Integration of Morphological and Ribosomal RNA Data on the Origin of Angiosperms

32 Pages·1994·15.2 MB·

by  James A Doyle

INTEGRATION OF
James
A. Doyle, 2
MORPHOLOGICAL AND Michael Donoghue, 3
J.
and Elizabeth A. Zimmer4
RNA
RIBOSOMAL DATA ON
THE ORIGIN OF
ANGIOSPERMS
1
Abstract
Previous phylogenetic analyses of morphological and rRNA data indicated that Gnetales are the closest living
relatives of angiosperms but gave different basal angiosperm relationships. A two-step morphological analysis of seed
plants (including fossils) and angiosperms rooted the latter near Magnoliales, with tricolpate eudicots and paleoherbs
(herbaceous magnoliids and monocots) forming a clade, whereas analyses of rRNA sequences rooted angiosperms
among
paleoherbs, with eudicots and woody magnoliids forming a clade. Experiments with a revised seed plant
morphological
data when
set raise further questions: angiosperms are scored like different angiosperm subgroups,
they
associate with different outgroups, although Gnetales are their closest living relatives. To test whether morphological
and rKINA
data are seriously contradictory or rather complementary, with inconsistencies being a function of better
resolution in different parts of the tree, we experimented with morphological and rRNA data sets including the same
six extant gymnosperm" and 12 angiosperm taxa. Both analyses again associate angiosperms and Gnetales. The
morphological
analysis differs from previous ones in placing Nymphaeales and monocots at the base of the angiosperms,
ut trees rooted next to Magnoliales are only one step less parsimonious. As in previous studies, the rRNA analysis
roots angiosperms rRNA
next to Nymphaeales and breaks up the eudicots. Bootstrap and decay analyses of the data
snow
strong support for the monophyly of angiosperms and Gnetales and their sister group relationship, but low
support
for groupings within angiosperms. However, one or another group of paleoherbs basal in most bootstrap
is
A
rees. combined
analysis favors a paleoherb rooting, but other relationships agree with the morphological results;
In Partlcular, eudicots form a clade. The conclusion that Gnetales are the closest living relatives of angiosperms
permits
a wide range of morphological scenarios, depending on the arrangement of fossil outgroups. Discovery of
ossils on the long branch leading to angiosperms, methods of factoring out artifacts in rooting, or molecular data on
e
control of floral morphogenesis angiosperms and Gnetales may be required for further progress in unraveling
in
ne
l origin of angiosperms.
Hecent
Our morphological analysis of seed plants
cladistic analyses of morphological and initial
rtbosomal RNA &
data have led to apparently con- (Doyle Donoghue, 1986), which included both
ung
results on the position of angiosperms among living and fossil taxa, treated angiosperms as a
plants, basal relationships among angiosperms, single taxon, modeled on Magnoliales and Winter-
and
resulting scenarios for the origin of angio- aceae, following the consensus at that time. This
sperms
(Crane, 1985; Doyle & Donoghue, 1986, study was designed especially to test the previous
&
992; Donoghue Doyle, 1989a; Zimmer analysis of Crane (1985) and other current ideas
et al.,
&
^989; Loconte Stevenson, 1990, 1991; Taylor on seed plant phylogeny, by including both char-
&
Hl &
<*ey, 1992; Hamby Zimmer, 1992). The acters used by Crane and conflicting similarities
Purpose
of this paper to investigate the causes that he had omitted. Contrary to our expectations,
is
a™
significance of these conflicts, and what any but as Crane had found, this analysis indicated that
if
u
st conclusions monophyletic group, with conif-
concerning the origin of angio- seed plants are a
sperms
can be drawn from these data. eropsids (cordaites, conifers, ginkgos) derived from
M. W. improvement of the manuscript.
JX^fJ- Chase and an anonymous reviewer provided valuable suggestions for
j*ction of 95616, U.S.A.
Evolution and Ecology, University of California, Davis, California
4
02138,
rtment Cambridge, Massachusetts
of 0l*ganismic and Evolutionary Biology, Harvard University,
U.S A
4
Laboratory 20560, U.S.A.
of Washington, D.C.
Molecular Systematics, Smithsonian Institution,
419-450. 1994.
