7
Evolution of the palm androecium
as revealed by character mapping
on a supertree
Sophie Nadot, Julie Sannier , Anders Barfod and
William J. Baker
7.1 Introduction
Over the last two decades, our insight into the phylogenetic relationships among
groups of living organisms has increased signiicantly (see, for example, the Tree
of Life Project, Maddison et al., 2007). Since the i rst burst in phylogenetic analyses
occurred in the early nineties triggered by the discovery of the PCR technique
(Saiki et al., 1988), constant improvements in laboratory techniques have made it
easier to reveal patterns of molecular variation across organisms (e.g. McCombie
et al., 1992; Ronaghi, 2001). At the same time, computer power, access to online
data and analytical tools have rapidly improved (see, for example, Guindon et al.,
2003 and 2005). he most popular methods are based on most parsimonious
reconstructions (MP) or Bayesian inference (BI), the latter allowing for molecular dating and therefore gaining in popularity (Huelsenbeck and Ronquist, 2001;
Ronquist and Huelsenbeck, 2003). he methods have been implemented in userfriendly software such as MacClade (Maddison and Maddison, 2001), Bayestraits
(available from http://www.evolution.rdg.ac.uk/BayesTraits.html, see also Pagel,
1999; Pagel et al., 2004) and the more recently developed Mesquite (Maddison and
Flowers on the Tree of Life, ed. Livia Wanntorp and Louis P. Ronse De Craene. Published
by Cambridge University Press. © The Systematics Association 2011.
E VO LU T I O N O F T HE PA L M A N D RO ECIU M
Maddison, 2009). As a consequence of these recent developments a large number
of robust and highly resolved phylogenies are now available for various taxonomic
levels, providing excellent frameworks for exploring character evolution through
space and time.
he palms (Arecaceae or Palmae) are an iconic family of lowering plants comprising around 2400 species distributed worldwide. Palms constitute a highly
distinctive component of tropical rain forests and often have major ecological
impacts in the plant communities where they occur. At the same time they are
of immense economic signiicance, both at the international level (e.g. oil palm,
date palm, coconut, rattan) and at the village level, where they provide shelter and
food. Research interest in the palm family has greatly increased in the last three
decades. he results have recently been synthesized into a monograph, which
describes the morphology, ecology and geographical distribution of all palm genera (Dransield et al., 2008a). Several authors have contributed to unravelling the
relationships among genera in the family (Asmussen and Chase, 2001; Hahn, 2002;
Lewis and Doyle, 2002; Asmussen et al., 2006). he results have been summarized
in a robust and comprehensive supertree phylogeny by Baker et al. (2009), including all genera of the family but the newly discovered Tahina (Dransield et al.,
2008b). h is represents an excellent opportunity for studying evolutionary trends
in morphological and ecological traits.
Palm lowers are usually small and trimerous, with a perianth typically consisting of three sepals and three petals. hey are actinomorphic to slightly asymmetric and usually rather inconspicuous. However, in other features there is wide
variation. h is applies particularly to loral arrangement, sexual expression in
space (hermaphroditism versus monoecy, dioecy or polygamy) and time (dichogamy), as well as number, size and synorganization of loral organs. he androecium, which we will focus on here, typically includes six stamens, but this number
can be reduced to three, like Nypa Wurmb (lowers with a single stamen have
been observed in Dypsis lantzeana Baill.: Rudall et al., 2003), it can vary between
6 and 12 in a more or less stable manner, like Roystonea O.F.Cook, or it may attain
very high numbers, such as tribe Phytelepheae (subfamily Ceroxyloideae), where
hundreds of stamens are packed together tightly on the loral apex (Fig 7.1). In
some species with unisexual lowers, noticeable diferences in number, size and
shape exist between the functional androecium of the male lower and the sterile androecium of the pistillate lower (Fig 7.1). he ontogenetic development of
selected polyandrous palm species has been studied by Barfod and Uhl (2001),
Uhl (1976), Uhl and Moore (1977), Uhl and Moore (1980) and Uhl and Dransield
(1984). Other studies concerned with the palm androecium have focused on
anther attachment and dehiscence, pollen wall ornamentation and pollen aperture type (Harley, 1999; Harley and Baker, 2001), as well as microsporogenesis
(Sannier et al., 2006).
157
158
FLOWERS ON THE TREE OF LIFE
(A)
(B)
(C)
(D)
Fig 7.1 Various lower morphologies in palms. (A) Hermaphroditic lower of Licuala
peltata (tribe Trachycarpeae, subfam. Coryphoideae) with six stamens. (B) Male lower
of Howea balmoreana (tribe Areceae, subfam. Arecoideae) with approximately 30 to 50
stamens. (C) Female lower of Howea balmoreana (only the three stigmas of the pistil are
visible, protruding from the lower; the three staminodes are not visible). (D) Male lower
of Aphandra natalia (tribe Phytelepheae, subfam. Ceroxyloideae) with approximately 500
stamens.
In this chapter we optimize characters relating to the palm androecium on the
recently published supertree by Baker et al. (2009). h is provides insights into the
role of stamen synorganization and morphology, in the diversiication of palms in
particular, and in monocots and lowering plants in general.
7.2 Materials and methods
7.2.1 Choice of characters and character coding
Table 7.1 shows the list of characters examined and the coding into discrete character states. All characters are related to the androecium except for ‘Petal connation’, which was recorded to enable a comparison with ‘Stamen connation’, petals
being the part of the perianth that is the closest to the androecium. All coding is
based on the information presented in the genus descriptions of Dransield et al.
(2008a). In most cases character variation was easily broken down into a limited
number of states. To avoid polymorphism the variation found for ‘Stamen connation’ and ‘Petal connation’ was coded using an additional character state that corresponds to the presence of two diferent states within the same genus. Dei ning
character states for stamen number proved to be problematic, both because of the
range of variation throughout the family (from three to hundreds) and because of
the range of variation within certain genera. We therefore chose to use a binary
coding for the character ‘Stamen number’, in which state 0 is oligandry (dei ned
here as six or less stamens) and state 1 is polyandry (more than six stamens). he
number six corresponds to twice the merism of all palm lowers. Stamen numbers
recorded for polyandrous genera are given in Table 7.2.
