Notes on the Evolution of Androecial Organisation
in the Magnoliophytina (Angiosperms)
L. P. Ronse Decraene and E. F. Smets
Laboratoryof Plant Systematics, Botanical Institute, Katholieke Universiteit Leuven, Kardinaal Mercierlaan 92, B-3001 Heverlee, Belgium
Received: January 5, 1996; Accepted: August 25, 1997
Abstract: This paper aims to summarize briefly and to update
our ideas about androecial architecture formulated in earlier
publications. Ontogenetic evidence of stamen development,
viz. the initiation, arrangement and relationship of stamens to
other floral morphomes, can be translated into a semophyletic
scheme reflecting the phylogeny of the androecium. The ances-
tral androecium is discussed in the light of recent theories
about angiosperm phylogeny. Two divergent androecial pro-
cesses are proposed for the angiosperms starting from a spiral
androecium with a moderate number of stamens. However,
transitions exist between spiral polyandry, numerous stamens
in whorls, and chaotic polyandry. From an androecium with
several alternating whorls of paired and single stamens, outer
stamen pairs are retained following the successive loss of inner
stamen whorls. Single stamens instead of pairs occur at the
very end of this line and represent a more advanced condition.
This line is mostly present in tri- and dimerous flowers. From
the same starting point diplostemony (with two alternating
whorls of single stamens) originated, again giving rise to var-
ious states usually present in pentamerous or tetramerous
flowers.
Key words: Androecium, character research, ontogeny, reduc-
tive trend, secondary increase, semophylesis, stamen pairs.
Comments on the Ancestral Androecium
Until recently, the traditional approach to the androecium
considered most multistaminate androecia as primitve and
most androecia with few stamens as derived (Arber and
Parkin, 1907; Bessey, 1915; Cronquist, 1981, 1988; Eames,
1961; Takhtajan, 1991; Weberling, 1989). The credo holds that
Magnolia-like flowers with many spirally inserted parts
represent the archetype for androecial evolution. However, it
became clear that all polyandrous forms cannot be regarded
as homologous in the angiosperms, and that many stamens
can be primitive in some cases, but not in others where
flowers with few stamens must be regarded as plesiomorphic
(see Kubitzki, 1973; Leins, 1964, 1975; Ronse Decraene and
Smets, 1987, 1992a). Ideas of the phylogeny of the angio-
sperms and the angiosperm flower have evolved dramatically
over the years. This led to a more prudent approach (Dilcher,
Bot. Acta 111 (1998)77-86
© GeorgThiemeVerlag Stuttgart NewYork
1979; Endress, 1986, 1987a, 1990, 1994a; Friis and Endress,
1990; Gottsberger, 1974,1988), considering different potential
archetypes, such as flowers with an intermediate number of
stamens or flowers with a loose organisation and great
plasticity in floral organ number, phyllotaxis and size. An
alternative to the classical theory is the idea that "paleoherbs"
represent the most primitive angiosperms (see Doyle and Hic-
key, 1976; Drinnan et aI., 1994; Endress, 1994b; Hickey and
Taylor, 1996; Taylor and Hickey, 1990,1992,1993). According
to this idea, the earliest angiosperms are considered to be
riparian weeds having small flowers with few parts. One
argument for this is that such flowers occupy a large part of
the earliest fossil record (Crane et aI., 1994, 1995; Crepet and
Nixon, 1996; Dilcher,1979; Endress and Friis, 1994; Friis and
Endress, 1990; Friis et aI., 1994; Hickey and Taylor, 1996; Qiu
et aI., 1993; Taylor and Hickey, 1990). Also rRNA sequence
data place the paleoherbs with Nymphaeales in a basal
position (see Doyle, 1994; Doyle et al., 1994). However, the
paleoherbs have been variously circumscribed (Table 1),
sometimes including taxa such as the monocotyledons and
Chloranthaceae, or excluding them. Also the description of
"primitive" paleoherbs tends to be disputed among authors,
as some favour small trimerous flowers with few parts as
ancestral (such as Saruma of the Aristolochiaceae, Cabomba of
the Cabombaceae, or Acarus of the monocotyledons), while
other interpretations of early angiosperms are based on
strongly "reduced" flowers (such as Piperales, Chloranthales:
e.g. Hickey and Taylor, 1996; Les et al., 1996), favouring an
origin such as postulated by Burger (1977, 1981) or Meeuse
(1986, and other works).
Endress and Friis (1994: 3) state that "it has become uncertain
whether the woody Magnoliales are at the base". However,
they admit that the abundance of small flowers may be a
reflection of rapid diversification, rather than reflecting the
basal floral organisation in angiosperms. The caveat for the
paleoherb hypothesis is the fact that smaller flowers can be
better preserved than massive flowers; wet habitats may also
be more "appropriate" for preservation. Indeed, the fossil
record must be approached very cautiously.