Ann. Missouri Bot. Gard. 81:
420
Annals of the
Missouri Botanical Garden
advanced "seed ferns" with platyspermic seeds and with pinnately veined leaves and paracytic
stomata.
saccate pollen (roughly as proposed by Rothwell, This recalls the views of Burger (1977, 1981)
on
1982), and that angiosperms belong to an "an- the primitive status of Piperales and/or monocots,
thophyte" clade also including Bennettitales, Pent- although not in detail.
oxylon, and Gnetales, which is in turn nested among More recently, the view that the first angio-
so-called Mesozoic seed ferns (corystosperms, glos- sperms were "paleoherbs" was elaborated by Tay-
&
sopterids, Caytonia). In response to a cladistic lor Hickey (1990, 1992), based on recognition
analysis involving only extant seed plants by Lo- of an Early Cretaceous (Aptian) paleoherb
fossil
&
conte Stevenson 1 990), we revised this analysis from Australia and their own morphological anal-
(
&
with generally similar results (Doyle Donoghue, ysis. Their tree differs in that Chloranthaceae are
1992), except for more definite placement of cy- basal, followed by Piperaceae, which contrasts with
among
cads platysperms and more uncertainty on the position of Chloranthaceae in Laurales in the
&
may
the position of ginkgos, which be associated analysis of Donoghue Doyle (1989a), well re-
with the Permian-Triassic seed fern Peltasper- moved from Piperales, and in the woody magnoliid-
mum &
instead of conifers (cf Meyen, 1 984). eudicot clade in Hamby Zimmer (1992). This
.
A
subsequent may
analysis of extant angiosperms difference be partly a result of treating cor-
&
(Donoghue
Doyle, 1989a), using the results of related ovule features related to orthotropy (which
the seed plant study to polarize characters within was assumed to be primitive) as three separate
the group, yielded trees rooted in or next to the characters, and partly a result of omitting taxa that
&
"woody
magnoliid" order Magnoliales (specifically linked groups differently in the Donoghue Doyle
families with granular exine structure, which ex- analysis Trimeniaceae, which tend to link
(e.g.,
cludes Winteraceae and Austrobaileya). This re- Chloranthaceae with other Laurales: cf. Endress,
sult is generally consistent with conventional views 1987).
on angiosperm
evolution (e.g., Takhtajan, 1969; The apparent conflicts between the morpholog-
Cronquist, 1981, 1988). The remaining angio- ical and molecular data, especially regarding "root-
sperms form four major clades: two other groups ing" of the angiosperms, were discussed by Don-
woody &
of magnoliids, Laurales, including Chlo- oghue Doyle 989b), who suggested that they
( 1 ) 1
(
ranthaceae, widely discussed because of their un- may illustrate a general conclusion drawn by Hillis
and
usually simple flowers, and (2) winteroids, including (1987): that conflicts between morphological
Winteraceae, and contradic-
Illiciales, possibly Canellaceae; molecular results rarely reflect serious
(3) dicots with tricolpate and derived pollen, later tions, but rather different levels of resolution of the
&
This
designated eudicots (Doyle Hotton, 1991); and two sorts of data in different parts of the tree.
(4) "paleoherbs," consisting of herbaceous or semi- seemed be supported by the fact that experi-
to
herbaceous magnoliids seed plant stud-
(Aristolochiaceae, Lactoris, ments with alternative trees in the
& shown
Piperales, Nymphaeales) and monocots. Somewhat Donoghue, 1986, 1992) had
(Doyle
ies
& seed
similar results were obtained by Loconte anthophytes within
Ste- that other positions of
were
venson
(1991); the most important difference, plants, and of angiosperms within anthophytes,
placement most par-
of Calycanthaceae and Idiospermata- only parsimonious than the
slightly less
ceae at the base of the angiosperms, may be due simonious arrangements. For example, it was o y
wi
to their use of Recent angiosperms
plants only as outgroups, one step less parsimonious to link
up
since the closest outgroup, Gnetales, shares fea- Caytonia and/or glossopterids, thus breaking
can*
tures such as opposite leaves and two-trace nodes anthophytes with
the anthophytes, or to link
wna
with Calycanthales. anthophytes—
eropsids, with Gnetales basal in
In contrast, analyses of partial 18S and 26S we a neo-englerian arrangement. Similar J ,
called
rRNA on-
sequences from angiosperms and angiosperms
other ex- in our morphological analysis of (
& w*n
tant seed plants (Hamby Zimmer, 1992), chosen oghue & 1989a), we had found trees
Doyle,
w
to provide a test of current morphological hypoth- angiosperms rooted among paleoherbs that
eses, placed a series of paleoherb taxa at the base only one step less parsimonious than those r
case
a
of the angiosperms (Nymphaeales, Piperales, and near Magnoliales. This may therefore be
Woody
monocots). ambl u0,
magnoliids and eudicots formed where morphological data are 6