E VO LU T I O N O F T HE PA L M A N D RO ECIU M
Table 7.1 List of characters examined in this study. All characters were treated as discrete
and coded as such.
Characters
Character states
Characters examined for genera bearing bisexual or unisexual lowers
Stamen number
Oligandry (6 stamens or less) = 0; Polyandry = 1
Anther dehiscence
Latrorse = 0; Extrorse = 1; Introrse = 2
Anther attachment
Dorsiixed = 0; Basiixed = 1
Stamen connation
Free = 0; Connate = 1; Free or connate* = 2
Petal connation
Free = 0; Connate = 1; Free or connate* = 2;
Connate in one ring = 3
Stamen adnation (to petals)
Free = 0; Adnate = 1
Characters examined only for genera bearing unisexual lowers
Staminode number (female lowers)
versus functional stamen number
(male lowers)
Identical = 0; Different = 1; Lacking = 2
Pistillode in male lowers
Present = 0; Lacking = 1; Minute = 2
*Infrageneric variation
7.2.2 Phylogenetic background and character optimization
Optimization of androecium characters was performed on a recent supertree
of palms (Baker et al., 2009). It includes all genera accepted by Govaerts and
Dransield (2005) plus those recognized later by Baker et al. (2006) and Lewis
and Zona (2008). We slightly modiied the supertree (see Fig 3 in Baker et al.,
2009) by considering only accepted genera according to Dransield et al. (2008a).
he recently discovered genus Tahina J.Dransf. and Rakotoarin. (Dransield
et al., 2008b) was not included in this tree. he original supertree included an
outgroup of 13 genera of commelinid monocots from which we selected the
following six to include in our study: Anigozanthos Labill. (Haemodoraceae),
Tradescantia Ruppius ex L. (Commelinaceae), Costus L. (Costaceae), Dasypogon
R.Br. (Dasypogonaceae), Fargesia Franchet (Poaceae) and Vriesea Lindl.
(Bromeliaceae).
We used Maximum Parsimony (MP) for character optimization as implemented
in the Mesquite software package (Maddison and Maddison, 2009). he default
settings were used (character states were considered as unordered).
159
Table 7.2 Palm genera including at least one species producing polyandrous lowers (i.e. bearing more than six stamens). Genera in
which all species are polyandrous are in bold and the number of species (from www.palmweb.org) is indicated. Genera with unisexual
and strongly dimorphic lowers are marked with an asterisk. Genera including polyandrous species in which developmental studies have
been conducted are marked with a plus sign. First and second columns: subfamily and tribe according to Dransield et al. (2005). Data
were obtained from Dransield et al. (2008a) and from www.palmweb.org.
SUBFAMILY
Calamoideae
TRIBE
Eugeissoneae
Lepidocaryeae
Calameae
Coryphoideae Caryoteae
Borasseae
Cryosophileae
Phoeniceae
Genera including polyandrous
species
+
Eugeissona Griff. (6 sp)
Raphia P.Beauv.
Calamus L.
Korthalsia Blume
Plectocomia Mart. and Blume
Stamen number
Plant
Flowers
Inflorescence unisexual
unisexual (0); unisexual (0); (0); bisexual
bisexual (1) bisexual (1) (1)
20–70
6–30
6 (12 in C. ornatus)
6–9
Usually 6, rarely to 12
0/1
0
0
1
0
1
1
0
1
0
1
1
0
1
0
0
0/1
1
0
0
0
0
0
1
1
1
1
1
1
0
1
0
0
0
0
1
1
1
1
1
1
0
1
1
0
0
0
1
1
1
1
1
1
0
Rarely 6–9, usually
more than 15
6–100
Caryota+ L.
Wallichia Roxb.
3–15
Borassodendron Becc.
6–15
Latania Comm. ex Juss. (3 sp) 15–30 or more
Lodoicea+ Comm. ex DC. (1 sp) 17–22
Chelyocarpus Dammer
5–9
Coccothrinax Sarg.
9(6–13)
Hemithrinax Hook.f.
6–8
Itaya H.E.Moore (1 sp)
18–24
Thrinax L.f. ex Sw.
5–15
Zombia L.H.Bailey (1 sp)
9–12
Phoenix L.
Usually 6, rarely
3 or 9
Arenga Labill. ex DC.
SUBFAMILY
TRIBE
Ceroxyloideae Phytelepheae
Ceroxyleae
Arecoideae
Areceae
Stamen number
Plant
Flowers
Inflorescence unisexual
unisexual (0); unisexual (0); (0); bisexual
bisexual (1) bisexual (1) (1)
Ammandra O.F.Cook* (1 sp)
Aphandra+ Barfod* (1 sp)
Phytelephas+ Ruiz and Pav.*
(6 sp)
Ceroxylon+ Bonpl. ex DC.
300–1200
400–650
36–900
0
0
0
0
0
0
0
0
0
6–15(–17)
0
0
0
Acanthophoenix H.Wendl.
Actinokentia Dammer (2 sp)
Actinorhytis H.Wendl. and
Drude (1 sp)
Adonidia Becc. (1 sp)
Archontophoenix H.Wendl. and
Drude (6 sp)
Areca L.
6–12
19–50
24–33
0
0
0
1
1
1
1
1
1
45–50
12–14
0
0
1
1
1
1
3,6,9 or up to
30 or more
24–50
100–230
6–140
ca 33
19–55
6–12
9–15
6–9
Numerous, up to 19
0
1
1
0
0
0
0
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
24–320 or more
9–10(12)
0
0
1
1
1
1
6–36
0
1
1
Genera including polyandrous
species
+
Balaka Becc. (11 sp)
Brassiophoenix Burret (2 sp)
Calyptrocalyx Blume (26 sp)
Carpentaria Becc. (1 sp)
Chambeyronia Vieill. (2 sp)
Cyphokentia Brongn.
Cyrtostachys Blume (11 sp)
Deckenia H.Wendl. ex Seem.
Dransfieldia W.J.Baker and
Zona (1 sp)
Drymophloeus Zipp. (8 sp)
Hedyscepe H.Wendl. and
Drude (1 sp)
Heterospathe Scheff.
Table 7.2 (cont.)