Other authors maintain that an androecium with many
stamens is primitive (see Leins and Erbar, 1991, 1994; Ronse
Decraene and Smets, 1993). Leins and Erbar (1991, 1994)
accepted the coexistence of fascicled and spiral androecia in
primitive angiosperms. They argued that a flower with a
variable number of fascicles may be primitive and that the
78 Bot. Acta 111 (1998)
number has become reduced and fixed to five in Paeonia. It is
then assumed that Paeonia is comparable to the spiral flower
of Magnolia, because the five primary stamen primordia arise
in a spiral sequence. The flower of Paeonia thus becomes an
essential link between the Magnoliidae and Dilleniidae. From
Paeonia-like or Magnolia-like androecial types one- or two-
whorled androecia (diplostemony and haplostemony) are
derived. We have criticized their 1991 interpretation in an
earlier paper (Ronse Decraene and Smets, 1992a) as we
believe that the opposite view (i.e. that fascicles may be
secondary) has as much raison d'etre and because we think
that the derivation of diplostemonous and haplostemonous
types, as proposed by Leins and Erbar, remains highly
complicated. In 1994 Leins and Erbar wrote that there is "a
secondary subdivision of only five, still spirally arranged,
androecial organs" in Paeonia (Leins and Erbar, 1994: 213).
However, we want to stress again that the androecium of
Paeonia is basically not much different from other cases with
few stamens, such as diplostemonous or haplostemonous
forms, because a spiral sequence is inherent to many flowers
and occurs also in the latter 1 (see Erbar and Leins,1985, 1988;
Ronse Decraene and Smets, 1995b). [f fascicled androecia
were primitive, then Paeonia can only be one of the proto-
types for diplostemonous flowers, when these are derived
from flowers with two whorls of fascicles, or when a number
of complicated side steps are included (building of an androecial
mound or ring wall with its partial reduction). Their concept
makes androecial evolution complicated, as fascicles would
first be formed by a subdivision of only five organs, as e.g. in
Paeonia, Stewartia or Garcinia, and would then undergo a
reduction to return to the original five stamens.
Referring to the emergence of major groups such as the
monocotyledons or basal "eudicots", cyclic flowers with a
relatively low number of parts are seen as basal (Drinnan et
al., 1994; Endress, 1995; Erbar and Leins, 1994), though the
number of stamens was probably relatively high (Ronse
Decraene and Smets, 1995a).
A Different Approach to the Evolution of the Androecium
The evolution of the androecium is the result of continuous
counterbalancing of reductions and secondary increases
(Fig.1). The presence of many stamens is either a secondary
phenomenon (complex or secondary polyandry with fascicled
or complex androecia, arising on common primordia, on a
ring wall or on other meristematic tissue), or a basic feature
(e.g. spiral polyandry, whorled polyandry or polycycly, chaotic
polyandry). The presence offew stamens has to be interpreted
likewise; it is either basic (resulting in higher numbers by
increase), or it is derived (by reduction from higher numbers).
As this idea is accepted by most researchers nowadays, a good
framework for approaching the differences between few and
many needs to be elaborated.
As for all characters it is important to rely on homologous
data to understand patterns of androecial evolution. Develop-
mental evidence can help to provide these data for evaluating
1 We want to rectify a statement made in our 1992 a paper, where we
erroneously wrote that Leins and Erbar "overlooked" the importance
of the spiral arrangement of the fascicles, while we wanted to stress
the opposite, viz. that they "overemphasized" the importance of it.
Leins and Erbar (1994: 216) were right to point to that inconsistency.
L. P. Ronse Decraene and E. F. Smets
potential homologies among different floral configurations
(cf. Drinnan et al., 1994). As written elsewhere (Ronse
Decraene and Smets, 1987,1993, 1995b, 1996) we proposed to
use two characters, each with a number of character states,
for circumscribing the architecture of the androecium, viz.
polymery and oligomery. We must stress that the characters
do not refer to structures, but to patterns. These two charac-
ters stand for two groups of ontogenetic patterns, which are
partially homologous. In this sense the oligomerous patterns
are derived from a polymerous pattern at one point. The
distinction between the occurrence of the polymerous and
the oligomerous patterns roughly corresponds with two
different "blocks" of angiosperms, without being necessarily a
reflection of two clearcut phylogenetic groups. At first glance
the terms polymery and oligomery may appear as superfluous
or even confusing. Our use of the terms oligomery and
polymery should not be mixed up with oligandry and poly-
andry, as polymery is not equivalent to many stamens and
oligomery is not equivalent to few. The terms we use can be
interpreted phylogenetically as two different generalized
androecial lines of evolution, one with originally many
stamens and the other with originally fewer stamens. Each
character can be subdivided in a number of character states
that we have presented in a semophyletic scheme (see Fig. 1).