the
^
a more derived clade, within which detailed rela- they favor a woody magnoliid prototype, bu il
strong-
tionships are poorly resolved. These results give a slightly—whereas the molecular data point
rooting,
different picture of the first angiosperms: they would one toward a paleoherb
ly in direction,
be herbaceous on re,at'°
or nearly evidence
so, with palmately veined and therefore provide better
u
leaves and anomocytic may molecular
stomata, rather than woody be the
ships. In other cases,
it
-
Number
3
Volume 81, Doyle
et
al. 421
1994 Integration of Morphological and rRNA Data
that are ambiguous and the morphological data oghue, 1986) was a function of the assumption
that are clearcut. Thus the two sorts of data may that the first angiosperms were like Magnoliales
be more complementary than contradictory. and Winteraceae. Perhaps then the basal position
we
In the present study, have attempted to of Magnoliales in the angiosperm analysis (Dono-
&
address these issues by comparing results derived ghue Doyle, 1989a) was a consequence of an
from morphological and molecular data for the incorrect identification of outgroups based on
this
same set of seed plant taxa, probing the strengths initial assumption. For the sake of rapid progress,
and weaknesses of the results with methods such we split the seed plant and angiosperm problems
as bootstrap and decay analysis, and analyzing a in two. This seemed reasonable at the time: there
combined data set. The question of analyzing mor- was already strong evidence that the angiosperms
phological and molecular data separately and com- were monophyletic, and there was some consensus
paring the results or combining them at the outset on basic states within the group. However, we
is a topic of ongoing debate (Kluge, 989; Barrett realized from the beginning that would eventually
1 it
&
etal., 1991; Donoghue Sanderson, 1992; Bull be necessary to carry out additional analyses de-
et al., 1993; de Queiroz, 1993). One argument signed to resolve simultaneously relationships at
against combining data sets that the greater the point where the two analyses intersect. For
is
number
of molecular characters simply over- example, we noted that Chloranthaceae share many
will
whelm
the morphological characters. However, features with Gnetales, and that angiosperms might
this
does not necessarily hold: if the molecular results therefore be directly associated with Gnetales if
are poorly resolved, as they often are, even a small Chloranthaceae were assumed to be primitive.
number
of morphological characters can have a It should be recognized that conclusions derived
&
decisive effect (Donoghue Sanderson, 1992). In from this sort of two-step procedure are not nec-
any
case, it is possible both to analyze data sets essarily incorrect: there might be only one most
separately and to combine them, and our results parsimonious position for angiosperms no matter
"nply
that this approach can give instructive re- what internal relationships or basal states in an-
sults. giosperms are assumed. should also be noted that
It
This study is not intended to be a comprehensive the problems are not unique to our study: ours is
examination of "morphological" versus "molecu- simply one example of a general method that Mish-
lar" data on method
this topic. Y. Suh (pers. comm.) has ler (1994) calls compartmentalization. This
obtained
different results from another part of the was also used within our angiosperm analysis (Don-
<ftS subunit of rDNA, which roots the angiosperms oghue & Doyle, 1989a), in which we did a prelim-
between
a clade including most Magnoliales and inary analysis of Laurales to determine basic states
u
urales and other angiosperms. Equally different in a derived subgroup referred to as "core Laura-
trees, with
the aquatic genus Ceratophyllum
basal les."
and
remaining angiosperms These problems were recognized and addressed
divided into tricolpate-
&
enved
eudicots and monosulcate magnoliids and in a series of experiments reported by Doyle
jnonocots, have been Donoghue which combined nine angio-
obtained from rbcL sequences (1990),
S et aL 1991; Chase 1993 Q sperm taxa with the 7 nonangiospermous groups
et al iu et al" 1
' "
i9Q o '
&
93). Analyses of shorter rRNA sequences by used in Doyle Donoghue (1992). Here we pre-
Wsky
which
et al. (1991) and a smaller rbcL data set sent an updated version of these experiments,
"
SCbe Ct a1 have the nature of the problem and the poten-
(1 2) given different trees illustrate
nL
'
'
notably and
with gymnosperms as a monophyletic tial value of considering both morphological
InStCad
weT °f considering aU these data sets, molecular evidence.
ave
chosen
to address the two that we know
^
St alth°ugh we
mention some
' will briefly prelim-
. TAXA, CHARACTERS, AND ANALYSES
analyses
including
rbcL.