SUBFAMILY
TRIBE
Genera including polyandrous
species
Howea Becc. (2 sp)
Hydriastele H.Wendl. and Drude
Kentiopsis Brongn. (4 sp)
Laccospadix H.Wendl.
and Drude (1 sp)
Lemurophoenix J.Dransf. (1 sp)
Linospadix H.Wendl.
Loxococcus H.Wendl.
and Drude (1 sp)
Nephrosperma Balf.f. (1 sp)
Normanbya F.Muell. ex Becc.
(1 sp)
Oncosperma Blume
Phoenicophorium H.Wendl.
(1 sp)
Pinanga Blume
Ponapea Becc. (3 sp)
Ptychococcus Becc. (2 sp)
Ptychosperma+ Labill. (29 sp)
Rhopaloblaste Scheff.
Solfia Rech. (1 sp)
Tectiphiala H.E.Moore
Veitchia H.Wendl. (8 sp)
Cocoseae
Wodyetia A.K.Irvine (1 sp)
Allagoptera Nees
Astrocaryum G.Mey.
Attalea Kunth
Stamen number
Plant
Flowers
Inflorescence unisexual
unisexual (0); unisexual (0); (0); bisexual
bisexual (1) bisexual (1) (1)
30–70 or more
6–24
11–38
9–12
0
0
0
0
1
1
1
1
1
1
1
1
52–59
6–12
12
0
0
0
1
1
1
1
1
1
40–50
24–40
0
0
1
1
1
1
6–9
15–18
0
0
1
1
1
1
Rarely 6, usually
12–68
Ca. 100
Up to 100
9–100 or more
6–9
35–37
6–7
Numerous to 100 or
more
60–71
6–100
(3–)6(–12)
3–75
0
1
1
0
0
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
0
0
0
0
1
1
1
0/1
1
1
0
1
SUBFAMILY
TRIBE
Genera including polyandrous
species
Bactris Jacq. ex Scop.
Beccariophoenix Jum. and
H.Perrier (2 sp)
Desmoncus Mart.
Jubaea Kunth (1 sp)
Jubaeopsis Becc. (1 sp)
Parajubaea Burret (3 sp)
Voanioala J.Dransf. (1 sp)
Euterpeae
Oenocarpus Mart.
Geonomateae
Asterogyne H.Wendl. ex Hook.f.
Geonoma Willd.
Welfia+ H.Wendl. (1 sp)
Iriartea Ruiz and Pav. (1 sp)
Iriarteeae
Socratea+ H.Karst. (5 sp)
Wettinia+ Poepp. ex Endl.
Manicaria Gaertn. (1 sp)
Manicarieae
Orania Zipp.
Oranieae
Reinhardtia Liebm. (6 sp)
Reinhardtieae
Roystonea O.F.Cook
Roystoneeae
Sclerospermeae Sclerosperma G.Mann and
H.Wendl. (3 sp)
Stamen number
Plant
Flowers
Inflorescence unisexual
unisexual (0); unisexual (0); (0); bisexual
bisexual (1) bisexual (1) (1)
(3–)6(–12)
15–21
0
0
1
1
1
1
6–9
18
(7-)8–16
13–15
12(–13)
6(7–8)9–20
6– c. 24
(3) 6(rarely more)
36(27–42)
9–20
17–145
6–20
30–35
3,4,6 or 9–32
8–140
6–12
60–100
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
164
FLOWERS ON THE TREE OF LIFE
7.3 Results
Figure 7.2 shows the MP optimization of the character ‘Stamen number’ on the palm
supertree. It strongly supports the widely accepted idea that six stamens represent
the ancestral state in palms. Ten genera include species in which the androecium is
reduced to three stamens (names followed by stars in Fig 7.2): Areca L., Astrocaryum
G.Mey., Attalea Kunth, Bactris Jacq. ex Scop., Dypsis Noronha ex Mart., Geonoma
Willd., Nypa Wurmb., Orania Zipp., Synechanthus H.Wendl. and Wallichia Roxb. In
the genera Areca and Orania, the number of stamens varies among species between
three and several dozen. Polyandrous lowers (with an androecium composed
of more than six stamens) have been recorded within 82 genera out of 183 (Table
7.2). Forty-ive of these genera produce exclusively polyandrous lowers (Table 7.2;
black rectangles in Fig 7.2), the remaining genera being polymorphic (grey boxes
in Fig 7.2). According to the optimization, polyandry has evolved numerous times
independently during the diversiication of palms, within all subfamilies except
Nypoideae. Due to the high number of polymorphic genera, it is diicult to identify
precisely the number of transitions towards polyandry. However, it can be noted
that the highest number of transitions, together with the widest range of variation
in terms of stamen number, occurs in Arecoideae, the largest subfamily, containing
about half of the species and genera recognized in the family.
Basii xed anthers represent the ancestral condition for the family as a whole
(optimization not shown) and for the subfamilies Calamoideae, Nypoideae and
Ceroxyloideae. Dorsii xed stamens evolved ive times within Calamoideae and
once in Ceroxyloideae; it represents the ancestral condition for the subfamilies
Coryphoideae and Arecoideae except the early diverging tribe Iriarteeae. In both
subfamilies there are reversals towards the basii xed condition in higher-order
branches. he vast majority of palm genera possess latrorse anthers that open by
longitudinal slits lateral to the i lament, which most probably represents the ancestral condition for the family. According to our optimization (not shown), introrse
anthers have evolved more than 20 times independently. It should be noticed that
this mode of dehiscence is synapomorphic for the Geonomateae + Manicarieae
clade.
Sixty-six or approx. one third of the genera include species with connate stamens. h is condition has evolved at least 29 times independently from ancestral free stamens, throughout all subfamilies (Fig 7.3). More than one third of
the genera with connate stamens belong to the Coryphoideae. he optimization
of petal connation shows that sympetaly is also derived (Fig 7.3). his character
state is a synapomorphy for the subfamilies Calamoideae and Coryphoideae, as
well as for a few genera within the Arecoideae. Several reversals towards free petals have occurred within Calamoideae and Coryphoideae. he single member
of Nypoideae, Nypa fruticans Wurmb, has the ancestral choripetalous corolla.