Ontogenetic evidence can help to discover each of these
character states. However, the distinction between different
character states of a character can be blurred as "character
states of the same character are homologous [ I but they may
vary quantitatively" (Smets and Cresens, 1988: 122). The
boundaries between the character states reflect the existence
of configurations that we want to emphasize for practical
reasons. We can illustrate this for polycycly (whorled poly-
andry). Polycycly comprises many different configurations of
the stamens (e.g. in pairs or single, with many or fewer
whorls). Shifts between these configurations can be under-
stood as gradual or continuous variations. We could also have
recognized an extra step for androecia with five whorls (viz.
pentacycly). However, we did not do this for practical reasons
(rarity and unstability of the character state). Moreover,
within the concept of polymery "spiral" flowers often only
exist as conceived in our mind, as there are constant shuffles
to and from whorled and unordered patterns (see also End-
ress, 1994a; Figs. 1,2). However, within well settled limits it is
possible to identify existing patterns as expressions of one
and the same configuration. As the number of stamens
decreases, stamen insertion becomes more fixed and clearer
"types" can be recognized. Indeed, the formation of regular,
polycyclic flowers is a prerequisite for a further loss of whorls
(Fig. 1). A pair of characters analogous to the duality oligo-
mery - polyrnery exists in the recognition of major evolutio-
nary lines based on chemical markers (see Gottlieb et al.,
1993; Kubitzki and Gottlieb, 1984a, b; Kubitzki, 1993);
Magnoliidae, Caryophyllidae and monocotyledons contain
secondary metabolites originating from a fully expanded
shikimate pathway; Hamamelidae, Dilleniidae, and Rosidae
only possess intermediate products from a truncated shiki-
mate pathway, and the Asteridae are further derived by a near
exclusion of the shikimate pathway and its substitution by
acetate and mevalonate as intermediates. The branching of a
generalized shikimate pathway thus gave rise to a whole
group of different chemical substances.
 ..~ --
Evolution of the Androecium Bot. Acta 111 (1998) 79
--------
POLYMERY Fig.1 Semophyletic scheme representing
OLiGOMERY the progressive reduction of the androe-
dum of the angiosperms. White arrows
point to major steps within a character:
black arrows point to bridges between
oligomery and polymery. The distinction
between the inner and outer perianth
whorlsas well as inner and outer stamens is
shown by the white and black curves and
dots. respectively.

~o~~
~ ~ ~)
(;~
diplostemony obdiplostemony
~ ::!'-. ~

@)
haplostemony
~
obhaplostemony
g
1 stamen 1 stamen

~
r~o
<:»
obmonocycly
~
1 stamen

Floral ontogenetic studies are important as: (1) they present a
plausible alternative to overcome preconceived barriers be-
tween many and few stamens. as if a condition with "many"
stamens is always homologous and conditions with few
stamens are always homologous; and (2) the importance of
the position of individual stamens in the flower is recognized.
and the consequences of their initiation related to each other
and to the other organs. Moreover. as homologous patterns
can be predicted on the basis of floral ontogenetic studies a
typological framework can be constructed. viz. the ontogeny
emphasizes the distinction between polymery and oligomery.
Finally. these characteristics of androecial arrangement can
be used in phylogenetic studies.
IsSpiral Polyandry Primitive?
The question of the primitive androecium is still disputed. We
believe that spiral polyandry represents a basic feature in the
evolution of the androecium. One cannot ascertain. however,
that it stands for the most primitive condition (see previous
and Endress, 1994a). as the fossil record yields numerous
flower types indiscriminatively, and spiral polyandry is only
80 Bot. Acta 111 (1998) L. P. Ronse Decraene and E. F. Smets

Fig.2 Example of a polycyclic

dimerous flower: Macleaya cor-
data (Mill.) R. Br. (Papaver-
aceae). Black and white dots
show alternating orthostichies
of alternating hexamerous
"whorls". Note the tendency to
form parastichies at the base of
the androecium; sepals remov-
ed. Bar = 100 urn,
Fig.3 Example of chaotic po-
lyandry: Drimys winteri J. R. & G.
Forster (Winteraceae). Note the
irregular arrangement of sta-
mens and carpels without clear
parastichies; sepals removed:
Bar = 100 urn.
Fig.4 Myosurus minimus L.