The revised seed plant and angiosperm matrix,
p nine-angiosperm anal-
henceforth designated the
BINING
Previ
ous Morphological Analyses
The
Appendix (Table
of S presented in the 1).
E£d ysis, is
Plants
and
Angiosperms
angiosperm taxa were selected to represent the
m
&
^° Donoghue Doyle 989a)
r COncern we major clades found by 1
that wish address (
to first
is th among
^°S rooted both near Magnoliales and
y tr| at previous inferences concern in trees
ine k .
origin which necessitated dividing the pa-
of angiosperms were compromised paleoherbs,
^
circular reasoning. Perhaps the position of an- leoherbs into four groups. In five cases these clades
P^rms in the seed plant analysis (Doyle & Don- are represented by individual taxa used in Dono-
422 Annals of the
Missouri Botanical Garden
&
we
ghue Doyle 1 989a), in four by composite taxa: states in other seed plants, scored the latter as
(
unknown;
Magnoliales, based on Degeneria, Myristicaceae, this is especially true of floral characters,
Annonaceae, and Magnoliaceae ("core Magnoli- where we hoped to avoid biasing the results by
&
ales" of Donoghue Doyle, 1989a); Piperales assuming questionable homologies of parts between
(Piperaceae, Saururaceae); Nymphaeales (Nym- angiosperms and other groups. These characters
phaeaceae, Cabombaceae); and eudicots (Ranun- also form the basis for the morphological analysis
Nelumbo, Trochodendrales, Hamameli- of Recent taxa presented below as a counterpart
culidae,
rRNA
we
These are scored terms of estimated of the analysis; for simplicity retained
dales). in
ancestral states for the whole taxon (theoretical nine states that were potentially informative in that
and practical problems in this procedure are dis- matrix but autapomorphic in the present one (e.g.,
cussed further below). Thus, where the taxon con- tetracytic stomates in Piperales, tricolpate pollen
sists of two taxa included in the previous analysis in eudicots).
and these have different stages, the group was Multistate characters were unordered, except
scored as uncertain (e.g., 0/1). In the case of for two easily ordered quantitative characters (pol-
Two
binary characters, where uncertain (0/1) and un- len megaspore wall thickness). multistate
size,
known are equivalent in tree construction, we characters involving exine structure deserve spe-
(?)
usually distinguished between the two scorings in cial consideration, since our decision not to order
the matrix to indicate the nature of the uncertainty, them had a significant impact on the results pre-
"?"
but we did not try to weed out cases where sented below.
all
&
had been used for uncertainty in the previous anal- In the angiosperm study (Donoghue Doyle,
we an structure
yses. In Magnoliales, basic states were estimated 1989a), recognized infratectal
and
based on the previous result that Degeneria the character with granular and columellar states
is
sister group of the other three taxa, which them- assumed that granular was primitive, based on out-
selves form an unresolved trichotomy. Eudicots group comparison with other anthophytes. In the
&
Donoghue, 1992),
were assumed to consist of two sister clades, Ranun- revised seed plant study (Doyle
culidae plus Nelumbo and Trochodendrales plus we recognized spongy-alveolar, honeycomb-alveo-
angiosperms as
Hamamelidales. Laurales were represented by Aus- and granular states and scored
lar,
structure
trobaileya, which was at or near the base of the granular, assuming that columellar
two
combining the
order in our previous trees, and Chloranthaceae, evolved within the group. In
within
which are of special interest because they have data our previous polarization of states
sets,
the
been widely discussed as possible primitive angio- angiosperms could be preserved by ordering
sperms. Use of Austrobaileya to represent Laur- character (spongy-honeycomb-granular-columel-
and
ales might be questioned, since it lacks many fea- lar). By placing two steps between alveolar
trees
tures commonly associated with the order. However, columellar, this ordering would bias against
out-
alveolar
our results bear out its use in this way, since Aus- in which angiosperms are linked with
columeUar
trobaileya associated with Chloranthaceae the groups Caytonia, glossopterids),
is in (e.g.,
granular
and
trees obtained, as it was with the larger data set. groups are basal in angiosperms,
conver-
a
Trees were rooted by including a taxon based on structure in groups like Magnoliales is
One-
and
Devonian "progymnosperms" Pentoxylon,
(Aneurophyton, Ar- gence with Bennettitales,
exuie
the
chaeopteris) as outgroup. This scenario involves four steps if
tales.