E VO LU T I O N O F T HE PA L M A N D RO ECIU M
Stamen and petal connation only partially co-occur throughout the palms, thus
several genera are either sympetalous or synandrous. In many genera with unisexual lowers, the degree of petal fusion difers between staminate and pistillate lowers. h is is the case in Ceroxyloideae, tribe Borasseae (in subfamily
Coryphoideae) and tribe Calameae (in subfamily Calamoideae). he optimization
furthermore indicates that stamens adnate to petals are ancestral in subfamily
Calamoideae and perhaps represent the original condition in palms overall. It is
considered a derived feature in most families of lowering plants. Adnation of stamens to petals is a synapomorphy for the tribes Trachycarpeae and Borasseae in
subfamily Coryphoideae, and for a clade within the Arecoideae which includes
Calyptronoma Griseb. + Calytrogyne H.Wendl. + Asterogyne H.Wendl. ex Hook.f. +
Geonoma Willd.
In genera with unisexual lowers we paid special attention to the diference
between the number of staminodes in female lowers and the number of stamens in male lowers respectively. Our results (Fig 7.4) show identical numbers
in the Calamoideae, and part of the Coryphoideae and Ceroxyloideae. Within the
Coryphoideae, the diference in the number of androecium parts is pronounced
in the tribes Borasseae + Caryoteae + Corypheae that form a clade. Within the
Ceroxyloideae the dioecious tribe Phytelepheae is characterized by a strong
dimorphism between male and female lowers and a more than tenfold diference
between functional stamens and staminodes in terms of number. In the Arecoideae
our optimization reveals an overall trend towards fewer staminodes relative to
the number of stamens. he presence of three staminodes in the female lowers is
characteristic of the clade composed of the Paciic subtribes Ptychospermatinae
+ Archontophoenicinae + Basseliniinae + Carpoxylinae + Clinospermatinae +
Linospadicinae + Loxococcus. he male lowers in these groups may have various
numbers of functional stamens, depending on the species. A staminodial ring is
found in subtribe Attaleinae, in which the number of stamens varies between 12
and 24.
We also optimized presence versus absence of sterile organs in genera with unisexual lowers (Fig 7.4) to check whether any trend in reduction of organs could
be detected. Most of the dioecious or monoecious genera have staminate lowers
with a pistillode and pistillate lowers with staminodes. Complete abortion of the
gynoecium occurs in 17 genera throughout the family and most likely evolved
from unisexual lowers with a pistillode. In several cases the character transformation passed through a transitional state, which involves a minute pistillode,
a state commonly found throughout the family. h is is the case for the [Salacca
Reinw. + Eleiodoxa (Becc.) Burret] clade in Calamoideae, for subtribe Rhapidinae
in Coryphoideae, for the [Phytelephas Ruiz and Pav. + Aphandra Barfod] clade in
Ceroxyloideae and for Howea in Arecoideae. Optimization of ‘Lack of staminodes’
showed that this character state evolved ten times independently.
165
(A)
Ceroxylon
Juania
Oraniopsis
Ravenea
Phytelephas
Aphandra
Ammandra
Pseudophoenix
Guihaia
Rhapis
Maxburretia
Rhapidophyllum
Trachycarpus
Chamaerops
Brahea
Johannesteijsmannia
Pholidocarpus
Pritchardiopsis
Licuala
Livistona
Acoelorraphe
Serenoa
Pritchardia
Copernicia
Washingtonia
Colpothrinax
Phoenix
Hemithrinax
Leucothrinax
Coccothrinax
Thrinax
Zombia
Schippia
Trithrinax
Chelyocarpus
Cryosophila
Itaya
Sabal
Borassodendron
Borassus
Lodoicea
Latania
Bismarckia
Satranala
Hyphaene
Medemia
Corypha
Arenga
Wallichia*
Caryota
Kerriodoxa
Nannorrhops
Chuniophoenix
Nypa*
Retispatha
Pogonotium
Daemonorops
Calamus
Ceratolobus
Pigafetta
Myrialepis
Plectocomiopsis
Plectocomia
Metroxylon
Salacca
Eleiodoxa
Korthalsia
Mauritia
Mauritiella
Lepidocaryum
Raphia
Laccosperma
Eremospatha
Oncocalamus
Eugeissona
Vriesea
Fargesia
Dasypogon
Costus
Tradescantia
Anigozanthos
Ceroxyleae
Phytelepheae
Cyclopatheae
Trachycarpeae
Phoeniceae
Cryosophileae
Sabaleae
Borasseae
Corypheae
Caryoteae
Chuniophoeniceae
NYPOIDEAE
Calameae
Lepidocaryeae
Eugeissoneae
OUTGROUPS
Fig 7.2 MP optimization of ‘Stamen number’ on the palm supertree. (a) all subfamilies
except Arecoideae. (b) Arecoideae (continuation of (a)). Upper left in (b): categories
(character states) dei ned here for the character. Branches are coloured according
to the inferred ancestral states. Boxes at the tip of branches correspond to the actual
observations. White = oligandry, Black = polyandry, Grey = infrageneric polymorphism
(oligandry + polyandry). Genera including species with three stamens only are indicated
by a star. Right hand side: tribe names according to Dransield et al. (2005).
E VO LU T I O N O F T HE PA L M A N D RO ECIU M
(B)
Stamen number
Oligandry (six or less stamens)
Polyandry (more than six stamens)
Both
Fig 7.2 (cont.)