(Ranunculaceae). Lateral view
of flower with a possible secon-
dary increase of the number of
carpels by an extension of the
ontogenetic spiral (the same
could be applied for the an-
droecium). Note that the outer
stamens (s) have been trans-
formed into nectar leaves (k): c,
sepal.
Fig.5 Pseudodiplostemonous
androecium: Phytolacca dode-
candia L. (Phytolaccaceae).
Numbers give the position of
the stamen primordia relative
to the sepals. The arrow points
to a hidden tenth stamen; se-
pals removed: Bar = 100 urn,
Fig.6 Diplostemonous an-
droecium of Coriaria myrtifolia
L. (Coriariaceae). Note the regu-
lar alternation of whorls and
petal primordia (k) resembling
the stamens; c. sepals.
Fig.7 Unusual hexamerous
flower of Xanthorrhiza simp/ids-
sima Marsch. (Ranunculaceae).
Note the presence of five stami-
nodial petals (k), five stamens
(s) and one intermediate struc-
ture (arrow); six sepals (c) pre-
sent.

one of these (see Crane et aI., 1994, 1995; Dilcher, 1979; 1984). Moreover, spiral phyllotaxis is less common in extant
Endress and Friis, 1994; Friis and Endress, 1990). Unequivocal Magnoliidae than originally believed, as an irregular or
Magnolia-like flowers date from the mid-Cretaceous (Crane et whorled phyllotaxis may be equally common. Spiral poly-
aI., 1994; Crepet and Nixon. 1994. 1996; Dilcher and Crane, andry represents only one case in the wide array of androecial
Evolution of the Androecium
Table 1 Different delimitations of the paleoherbs.
Author Aristolo- Piper- Saurur- Nymphae-
chiaceae aceae aceae aceae
Loconte and + + + +
Stevenson, 1991
Loconte, 1996 + + + +
Endress, 1994b + + + +
Qiu et aI., 1993 + + + +
Donoghue and + + + +
Doyle, 1989
Doyle et al., 1994 + + + +
Taylor and Hickey, + + + +
1992
Hickey and Taylor, + + + +
1996
configurations (see Endress, 1986, 1987a, 1990, 1994a). The
fact that a spiral can be easily turned into a whorl or an
unordered arrangement does not reduce its importance as a
basic configuration. A spiral flower inception does not differ
from the common inception of vegetative parts on a stem.
Moreover, the limits between different floral parts are vague
and the flower may easily transgress into the vegetative parts
through a variable number of phyllomes.
Spiral polyandry is limited to the Magnoliidae, Ranunculidae
and Rosidae.There is no unequivocal evidence for a secondary
origin of spiral flowers from whorled or chaotic precursors,
only a tendency for intergrading. The fact that Ceratophyllum
has spiral and whorled staminate flowers in equal proportions
(Endress, 1994c) does not clarify which is the most primitive.
Takhtajan (1991) assumes that the general direction of evolu-
tion is from a spiral to a whorled arrangement, but that
reversals are possible. As discussed previously (Ronse De-
craene and Smets, 1993), a spiral flower remains on structural
grounds the best starting point for considering androecial
evolution. Still, another possibility for a starting point are
androecia with an unordered (chaotic) inception, as in the
Winteraceae (Figs. 1, 3; Endress, 1990, 1994a; Erbar and Leins,
1983; Gottsberger, 1988). But where is the difference between
a chaotic initiation and a modified spiral? However, cladistic
analyses of molecular and morphological data do not place
the Winteraceae as the basalmost lineage (Chase et aI., 1993;
Doyle, 1994; Doyle et aI., 1994). On the contrary, Donoghue
and Doyle (1989) identified the Magnoliales as the basalmost
lineage of angiosperms in a cladistic study of mostly morpho-
logical characters. Moreover, it is not excluded that certain
spirals are further elaborations of cases with fewer stamens
(Fig.4; cfTakhtajan, 1991; Crepetand Nixon,1996).
Crepet and Nixon (1996) considered the primitive stamen
number to be relatively low and without division of labour,
i.e, attraction and rewards being simultaneously presented by
the stamens. An elaboration with division of labour in
nectaries and petals would necessitate a higher number of
stamens and thus an increase in the number of spirally
arranged stamens, or duplication of stamen cycles. To us such
Bot. Acta 111 (1998) 81
Cabomb- Lactorid- Ceratophyl- monocoty- Chloranth- Nelumbon-
aceae aceae laceae ledons aceae aceae
+ + +
+ + + +
+ + + H
(+)
+ + +
+ ? + +
+ + +
+ + + +
an increase is unlikely, as a transformation of parts (homeosis
or any other process) is genetically more easily obtained than
a necessary addition of structures. The development of petals
requires the transformation of few outer stamens (e.g.