Sucn a
not.
Characters are primarily a combination of those character ordered but three if it is
is
coexistent
& on the
used in the seed plant analysis of Doyle Don- bias might be defended based
tran
(and
oghue (1992) and those in the angiosperm analysis of columeUar and granular structure
& (Walker,
of Donoghue Doyle 989a) angiosperms
that are potentially tional states) within
1 '
(
and r '
informative for the taxa under consideration. To Le Thomas, 980- 98 and of alveolar & *
1 1 )
1
Campo & *
(Van
these we added several apomorphies that poten- ular structure within conifers
unwarran*
seems
tially hold angiosperms together as a monophyletic gardon, 1973). However, ^
it
alveoar^
from
group, new
either as characters or as additional assume that a direct transition
ca^
other
states of existing seed plant characters (e.g., three- columeUar could not have occurred in
*^
Ca tonia
y
nucleate microgametophyte, complete loss of the Trees with angiosperms linked with
e
trees in
megaspore some shortest
wall). In cases, features that vary only one step longer than the *»
data
& 1992)
within angiosperms are expressed as additional states of the Doyle Donoghue (1986,
granular *
of characters recognized in seed plants as a whole and a transition from alveolar to ^
grounds («•*'
(e.g., palmate leaf venation). For angiosperm char- conceivable on structural
tainly
acters in which there are no comparable
clearly
n
Number
3
Volume 81 Doyle et 423
al.
,
1994 Integration of Morphological and rRNA Data
the junctions between the walls as columellae: E. 1991). Since there are too many taxa for branch-
Masure, pers. comm.). and-bound analysis, which guarantees finding
all
Endexine structure was not included as a char- most parsimonious we used
trees, the heuristic
&
acter in the seed plant analyses (Doyle Dono- search algorithm, with 10 replicates of stepwise
TBR
ghue, 1986, 1992), because all groups except an- random addition of taxa and branch swapping.
giosperms have a uniformly laminated endexine, This increases the probability of finding most par-
making the character uninformative. Of the two simonious trees that belong to different * 'islands"
states in angiosperms, endexine present or absent (Maddison, 1991), which were found
in fact in
in the extra-apertural areas, absence of endexine some experiments (see results). Alternative ar-
&
was assumed to be ancestral (Donoghue Doyle, rangements were investigated using MacClade and
1989a). This was based on the hypothesis that the the constraints option in PAUP.
laminated endexine of other seed plants homol-
is
ogous with the footlayer of angiosperms, since both
SINGLE-ANGIOSPERM ANALYSES
develop from similar tangential lamellae, and that
the endexine of angiosperms, which nonlami- Experiments with single angiosperm taxa re-
is
nated except sometimes under the apertures, a sulted in several different positions of the angio-
is
new
layer (Zavada, 1984). Again, the original po- sperms relative to other anthophytes (Pentoxylon,
larization could be preserved in the combined data Bennettitales, Gnetales), and of anthophytes within
set by ordering the character (endexine laminated- seed plants.
absent-nonlaminated). However, because the ho- As expected, when Magnoliales are substituted
mologies involved are rather speculative Ga- for angiosperms (Fig. angiosperms are the sister
(cf. 1),
barayeva,
1991), seems preferable to treat the group of other anthophytes, and anthophytes are
it
three
states as unordered. associated with one or another combination of Cay-
We
made
also a few substantive changes based tonia, glossopterids, and corystosperms, as in Doyle
on new &
among
data, such as recognition that pollen of Donoghue (1986, 1992). Relationships
&
nperaceae
(Piperales) has supratectal spinules and other groups also parallel those found by Doyle
a sculptured sulcus (Bornstein, 1989), Cabomba- Donoghue (1992), including some with the ar-
ceae
(Nymphaeales) have a columellar exine struc- rangement of extant cycads, Ginkgo, and conifers
ture (Osborn et 1991), Myristicaceae (Mag- found by Loconte & Stevenson 990). As shown
al., 1
(
noliales) have both S and PI type sieve-tube plastids, in Figure 1, one of the characters that supports
and
Aristolochiaceae have basically PI type plas- this position of Magnoliales is the presence of gran-
I
ms
(as seen Saruma
in and Asarum), mono- ular exine structure.