Brassiophoenix
Drymophloeus
Ptychococcus
Carpentaria
Wodyetia
Normambya
Balaka
Solfia
Veitchia
Adonidia
Ponapea
Ptychosperma
Kentiopsis
Actinokentia
Archontophoenix
Chambeyronia
Actinorhytis
Calyptrocalyx
Burretiokentia
Cyphophoenix
Physokentia
Cyphosperma
Basselinia
Hedyscepe
Rhopalostylis
Lepidorrhachis
Howea
Laccospadix
Linospadix
Dransfieldia
Heterospathe
Clinosperma
Cyphokentia
Carpoxylon
Neoveitchia
Satakentia
Loxococcus
Pinanga
Nenga
Areca*
Bentinckia
Clinostigma
Cyrtostachys
Tectiphiala
Acanthophoenix
Deckenia
Oncosperma
Hydriastele
Dictyosperma
Rhopaloblaste
Lemurophoenix
Dypsis*
Marojejya
Masoala
Roscheria
Verschaffeltia
Nephrosperma
Phoenicophorium
Iguanura
Sommieria
Pelagodoxa
Neonicholsonia
Oenocarpus
Prestoea
Euterpe
Hyospathe
Calyptronoma
Calyptrogyne
Asterogyne
Geonoma*
Pholidostachys
Welfia
Manicaria
Leopoldinia
Sclerosperma
Orania
Podococcus
Allagoptera
Lytocaryum
Syagrus
Attalea*
Cocos
Parajubaea
Jubaea
Butia
Voanioala
Jubaeopsis
Beccariophoenix
Bactris*
Desmoncus
Astrocaryum*
Aiphanes
Acrocomia
Elaeis
Barcella
Reinhardtia
Roystonea
Chamaedorea
Gaussia
Wendlandiella
Synechanthus*
Hyophorbe
Wettinia
Iriartella
Dictyocaryum
Socratea
Iriartea
Areceae
Pelagodoxeae
Euterpeae
Geonomateae
Manicarieae
Leopoldinieae
Sclerospermeae
Oranieae
Podococceae
Cocoseae
Rheinardtieae
Roystoneae
Chamaedoreae
Iriarteeae
167
168
FLOWERS ON THE TREE OF LIFE
(A)
Arecoideae (fig. 7.3B)
Ceroxylon
Juania
Oraniopsis
Ravenea
Phytelephas
Aphandra
Ammandra
Pseudophoenix
Guihaia
Rhapis
Maxburretia
Rhapidophyllum
Trachycarpus
Chamaerops
Brahea
Johannesteijsmannia
Pholidocarpus
Pritchardiopsis
Licuala
Livistona
Acoelorraphe
Serenoa
Pritchardia
Copernicia
Washingtonia
Colpothrinax
Phoenix
Hemithrinax
Leucothrinax
Coccothrinax
Thrinax
Zombia
Schippia
Trithrinax
Chelyocarpus
Cryosophila
Itaya
Sabal
Borassodendron
Borassus
Lodoicea
Latania
Bismarckia
Satranala
Hyphaene
Medemia
Corypha
Arenga
Wallichia
Caryota
Kerriodoxa
Nannorrhops
Chuniophoenix
Nypa
Retispatha
Pogonotium
Daemonorops
Calamus
Ceratolobus
Pigafetta
Myrialepis
Plectocomiopsis
Plectocomia
Metroxylon
Salacca
Eleiodoxa
Korthalsia
Mauritia
Mauritiella
Lepidocaryum
Raphia
Laccosperma
Eremospatha
Oncocalamus
Eugeissona
Vriesea
Fargesia
Dasypogon
Costus
Tradescantia
Anigozanthos
Stamen connation
Stamens distinct
Stamens connate
Stamens distinct or connate
Petal connation
Petals distinct
Petals connate
Petals distinct or connate
Petals fused in one ring
Fig 7.3 Mirror trees showing the MP optimization of ‘Stamen connation’ (left tree) versus
‘Petal connation’ (right tree) on the palm supertree. (A) all subfamilies except Arecoideae.
(B) Arecoideae (continuation of (a)). Upper left and upper right: character states dei ned
here for each character. Left: White = distinct stamens, Black = connate stamens, Grey =
distinct or connate stamens. Right: White = distinct petals, Black = connate petals, Grey
= distinct or connate petals, Dark grey = petals fused in a ring. Branches are coloured
according to the inferred ancestral states. Boxes at the tip of branches correspond to the
actual observations.
E VO LU T I O N O F T HE PA L M A N D RO ECIU M
(B)
Stamen connation
Stamens distinct
Stamens connate
Stamens distinct or connate
Fig 7.3 (cont.)
Brassiophoenix
Drymophloeus
Ptychococcus
Carpentaria
Wodyetia
Normambya
Balaka
Solfia
Veitchia
Adonidia
Ponapea
Ptychosperma
Kentiopsis
Actinokentia
Archontophoenix
Chambeyronia
Actinorhytis
Calyptrocalyx
Burretiokentia
Cyphophoenix
Physokentia
Cyphosperma
Basselinia
Hedyscepe
Rhopalostylis
Lepidorrhachis
Howea
Laccospadix
Linospadix
Dransfieldia
Heterospathe
Clinosperma
Cyphokentia
Carpoxylon
Neoveitchia
Satakentia
Loxococcus
Pinanga
Nenga
Areca
Bentinckia
Clinostigma
Cyrtostachys
Tectiphiala
Acanthophoenix
Deckenia
Oncosperma
Hydriastele
Dictyosperma
Rhopaloblaste
Lemurophoenix
Dypsis
Marojejya
Masoala
Roscheria
Verschaffeltia
Nephrosperma
Phoenicophorium
Iguanura
Sommieria
Pelagodoxa
Neonicholsonia
Oenocarpus
Prestoea
Euterpe
Hyospathe
Calyptronoma
Calyptrogyne
Asterogyne
Geonoma
Pholidostachys
Welfia
Manicaria
Leopoldinia
Sclerosperma
Orania
Podococcus
Allagoptera
Lytocaryum
Syagrus
Attalea
Cocos
Parajubaea
Jubaea
Butia
Voanioala
Jubaeopsis
Beccariophoenix
Bactris
Desmoncus
Astrocaryum
Aiphanes
Acrocomia
Elaeis
Barcella
Reinhardtia
Roystonea
Chamaedorea
Gaussia
Wendlandiella
Synechanthus
Hyophorbe
Wettinia
Iriartella
Dictyocaryum
Socratea
Iriartea
Petal connation
Petals distinct
Petals connate
Petals distinct or connate
Petals fused in one ring
169
170
FLOWERS ON THE TREE OF LIFE
(A)
Arecoideae (fig. 7.4B)
Ceroxylon
Juania
Oraniopsis
Ravenea
Phytelephas
Aphandra
Ammandra
Pseudophoenix
Guihaia
Rhapis
Maxburretia
Rhapidophyllum
Trachycarpus
Chamaerops
Brahea
Johannesteijsmannia
Pholidocarpus
Pritchardiopsis
Licuala
Livistona
Acoelorraphe
Serenoa
Pritchardia
Copernicia
Washingtonia
Colpothrinax
Phoenix
Hemithrinax
Leucothrinax
Coccothrinax
Thrinax
Zombia
Schippia
Trithrinax
Chelyocarpus
Cryosophila
Itaya
Sabal
Borassodendron
Borassus
Lodoicea
Latania
Bismarckia
Satranala
Hyphaene
Medemia
Corypha
Arenga
Wallichia
Caryota
Kerriodoxa
Nannorrhops
Chuniophoenix
Nypa
Retispatha
Pogonotium
Daemonorops
Calamus
Ceratolobus
Pigafetta
Myrialepis
Plectocomiopsis
Plectocomia
Metroxylon
Salacca
Eleiodoxa
Korthalsia
Mauritia
Mauritiella
Lepidocaryum
Raphia
Laccosperma
Eremospatha
Oncocalamus
Eugeissona
Vriesea
Fargesia
Dasypogon
Costus
Tradescantia
Anigozanthos
Staminodes in female flowers
Staminodes 6 or 6+
Staminodes 3 (often tooth like)
Staminodes lacking
Non applicable
Pistillode in male flowers
Pistillode present
Pistillode lacking
Pistillode minute
Non applicable
Fig 7.4 Mirror trees showing the MP optimization of ‘Number of staminodes versus
functional stamens’ (left tree) versus ‘Pistillode in male lowers’ (right tree) on the palm
supertree. (A) All subfamilies except Arecoideae. (B) Arecoideae (continuation of (a)).
