
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EVOLUTION NOVEMBER 2007
The commonest and perhaps ancestral (see above) sexual system in Acer is monoecy with dichogamous and duodichogamous
flowering. Duodichogamy is only known from four or five unrelated groups of flowering plants (Luo et al. 2007) and may be
favored by intrasexual competition among pollen parents for access to ovules (Lloyd and Webb 1986: p. 147). Such competition
is expected to be strongest if few ovules are offered or matured
into fruits. Indeed, all known duodichogamous taxa (Castanea,
Cladium, Dipteronia) have few ovules, and Acer, with two ovules
per ovary of which only one develops into a seed, is no exception. Spring-blooming trees with vast numbers of flowers, such as
maples, may also experience pollinator scarcity, at least in some
years. Both factors may favor duodichogamy, which in turn may
facilitate the establishment of inconstant males or male mutants
(i.e., androdioecy) if inconstant males physiologically are able to
“commit” to fruiting late under particularly good conditions (other
pollen donors still be available because of the second male phase
of duodichogamous trees).
Together, the macroevolutionary perspective on sexual system evolution in Acer provided here and results from recent modeling efforts (Ehlers and Bataillon 2007; Gleiser et al., unpubl.
ms.) suggest that monoecy with variable flowering strategies and
the ability of some fraction of trees to change sex expression set
up conditions that slowed down or prevented the evolution of sex
specialization (dioecy). Even if some of the species included here
turn out erroneously scored in terms of their flowering pattern
(duodichogamy vs. heterodichogamy), this would not change the
distribution of dioecy relative to monoecy nor the conclusion that
dioecy in Acer evolved very few times, and mostly a long time ago.
The phylogenetic clustering of the sexually most plastic species
(Fig. 2) was unexpected. There are several other clades of flowering plants that appear to be characterized by labile sex expression (also referred to as environmental sex determination, gender
diphasy, or sex choice [Freeman et al. 1980; Schlessman 1988;
Korpelainen 1998; Guillon et al. 2006]), for instance, species in
the genera Gurania and Psiguria in the Cucurbitaceae, several
oil palms (Elaeis), Arisaema (Araceae), and Catesetinae orchids
(Schlessmann 1988), implying that sexual plasticity can be an
inherited trait.
ACKNOWLEDGMENTS
For plant material we thank A. S. Aiello, the Director of Horticulture and
Curator of the Morris Arboretum of the University of Pennsylvania; Dr.
K. Camelbeke, Director of the Stichting Arboretum in Haacht-Wespelaar,
Belgium; and D. J. Werner, Director of the J. C. Raulston Arboretum,
Department of Horticultural Science, North Carolina State University.
For critical input we thank B. Ehlers, O. Tal, and J. Pannell, and the
Associate Editor J. Kohn. Support came from the National Evolutionary
Synthesis Center (NESCent), NSF #EF-0423641.
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Supplementary Material
The following supplementary material is available for this article:
Table S1. Species with their placement in the classification of van Gelderen et al. (1994) and status as nomenclatural types, DNA
sources, geographic origin, chloroplast regions sequenced and GenBank accession numbers. BG stands for botanical garden,
s.n. for sine numero (without collection number), and TROPICOS for the specimen database of the Missouri Botanical Garden
at http://mobot.mobot.org/W3T/Search/vast.html.
This material is available as part of the online article from:
http://www.blackwell-synergy.com/doi/abs/10.1111/j.1742-4658.2007.00221.x
(This link will take you to the article abstract).
Please note: Blackwell Publishing is not responsible for the content or functionality of any supplementary materials supplied by
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