like
c°ts (Behnke, We
1 988). added one new potential In contrast, when Winteraceae, Austrobaileya,
synapomorphy
of angiosperms and Gnetales, dou- eudicots, Aristolochiaceae, or monocots are sub-
«
fertilization, angiosperms, the angiosperm taxon
in the sense of regular fusion of stituted for
e secon
d sperm nucleus with a second megaga- connects with Caytonia or Caytonia plus glossop-
metophyte when
nucleus. This has been confirmed in terids. This is also true of most trees found
£
dra
and seems independent of (although prob- Nymphaeales are substituted for angiosperms (Fig.
a
Y prerequisite for) the uniquely angiospermous although in two such trees the Bennettitales-
2),
eature of endosperm formation (Friedman, 1990, Pen toxylo -Gnetales clade, Nymphaeales, and
y
&
92; Donoghue Scheiner, 1992). Caytonia form a paraphyletic group at the base
vera
very un-
sets °f analyses were performed using of the platysperms (a stratigraphically
'
,
new
nine-angiosperm we parsimonious arrangement). These trees break up
matrix. In one
set,
alyzed
the matrix with each of the nine angio- the anthophytes, although the Bennettitales-Penf-
5perm
groups substituted individually for angio- o*y/orc-Gnetales clade is still the next-closest group
Perms.
n removing might be questioned
I the eight remaining taxa, we to angiosperms. This result
gained
Caytonia and/
characters that then became autapomor- because implicitly assumes that
it
leS
lX ls often desirable remove such char- or glossopterids had angiosperm and gnetalian states
to
'
a
FS Decau unknown
se they are uninformative and distort for several characters that were scored as
eas
Ures
of homoplasy, but this not a problem because they are not preserved or not yet estab-
is
resent chemistry, a tunica
case, where we are not concerned lished in fossils, such as lignin
f
witk
re,ative levels of homoplasy. However, we did layer in the apical meristem, and siphonogamy (the
n
and Pentoxylon
"Jove invariant characters with MacClade (Mad- same is also true for Bennettitales
&
n One
Maddison, 1992). All these data sets were in trees of the sort shown in Fig. 1). reason
a
^'yzed
with PAUP for the new nosition of these anciosperm taxa is
(version 3.0L, Swofford,
424 Annals of the
Missouri Botanical Garden
— * a 5
CD
u <s> X
UUZICQUS— O
IU(9U
U U U LU LU Q_
k
a- lu
E3
spongy
honeycomb
granular
30
Treelength columellar
1
:
FIGURE Representative most parsimonious tree (of 66 Chars. uncertain
1
.
equivocal
(MAGN)
94) found when "core" Magnoliales are substi-
tuted for angiosperms as a whole in the nine-angiosperm
FIGURE Representative most parsimonious tree (of
2.
analysis of extant and fossil seed plants. Shading of branch-
(NYMP)
31) found when Nymphaeales are substituted
es shows distribution of the exine structure character,
angiosperms, showing distribution of the exine struc-
for
which tends to link Magnoliales with other anthophytes
(some with angio-
PROG = ture character. Generally similar trees
"progym-
{Pentoxylon, Bennettitales, Gnetales).
when
found
ELKI = MEDU = sperms linked with Caytonia alone) are also
nosperms"; Elkinsia; Medullosaceae;
CALL = CONI = GINK = Winteraceae, Austrobaileya, eudicots, Aristolochiaceae,
Callistophyton; Coniferales;
Arrows
CORD = PELT = and monocots are substituted for angiosperms.
Ginkgoales; Cordaitales; Peltasper-
mum; CYCA = CORY = indicate possible exine states on branches where the state
Cycadales; Corystospermaceae;
GLOS = CAYT = PENT = equivocal. Other abbreviations as in Figure 1.