Upper left and upper right: character states dei ned here for each character. Left:
White = six or more staminodes, Dark grey = three staminodes, Black = staminodes
lacking, Light grey = not applicable (bisexual lowers only). Right: White = pistillode
present, Black = pistillode lacking, Dark grey = pistillode minute, Light grey = not
applicable (bisexual lowers only). Branches are coloured according to the inferred
ancestral states. Boxes at the tip of branches correspond to the actual observations.
Black bars indicate a transition towards a staminodial ring.
E VO LU T I O N O F T HE PA L M A N D RO ECIU M
Brassiophoenix
Drymophloeus
Ptychococcus
Carpentaria
Wodyetia
Normambya
Balaka
Solfia
Veitchia
Adonidia
Ponapea
Ptychosperma
Kentiopsis
Actinokentia
Archontophoenix
Chambeyronia
Actinorhytis
Calyptrocalyx
Burretiokentia
Cyphophoenix
Physokentia
Cyphosperma
Basselinia
Hedyscepe
Rhopalostylis
Lepidorrhachis
Howea
Laccospadix
Linospadix
Dransfieldia
Heterospathe
Clinosperma
Cyphokentia
Carpoxylon
Neoveitchia
Satakentia
Loxococcus
Pinanga
Nenga
Areca
Bentinckia
Clinostigma
Cyrtostachys
Tectiphiala
Acanthophoenix
Deckenia
Oncosperma
Hydriastele
Dictyosperma
Rhopaloblaste
Lemurophoenix
Dypsis
Marojejya
Masoala
Roscheria
Verschaffeltia
Nephrosperma
Phoenicophorium
Iguanura
Sommieria
Pelagodoxa
Neonicholsonia
Oenocarpus
Prestoea
Euterpe
Hyospathe
Calyptronoma
Calyptrogyne
Asterogyne
Geonoma
Pholidostachys
Welfia
Manicaria
Leopoldinia
Sclerosperma
Orania
Podococcus
Allagoptera
Lytocaryum
Syagrus
Attalea
Cocos
Parajubaea
Jubaea
Butia
Voanioala
Jubaeopsis
Beccariophoenix
Bactris
Desmoncus
Astrocaryum
Aiphanes
Acrocomia
Elaeis
Barcella
Reinhardtia
Roystonea
Chamaedorea
Gaussia
Wendlandiella
Synechanthus
Hyophorbe
Wettinia
Iriartella
Dictyocaryum
Socratea
Iriartea
(B)
Staminodes in female flowers
Staminodes 6 or 6+
Staminodes 3 (often tooth like)
Staminodes lacking
Non applicable
Fig 7.4 (cont.)
Pistillode in male flowers
Pistillode present
Pistillode lacking
Pistillode minute
Non applicable
171
172
FLOWERS ON THE TREE OF LIFE
7.4 Discussion
7.4.1 Stamen number
An androecium composed of numerous stamens has long been considered an
ancestral feature in angiosperms. Both in monocots and eudicots evolution
has proceeded towards a reduction of the stamen number. However, secondary
increases have evolved several times in both clades. According to traditional perception, ancestral polyandry is associated with a spiral organization of stamens,
whereas derived polyandry is associated with cyclic organization (Endress and
Doyle, 2007), although this view was recently challenged by Endress and Doyle
(2009).
Although palm lowers follow the basic monocot arrangement of organs, they
stand out in several aspects. h is applies to the androecium, which is a focus of
this chapter, but also to other morphological characters which display a variation
unequalled or almost so within the monocots. Polyandry (deined here as more
than twice merism, i.e. more than six stamens) occurs in 19 monocot families representing six diferent orders (Fig 7.5). In most families except palms, only one or
a few genera display polyandry (data extracted from Dahlgren et al., 1985), and
in most polyandrous genera the number of stamens does not exceed 12. Palms
clearly stand out compared to all other monocot families, since polyandrous lowers are present in almost half of the 183 genera. Furthermore the range of variation in stamen number is exceptionally wide in palms, ranging from only one
Zingiberales
Commelinales
Poales (in Cyperaceae and Poaceae)
Arecales (in Arecaceae)
Dasypogonaceae
Asparagales (in Amaryllidaceae, Asparagaceae and Hypoxidaceae)
Liliales (in Smilacaceae and Melanthiaceae)
Dioscoreales
Pandanales (in Cyclanthaceae, Pandanaceae and Velloziaceae)
Petrosaviales
Alismatales (in Alismataceae, Aponogetonaceae, Butomaceae,
Acorales
Hydrocharitaceae, Juncaginaceae, Limnocharitaceae,
Potamogetonaceae, Ruppiaceae and Tofieldiaceae)
Fig 7.5 Tree of the monocot orders (topology as from Stevens, 2001 onwards) showing the
orders (bold) and families (grey) in which lowers with androecia including more than six
stamens are found.