Ranunculaceae, Figs.4, 7) or tepals (e.g. Paeoniaceae), while
the development of nectaries may be combined with the
petals, or be independent of it.
There is more difficulty for visually deriving the elaborate
spiral flower of Magnoliids from oligandrous types (e.g.
Paleoherbs ). Taking the Paleoherbs as the ancestral group for
the angiosperms leads inevitably to a number of difficulties 2.
For example, deriving androecia with many stamens inserted
in a regular, rhythmic sequence becomes difficult, especially
when starting from oligandrous taxa, such as Lactoris (Lacto-
ridaceae), Cabomba (Cabombaceae), Saruma (Aristolochia-
ceae), Chloranthaceae, Piperaceae or Saururaceae. One has to
assume the de novo origin of structures, transitional steps
with increases of stamens and stamen whorls, fusions of
different flowers into larger units, etc. Evidence for these
trends is difficult to find in extant plants, contrary to an
assumption of the opposite. For example, Ito (1986) could
easily discuss on floral anatomical grounds how the simple
flower of Cabomba may be derived from a more complex
Brasenia flower type by decrease in the number of stamens
and carpels. The opposite would be more difficult. Ceratophyl-
lum tends to fall outside this discussion, as the androecium of
male flowers has few to numerous stamens arranged in a
spiral or whorls (Endress, 1994c). This does not contradict the
basal position of the Ceratophyllaceae in the molecular
phylogeny of the angiosperms (Chase et aI., 1993; Crane et al.,
1995; Qiu et al., 1993). Aristolochiaceae, Nymphaeaceae,
Saururaceae and Cabombaceae have trimerous or dimerous
2 The Paleoherbs tend to diverge in two groups, considering their floral
symmetry and ontogeny (Tucker and Douglas, 1996; Endress,1994b).
The group is probably not monophyletic. Also the delimitation of
Paleoherbs is rather confusing (see Table 1). Loconte (1996) argued
that rooting of the angiosperms among the Paleoherbs would
necessitate important transformations in nearly all commonly
accepted character states.
82 Bot. Acta 111 (1998)
flowers with paired outer or firstly formed stamens (replaced
by petals in the Nymphaeaceae), but these are undoubtedly
derived from a higher number of whorls (except in some
Nymphaeaceae and Nelumbo, with a possible secondary
increase: Moseley and Uhl, 1985; Schneider, 1976).
Another group that has been presented as the earliest
angiosperms are the Chloranthaceae, as they are present
among the oldest fossil evidence (see Herendeen et aI., 1993
and Crepet and Nixon, 1996 for an overview). The trilobed
stamen of Chloranthus represents a controversial topic for
discussing the evolution of the androecium. Rohwer (1994)
pointed to the similarity between the trilobed Chloranthus
stamen and stamen appendages of the Lauraceae and hypo-
thesized that stamen fascicles are primitive for the Lauraceae
and even for the whole of the angiosperms (cI. Leins and
Erbar, 1991, 1994). On the other hand, there is evidence for
considering the appendages of Lauraceae (Laurales) as secon-
dary elaborations of the stamen flanks (see Endress, 1980).
The case of Chloranthus is controversial: either a trilobed
structure is primitive and cases without lobes are derived by
reduction (e.g. Sarcandra), or simple stamens, as in Sarcandra,
are primitive and a Chloranthus-like stamen is either derived
by fusion of three Sarcandra-like stamens (Crane et aI., 1989),
by polymerisation, or by partitioning of one Sarcandra-like
stamen (Endress, 1987b). The discovery of lower Cretaceous
Chloranthoid stamens with two thecae on each of the three
lobes, in contrast to the single theca on the lateral lobes of
extant Chloranthus tends to support the latter interpretation.
Moreover, to derive a complex flower from the simplified
Chloranthus flower demands hypotheses of aggregations of
individual flowers (cI. Burger, 1977, 1981; Hickey and Taylor,
1996; see also Endress, 1994b), and evidence for this is
limited. Also, Chloranthaceae are placed as relatively advanc-
ed on different trees, suggesting that their simple flowers are
reduced (Chase et al., 1993; Donoghue and Doyle, 1989; Doyle,
1994; Doyle et al.,1994; Loconte and Stevenson, 1991; Lo-
conte, 1996; Tucker and Douglas, 1996).