Glossopteridales; Caytonia; is
BENN = EPHE =
Pentoxylon; Ephedra;
Bennettitales;
WELW
= GNET =
Welwitschia; Gnetum.
putative
which maintain the
nettitales (Fig. 3b),
and Gnetales,
homologies between Chloranthaceae
symplesiomorphies.
presumably that they have columellar rather than such as compound strobili, as
granular exine structure (or both columellar and Anthophytes are not broken up in any of these
granular structure in the case of Nymphaeales,
trees.
when Piperales
which were therefore scored as uncertain), so they The most varied trees are found
when Chloran-
As
are not as strongly "attracted" to other granular are substituted for angiosperms.
these
group,
anthophytes as Magnoliales are. The exine struc- thaceae are the single angiosperm
are
ture character would have tended to associate an- include neo-englerian trees where Piperales
and trees
giosperms with other anthophytes had been Pentoxylon and Bennettitales
linked with
if it
other
group of
ordered, with columellar implicitly derived from where anthophytes are the sister
sor
granular, but does not when treated as platysperms. However, in trees of the latter
it it is
rather
but
unordered. Competing characters attracting angio- Piperales are not linked with Gnetales
1S
sperms in general to Caytonia are reticulate ve- with Pentoxylon and Bennettitales (Fig. 4).
U e
have features
nation, flat guard cells, and anatropous cupules presumably because Piperales
is
them
allow
(scored like anatropous bitegmic ovules). orthotropous and bitegmic ovules that
Gneta es.
and
As
anticipated, in most of the trees found when to be nested between Bennettitales
two-trac
and
Chloranthaceae are substituted for angiosperms (Fig. but not features like opposite leaves
Chloranthaceae^
and
3a), Chloranthaceae are linked directly with Gne- nodes that unite Gnetales
^
GnetaIe
tales, with which they share such features as op- However, Piperales are linked with
*^
re
trees
unparsimonious
posite leaves, two-trace nodes, spicate inflores- few stratigraphically
the
group at
cences (scored as compound strobili), and anthophytes form a paraphyletic
numerous
^
orthotropous ovules. In these trees, the position of of platysperms. Finally, there are
hyt
antho
anthophytes is highly unstable: they may be the in which Piperales are basal in P ^
sop.
group among Caytonia, g ^
sister of other platysperms or variously anthophytes are nested ^
as-
to tr
analogous
sociated with cycads, glossopterids, Caytonia, or and corystosperms,
terids,
*
found
a corystosperm-glossopterid- Caytonia The & Donoghue (1992) and trees
clade. Doyle
ermS
exceptions are neo-englerian trees in which Chlo- Magnoliales are substituted for angiosP
,
J
nke
are
ranthaceae are linked with Pentoxylon and Ben- and a few trees where Piperales
1),
Number 3
Volume 81 Doyle et 425
al.
,
rRNA
1994 Integration of Morphological and Data
B 3
— o o ^ a
U
a - ^
Q u U
z <s> (/>
o v
LS *uSIU© OU UUUUOODIU UUUQ.UUUOUo3
r
3 u
a. a. oo
a d a a
a
3 steps
unordered
lyginopterid]
138
Treelength:
none
67 Chars. anatropous
orthotrop
FIGURE Representative most parsimonious tree (of
4.
155) found when Piperales (PIPE) are substituted for
angiosperms, showing distribution of the cupule character.
more comparable
Other equally parsimonious trees are to
those in Figures 1, 2, and 3b. Other abbreviations as in
Figure
1.
are linked with Caytonia and/or glossopterids im-
reproductive structures
ply that flowerlike origi-
nated independently in angiosperms and the clade
Pentoxylon, and Gne-
consisting of Bennettitales,
Trees which angiosperms are linked with
tales. in
Gnetales, and/or neo-englerian trees in which an-
and Gne-
thophytes are linked with coniferopsids
HGURE
Two
3. representative most parsimonious trees
tales are basal, imply that angiosperm flowers and
(of 166) found when (CHLO)
Chloranthaceae are substi-
tuted parts, especially carpels containing several
for angiosperms, showing distribution of the phyl- floral
lot*xy (a) and strobilus (b) characters; (b) is a neo-englerian ovules with two integuments, were elaborated from
tree with
anthophytes nested among "coniferopsids" simpler structures like those of Gnetales, or derived
'ginkgos,
conifers, cordaites). Other abbreviations as in
by aggregation of several gnetalian "flowers" (i.e.,
r »gure
1.
pseudanthial interpretation).