E VO LU T I O N O F T HE PA L M A N D RO ECIU M
(Dransield et al., 1995) to more than one thousand (Dransield et al., 2008a). he
ancestral stamen number inferred for the palm family is six, which is also the
ancestral number found for monocots as a whole (Nadot, unpubl. data). In four out
of ive subfamilies polyandry evolved several times from this trimerous androecium (with six stamens). he highest number of transitions towards polyandry,
but also towards reduction in stamen number (from six to three) is found within
subfamily Arecoideae, which include approx. half of all species of palms. It should
be noted that lowers of all arecoid palms are unisexual and that almost all species
are monoecious.
he spatial separation of sexual expression is highly variable in palms.
Hermaphroditism, monoecy and dioecy are widespread in the family. Cases of
polygamy (which corresponds to various combinations of sexual expression,
such as andromonoecy or androdioecy) are also found. All three types of sexual
expression are represented in the subfamilies Calamoideae and Coryphoideae.
he subfamily Arecoideae is almost entirely monoecious, except for two dioecious
genera (Chamaedorea Willd. + Wendlandiella Dammer), whereas Ceroxyloideae
are mostly dioecious, with only one hermaphroditic to polygamous genus
(Pseudophoenix H.Wendl. ex Sarg.). Nypa is monoecious, but highly unusual morphologically with the proximal position of the male lowers and the distal position of the female lowers (acrogyny). Inlorescence acrogyny is found in Arenga
(Coryphoideae) in which sometimes distal inlorescences bear female lowers and
proximal inlorescences bear male lowers. Polyandry coincides in most genera
with unisexual lowers (Table 7.2), but whether this pattern results from adaptation
in relation to pollination mechanisms or results from some constraints imposed
by shared ancestry remains to be explored.
7.4.2 Anther features
Orientation of anther dehiscence is a relatively stable character in palms. here
are only ive transitions from latrorse to extrorse dehiscence, all in unrelated
genera (Nypa, Wallichia, Hemithrinax Hook.f., Allagoptera Nees and Orania),
and some 20 transitions from latrorse to introrse, also almost all in unrelated
genera, with the exception of the [Manicarieae + Geonomateae] clade, for which
introrse anthers are a synapomorphy. An unusual case of apical opening by pores
is found within the genus Areca. Studies of pollination mechanisms in palms
have revealed the existence of interactions with a number of pollinating insects,
especially curculionid, nitidulid and staphylinid beetles, halictid bees and various groups of l ies. he ecological and evolutionary signiicance of dehiscence
remains unclear, since only a few studies have focused on the mechanisms of
pollen transfer.
We are well aware that variation in the character ‘anther attachment’ is almost
continuous. For convenience however, we use here the classical main categories
173
174
FLOWERS ON THE TREE OF LIFE
recognized in the botanical literature, namely dorsii xed and basii xed anthers.
Our character optimization suggests that basally attached anthers represent the
ancestral condition for the family and that the dorsal type of attachment has
evolved several times during the diversiication of palms. It represents the ancestral condition for subfamilies Coryphoideae and Arecoideae, in which reversals
to the basii xed type have occurred several times. For the same reasons as cited
above, the ecological and evolutionary signiicance of this variation is unknown,
but would be well worth exploring, considering the diversity of palm pollinators.
he importance of anther dehiscence, opening and attachment in pollination
processes was underlined by D’Arcy (1996).
7.4.3 Organ synorganization
he connation of petals and stamens is another variable feature within the palm
family. Our results suggest that both free petals and free stamens are ancestral
states in the family. Partial fusions in the corolla and androecium have evolved
several times. Fusions in the androecium evolved predominantly in taxa with connate petals (Calamoideae, Coryphoideae and the clade composed of Manicarieae
+ Geonomateae within Arecoideae). Although the two phenomena are correlated,
it should be noted that not all genera with connate anthers have connate petals
and vice versa. In lineages with unisexual lowers, petal connation in staminate
and pistillate lowers is similar, whereas fusions are less closely linked in pistillate and staminate androecia. he number of staminodes can be quite diferent
from the number of functional stamens, especially in polyandrous genera, which
suggests further sex divergence of the genetic control mechanisms underlying the
formation of the androecium.
Adnation of stamens to petals has evolved several times and predominantly in lineages with connate petals and typically connate stamens, such as
Coryphoideae, Calamoideae and Geonomateae. Only in the two sister genera,
Oraniopsis (Becc.) J.Dransf., A.K.Irvine and N.W.Uhl, and Ravenea H.Wendl. ex
C.D.Bouché (Ceroxyloideae) does adnation occur between free petals and free
stamens. Increase in stamen number is apparently unconstrained by stamen synorganization, since polyandry is almost equally represented in groups with free or
fused stamens respectively.
7.4.4 Sterile organs
Character optimization shows that in Calamoideae, Ceroxyloideae and
Coryphoideae (except Medemia Wurttenb. ex H.Wendl.), the number of staminodes in female lowers is equal to the number of functional stamens in the male
lowers, if this is six. h is pattern is contrasted in several arecoid genera that
have six functional stamens and a diferent number of staminodes. In one particular clade that includes genera with six stamens and genera with more than
E VO LU T I O N O F T HE PA L M A N D RO ECIU M
six stamens, the number of staminodes is reduced to three. Overall, the number
of staminodes is often lower than the number of functional stamens in taxa with
more than six stamens, and staminodes are completely lacking in a few hexandrous genera, such as in Nenga H.Wendl. and Drude (Arecinae) (some species
of Nenga do produce minute staminodes, however) and the closely related genera in tribe Euterpeae, Neonicholsonia Dammer, Oenocarpus Mart. and Euterpe
Mart. Interestingly, in our optimization no straightforward connection appears
between the absence of a pistillode in staminate lowers and the absence of
staminodes in female lowers. h is may be a result of diverging selective pressures acting upon male and female lowers. he fact that species deviating from
the ancestral hexandrous condition tend to produce less staminodes suggests a
loss in the adaptive value of staminodes, since they do not produce pollen, and
therefore are under a diferent selective pressure compared to the functional
stamens.