Derivations from Spiral Polyandry: the Importance of
Stamen Pairs
Multistaminate androecia consisting of numerous alternating
whorls often have alternating stamens in paired and unpaired
positions. In our opinion, the derivative model proposed by
Erbar and Leins (1981, 1994; Erbar, 1988) represents a major
trend in androecium evolution. These authors stress the fact
that trimerous flowers with three outer stamen pairs and a
variable number of intermediate whorls can be derived from
spiral flowers by repetitive breaks in the ontogenetic spiral of
stamens and carpels and space restrictions caused by the
larger size of the fewer perianth parts. Erbar and Leins restrict
their model to trimerous flowers and limit their analysis of
the androecium to the outer stamen pairs. However, it is also
important to extend this model (we called it polycycly) to
dimerous and pentamerous flowers, and to consider upper
whorls with paired and unpaired stamens as well (Fig.2; see
Ronse Decraene and Smets, 1990a, b, 1993,1994,1996). Dime-
rous flowers seem to have as great a distribution as trimerous
flowers and are frequently related to numerous alternating
whorls (Ronse Decraene and Smets, 1993, 1996). We believe
that the presence of paired stamens in upper whorls is not
incidental or the result of doubling, but is a basic condition
(see also Ronse Decraene and Smets, 1996). The importance of
L. P. Ronse Decraeneand E. F. Smets
stamen pairs in the phylogeny of the androecium is also
expressed by the presence of lauraceous fossil flowers with
stamen pairs (Crane et aI., 1994).
We must realize that in polycyclic flowers not only the outer
stamen pairs represent a regular arrangement in the flower,
but upper whorls also arise in a fixed sequence (i.e. an
alternation of whorls of three and six organs in trimerous
flowers, an alternation of whorls of four and two organs in
dimerous flowers, and intermediate situations in pentame-
rous flowers; Fig. 2). This regularity can in some cases be
disturbed by occasional doublings of stamen positions or a
secondary addition of the number of stamens correlated with
their smaller size (Ronse Decraene and Smets, 1996). In other
instances the centripetal initiation of whorls tends to be
reversed, as in the Aristolochiaceae (Leins and Erbar, 1985,
1995; Leins et al., 1988; Tucker and Douglas, 1996), Phytolac-
caceae (Hofmann, 1993; Ronse Decraene and Smets, 1991;
Ronse Decraene et al., 1997) or Capparaceae (Ronse Decraene
and Smets, 1997). In many cases the regular pattern decreases
in upper whorls of the androecium or gynoecium as space
becomes more limited and the influence of the perianth
insertion is less clear (e.g. in Annonaceae: Ronse Decraene
and Smets, 1990a). Trimerous and dimerous polycyclic flow-
ers represent almost equivalent arrangements. Dimery has
been derived from trimery (as is probably the case for
Ranunculaceae, Berberidaceae and Papaveraceae), has arisen
independently, or was derived from pentamery (as in Phyto-
laccaceae: cI. Ronse Decraene and Smets, 1991,1994).
By the progressive loss of upper whorls, the number of cycles
diminishes and tends to attain an intermediate level, which
we described as tetracycly and tricycly (Ronse Decraene and
Smets, 1993; other appellations could be "tetrastemony" and
"tristemony").
These conditions can be much variable and, as for polycycly,
depend on whether pairs or single stamens occur in a given
whorl. For example, there are five concrete possibilities for a
trimerous flower with three stamen whorls considering that
stamen pairs are preferentially situated on the outer limits of
the flower (6+6+6,6+6+3,6+3+6,6+3+3,3+3+3). We
have not encountered the first cases (viz. 6 + 6 + 6,6 + 6 + 3) in
the literature, probably because of space restrictions for a
repetitive sequence of hexamerous whorls. 6 + 3 + 6 exists in
such sequence, but with more inner stamens (e.g. Sagittaria
sp.), though most often there is the insertion of an extra whorl
of three stamens in between (6 + 3 + 3 + 6 + ..., see Ronse
Decraene and Smets, 1995a). 6 + 3 + 3 occurs more frequently,
as in Asarum (Aristolochiaceae, though the initiation of
stamens is centrifugal: see Leins and Erbar, 1985; Leins et aI.,
1988), Stratiotes (Hydrocharitaceae), Echinodorus and Ranalis-
rna (Alismataceae). 3 + 3 + 3 is also found, as in Elodea (Hydro-
charitaceae), Pseudosmilax (Smilacaceae), Lindera (Lauraceae)
or Disciphania (Lardizabalaceae). As a rule, the innermost
paired stamens tend to interchange with single stamens
before the outer paired stamens are affected.
In several instances the outer paired stamens become replac-
ed by petals. This may be explained as a case of homeosis, as
in Actaea (Ranunculaceae) and Sanguinaria (Papaveraceae)
(Lehmann and Sattler, 1993,1994); in Madeaya the homeotic
process replaces petals by stamens (Ronse Decraene and
Smets, 1990b; Fig.2); this may also be the case in Myosurus
Evolution of the Androecium
(Fig.4). Indeed, the existence of staminodial petals is a hypo-
thesis that tends to be supported in several groups of plants.