7.4.5 How and why has polyandry evolved in palms?
Increase in stamen number appears to have occurred in diferent ways and perhaps
in response to diferent factors in diferent groups of palms.
(Uhl and Moore, 1980).
he increase in stamen number in palms may relect adaptation to diferent
pollen transferring agents. In palms the framework of interaction with the pollinating agents as set by the plant is typically rather loose. his means that closely
related species and even populations of the same species are visited by diferent
taxonomic groups of potential pollinators, as revealed in genera such as Euterpe
(Bovi and Cardoso, 1986; Reis et al., 1993; Kuchmeister et al., 1997;), Aiphanes
Willd. (Listabarth, 1992; Borchsenius, 1993) and Licuala Wurmb (Barfod et al.,
2003). Since most studies of palms are only dealing with the pollination mechanism at one speciic site at one speciic time, it is diicult to generalize about the
co-evolutionary relationships. Both beetles and bees, which are the predominant
pollinators of palms (Sannier et al., 2009 for a review), are attracted to lowers or
inlorescences that produce copious amounts of pollen, and polyandry is one way
that this can be potentially achieved. Another way is by close insertion of the lowers along the rachillae, whereby parts of or the entire inlorescence may constitute
the functional unit in the interaction with the potential pollinators. Both strategies co-exist in palms, which can display both highly polyandrous lowers and
densely packed lowers. herefore, although polyandry may be of key importance
for our understanding of the diversiication of the palm lower, it is not straightforward to understand the underlying evolutionary processes that led to its multiple
appearances in the evolution of palms.
Several polyandrous palm lowers belonging to all four subfamilies in which
polyandry occurs have been the subject of developmental studies (see Table 7.2)
175
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FLOWERS ON THE TREE OF LIFE
(Uhl, 1976; Uhl and Moore, 1977, 1980; Uhl and Dransield, 1984; Barfod and
Uhl, 2001). In all groups but tribe Phytelepheae, which is exceptional in having
a centrifugal stamen development, the androecium of polyandrous taxa exhibits
underlying trimery and the stamen initiation follows the order of inception of
the perianth parts, with antesepalous stamens being formed before antepetalous ones, in distinct sectors (Uhl and Dransield, 1984). Besides these basic common features, there is nevertheless considerable variation in the arrangement
of stamens and in the way the loral apex expands to accommodate numerous
stamens. In Ptychosperma mooreanum Essig (Uhl, 1976), Lodoicea maldivica
(J.F.Gmel.) Pers. ex H.Wendl. and Caryota mitis Lour. (Uhl and Moore, 1980), the
high and rather variable number of stamens is a consequence of the loral apex
varying in width and height, as well as of diferences in the number of primordia that can form in the outer, and quite wide, antepetalous whorl. In these
species, never more than one stamen occurs in the antesepalous position (Uhl
and Moore, 1980), whereas several stamens can form in antesepalous positions
in Socratea exorrhiza, Wettinia castanea and Welia georgii. In Eugessiona utilis,
which has the highest number of stamens in the genus, an additional row of antepetalous stamens develop centrifugally outside of and alternating with the i rstformed row (Uhl and Dransield, 1984), perhaps due to the presence of residual
meristem. Increase in stamen number through duplication of the primordia is
probably made possible by expansion of the loral apex, which may be released
from spatial constraints and hormonal control by the apical meristem. Trimery
is lost in Phytelepheae, which display the highest stamen numbers in monocots.
In this tribe, centrifugal expansion is believed to represent an alternative way to
increase the size of the loral apex thereby accommodating numerous stamens
(Uhl and Moore, 1977). Apical expansion and polyandry are thought to have
arisen following changes in the morphology of inlorescence bracts and perianth
segments (Uhl and Moore, 1980), a point that could be further explored within a
phylogenetic framework.
7.5 Conclusion
he present chapter highlights the outstanding diversity of the palm androecium
compared to other monocots, opening the way to various future studies. As mentioned above, the observed pattern of variation across the phylogeny raises questions about the ecological and evolutionary signiicance of the variation in stamen
number. It also raises the question of the molecular processes that underlie such
variation. he molecular basis of loral development has been rather thoroughly
investigated across angiosperms including palms over the last 20 years (Adam
et al., 2007a, b). Although relatively few studies have focused on the molecular
basis of loral organ variation, the SUPERMAN gene has been shown to cause an
E VO LU T I O N O F T HE PA L M A N D RO ECIU M
increase in stamen number in A. thaliana and Petunia hybrida when mutated
(Bowman et al., 1992; Nakagawa et al. 2004), and mutated forms of the FON gene
(Floral Organ Number) have led to an increase in stamen number in conjunction
with an increase in loral meristem size in rice (Suzaki, 1991; Nagasawa et al. 1996;
Suzaki, 2006). hese studies provide excellent candidate genes for further exploration of the molecular mechanisms underlying the extraordinary variation in loral apex expansion and stamen number in palms.
Acknowledgements
We are gratefully indebted to Peter Endress and John Dransield for carefully
reviewing this manuscript and suggesting valuable improvements. he Aarhus
University Research Foundation is acknowledged for funding SN as guest
researcher at Aarhus University, Denmark.
7.6 References
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(2007a). Determination of lower
structure in Eleais guineensis: do palms
use the same homeotic genes as other
species? Annals of Botany, 100, 1–12.
Adam, H., Jouannic, S., Orieux, Y. et al.
(2007b). Functional characterization
of MADS box genes involved in the
determination of oil palm lower
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Asmussen, C. B. and Chase, M. W. (2001).
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Asmussen, C. B., Dransield, J., Deickmann,
V. et al. (2006). A new subfamily
classiication of the palm family
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Baker, W. J., Savolainen, V., AsmussenLange, C. B. et al. (2009). Complete
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Baker, W. J., Zona, S., Heatubun, C. D. et al.
(2006). Dransieldia (Arecaceae) – a
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Barfod, A., Burholt, T. and Borchsenius, F.
(2003). Contrasting pollination modes
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D’Arcy, W.G. (1996).Anthers and stamens
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