The reduction of an inner whorl in a trimerous or dimerous
flower with three stamen whorls leads to a widespread and
stable condition that we described as dicycly (Fig. I). Outer
stamens are originally inserted in pairs, but very often single
stamens replace the pair; the case with single outer stamens
and paired inner stamens has obviously not been observed.
Evidence for a one way shift between pairs and single
stamens is supported by many examples (e.g. Polygonaceae:
Ronse Decraene and Smets, 1993; Cabombaceae: Moseleyet
al., 1984; Fumariaceae: Ronse Decraene and Smets, 1992b;
Buxaceae: Van Tieghem, 1897). The switch between paired
stamens and single stamens can be observed as a lateral
fusion, as in Hypecoum (Ronse Decraene and Smets, 1992b,
1996), though this interpretation has not been accepted
unanimously for the Fumariaceae by authors who favour a
process of splitting (e.g. Drinnan et al., 1994; Kadereit et al.,
1994). In other instances, a single stamen replaces the pair in
a closely related species.
The further loss of a stamen whorl leads to androecia of one
whorl, which we termed monocycly or obmonocycly, depend-
ing on the position of the remaining stamens. Interestingly,
paired stamens may still be present, as in Rumex (Poly-
gonacceae) or Meconella (Papaveraceae), though these are
most often replaced by single stamens (see also Ronse
Decraene and Smets,1993).
Multiple Derivations of Diplostemonous Androecia
We have discussed the derivation of two-whorled androecia
(dicycly) from trimerous or dimerous prototypes with a
tepaline perianth. However, it is important to recognize that
two-whorled androecia (diplostemony, dicycly,or whatever it
is called) are not necessarily homologous, because androecia
with two stamen whorls that are associated with pentame-
rous petaliferous flowers are highly different in ontogeny and
architecture. Pentamerous flowers that have traditionally
been described as diplostemonous can be derived ontogene-
tically from different configurations and are therefore not
homologous (Figs. 5 -7). As discussed elsewhere (Ronse De-
craene and Smets, 1993, 1995b), we believe that certain
configurations that were described as diplostemony in the
past have in fact arisen independently and should be seen as
cases of pseudodiplostemony that can be traced back to a
polymerous form (see Ronse Decraene and Smets, 1993;
Ronse Decraene et al., 1997). Indeed, the transition from a
trimerous to a pentamerous flower, together with the sterili-
sation of the outer stamen whorl into petals has led to the
arrangement of two whorls of stamens comparable to a
diplostemonous flower. The following examples show the
divergence between "diplostemonous androecia":
(1) In the Caryophyllidae there are sufficient indications for
postulating an independent origin from multistaminate pro-
totypes with paired and unpaired stamens (see also Ronse
Decraene and Smets, 1993; Ronse Decraene et al., 1997;
unpubl. obs.). For example, in Phytolacca dodecandra (Fig. 5)
with an apparently diplostemonous androecium the stamens
arise in the following order: two stamen pairs opposite sepals
one and two, a single stamen between sepals three and five,
single stamens opposite sepals three, four and five in variable
Bot. Acta 111 83
sequence, and finally single externally placed stamens oppo-
site sepals one and two. In other words, diplostemony as
conceived in other groups of plants is different and certainly
not basic in the Centrospermae.
(2) The majority of dicots have diplostemonous androecia
arising mainly as a regular alternation of pentamerous whorls
(with stamens arising simultaneously or sequentially within
each whorl) (Fig. 6).
(3) The case of pentamerous Ranunculaceae with an alterna-
tion of numerous whorls (polycycly, for which Aquilegia
stands as a model) may well be a prototype in the derivation
of diplostemony. In Aquilegia there are numerous whorls of
five stamens, clearly alternating with each other and forming
ten orthostichies (see Tepfer, 1953; Endress, 1987a: Fig.2a,
2b). Some taxa have androecia approaching a diplostemonous
or haplostemonous condition (e.g. Xanthorrhiza, Fig.7), but
the number of parts is often unstable.
As we have repeatedly suggested (see Ronse Decraene and
Smets, 1993, 1995b), we believe a semophyletic series,
running from many stamens inserted in a spiral (eventually
interchangeable with a chaotic arrangement or with trime-
rous/dimerous whorls) to fewer stamens in a low number of
whorls, to be the main trend in the phylogeny of the
androecium (see Fig. 1). The derivation of an essentially
pentamerous evolutionary line with two stamen whorls
should be seen as a side step on this evolutionary line. The
switch of a trimerous flower having four stamen whorls
(tetracycly, or with one whorl more than in the pentamerous
condition) into a pentamerous flower with three stamen
whorls (tricycly, or with one whorl less than the trimerous
condition) is seen as an essential step in the derivation of this
line. The outer whorl, viz. the petals, has mostly a staminodial
origin in the oligomerous line (Fig.6), although this is not
evident for several taxa (e.g. Theaceae, Flacourtiaceae, Clusia-
ceae, Myrtaceae).
The fact that basic entities can be recognized ontogenetically
by their floral configuration and androecium is of greater
necessity Given the Widespread occurrence of diplostemony
in many "derived" angiosperms (eudicots), phylogenetic shifts
have mainly caused the loss of the antepetalous stamen whorl
(haplostemony), as this led to a stable configuration. Obha-
plostemony occurs less frequently, perhaps because of a lack
of harmony in the floral symmetry, as the alternation of
whorls is not respected. Obdiplostemony is mainly an inter-
mediate condition in the transition between diplostemony
and haplostemony, or less frequently in the transition be-
tween diplostemony and obhaplostemony. For more details
we refer to Ronse Decraene and Smets (1995b).
We originally included "complex polyandry" and "cyclic poly-
andry" (as in the Rosaceae) as character states of oligomery,
as well as "secondary polyandry" in polymery (cf Ronse
Decraene and Smets, 1987). This would define three indepen-
dent processes for a secondary increase. However, later
research indicated that all cases of secondary increase should
fall under the same denominative of complex polyandry (see
Ronse Decraene and Srnets, 1992a, 1993, 1995a, b). Complex
polyandry can be generated at any level by a subdivision of
primordia and has only limited taxonomic value as such (cf
Ronse Decraene and Smets, 1993,1995b).
84 Bot. Acta 111 (1998)
Conclusions
We have demonstrated that the existence of ontogenetic
patterns of androecium development can be translated in a
phylogenetic sequence. In earlier publications we have also
emphasized that the distinction between polymery and
oligomery corresponds more or less with a split between a
polymerous and an oligomerous line (see Ronse Decraene and
Smets, 1987, 1993, 1995b, 1996). In polymerous taxa (such as
the Magnoliidae, Caryophyllidae, part of the Hamamelidae,
and monocotyledons) androecial evolution is essentially
marked by a reductive trend (although there are several
reversals), leading to shifts of stamens in pairs, reduction of
whorls and replacement of the pairs by single stamens; in
oligomerous taxa (such as the Dilleniidae, Rosidae, Asteridae,
and part of the Hamamelidae) a reductive trend has been
reversed many times, increasing the number of stamens in
the flower, and offering greater rewards to visiting insects and
new possibilities for floral evolution 3. Similar trends can also
be found - to a lesser extent - within the polymerous
alliance.
The proposed distinction corresponds to earlier divisions in
two major groups, as proposed by Kubitzki and Gottlieb
(1984a, b) and Huber (1982), and is supported by phyto-
chemical (Kubitzki and Gottlieb, 1984a, b; Kubitzki, 1993), as
well as evidence of epicuticular waxes (Barthlott, 1990). Apart
from such taxa such as the lower eudicots and CaryophyIIids,
it is also roughly reflected in the rbcl tree of Chase et al.
(1993) who obtained a split between two major groups that
are characterized by different pollen types (monosulcate and
monosulcate-derived versus tricolpate and tricolpate-deri-
ved).
Before definite answers can be proposed a more in-depth
analysis of different molecular data sets should be performed;
they should be compared with morphological data sets
(including ontogenetic data to a rising degree), and finally be
combined with them, as different answers remain possible.
One of the most important shortcomings of phylogenetic
systematics remains the definition and identification of
homologous patterns and features. For the androecial arran-
gement, we hope that our proposal is a step in the right
direction.
Acknowledgements
We wish to express our thanks to the Flemish Fund for
Scientific Research (F. W.O.) for financial support (project W
2.0038.91, Scanning electron microscopy and project W
G.0143.95, General research project). We are grateful to Mr.
Gert Ausloos for initiating us into the art of computer graphics
and to Jan De Laet for fruitful comments on the manuscript.
We acknowledge the constructive comments of an anony-
mous reviewer. The first author is a postdoctoral fellow of the
F. W. O.
3 Complex polyandry has arisen many times within the oligomerous
line. Different trends have been recognized in relation to the
availabilityof space in the flower, the floral shape and the number of
stamen whorls (see RonseDecraene and Smets, 1992a).ln most cases
the polyandrous form can be connected to a diplostemonous or
(ob)haplostemonous framework. For a different view, see Leins
(1979)and Leins and Erbar(1991,1994).
L. P. Ronse Decraene and E. F. Smets
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