a
These bear out the concern that the
results
irectly with Caytonia, thus breaking up the an- position of angiosperms in previous analyses (Doyle
foophytes. Presumably, & Donoghue, 1986, 1992) may have been incor-
Piperales have fewer char-
C ers tnat support any one of these arrangements rect because of initial assumptions about basal states
0v
er
another. angiosperms. They also raise the possibility that
in
e "an-
instability of angiosperm relationships seen angiosperms are polyphyletic, with different
"gymno-
'" ese experiments when giosperm" groups related to different
not evident extant
is
*X
* a,one are considered, since in almost all trees sperms." However, neither conclusion necessarily
how
'netales are depend on whether and the
the closest living relatives of angio- follows, since they
sperms
(the exceptions are the few trees in which various angiosperm groups link up with each other.
ymphaeales
and
Gnetales form a paraphyletic
group). Th
e
variations are a function of different
ANALYSES
NINE-ANGIOSPERM
at,0ns
h»ps between
angiosperms and various fos-
...
taxa we included
However, the would have To assess the possibilities just raised,
different trees
-
f
I7 ifferent angiosperm groups and analyzed the re-
implications for basic states and char- all nine
er ey random ad-
stepwise
olution matrix (35 replicates,
within the angiosperms, and this sulting
s rates TBR branch swapping). This analy>i-
the severe based on dition of taxa,
limitations of trees
92
axa most parsimonious trees of steps,
l alone yielded 1
in evaluation of evolutionary 1 1
enanos, arrangements within a clade
because of the gaps between extant which differ only in
MnodiM
cory-
Ps for nf r.nllistnnhvton. coniferopsids,
example,
trees which angiosperms
- in
426 Annals
of the
Missouri Botanical Garden
GNETAL RNGIOSPERMS
r
3
_ a ^
CD Z
lu I
u </> <s> CD
LU
CC
z!I3 (/)
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spongy
honeycomb
92
Treelength
granular
1
:
1 |
columellar
uncertain
FIGURE 5. Representative most parsimonious tree (of 11) found when all nine angiosperm taxa are included in
NYMP
= =
the analysis, showing distribution of the exine structure character. PIPE Piperales; ARIS Aristolochiaceae;
= Nymphaeales; MONO = monocots; MAGN = "core" Magnoliales; WINT = Winteraceae; EUDI = eudicots (-
= =
groups with tricolpate and derived pollen); AUST Austrobaileya; CHLO Chloranthaceae; other abbreviations as
Figure
in
1.
&
stosperms, Peltaspermum, and cycads (e.g., Fig. nious by Doyle Donoghue (1986, 1992) and
& among one
5). In these trees, angiosperms form a monophy- Donoghue Doyle 989a) are seen
1
(
letic group, and Gnetales are their closest living step less parsimonious ("one-off") trees (193 steps)
of
relatives. However, in contrast to trees of Doyle Some of these trees show the sorts
(Fig. 6).
&
Donoghue the
(1986), where angiosperms are the relationships that were most parsimonious in
sister group of other anthophytes, angiosperms which anthophytes are as-
are previous analyses, in
angio-
linked with Caytonia and when Caytonia and glossopterids,
glossopterids, as sociated with
anthophyte
Winteraceae, Austrobaileya, eudicots, and some sperms are the sister group of other
oaj.
paleoherbs were angiosperms (Fig.
substituted for angiosperms (Fig. and Magnoliales are basal in
are
2). Furthermore, the arrangement within angio- As the previous analyses, other one-off trees
in
which an-
sperms differs from any seen previously: they of the neo-englerian type (Fig. 6b), in
split
One-
and
one
into clade consisting of paleoherbs (including thophytes are linked with coniferopsids,
are
monocots) and another consisting of woody mag- with linear leaves and simple sporophyll^
tales,
anthophytes.
noliids and eudicots. As with trees where single basal and relatively pleomorphic in
w
basal
angiosperm Nymphaeales are
taxa were associated with Caytonia In other 193-step trees,
(na
and/or rRNA data
glossopterids, rearrangement from
this pre- angiosperms, as inferred .
is
e
have
&
sumably influenced by treatment of the exine struc- Zimmer, 1992); in fact, some of these t
^
ture and endexine taxafound
characters as unordered. This same arrangement of paleoherb
*^
change ^P6'*
in character analysis weakens the tendency rRNA analyses presented below, with 1
wit
of angiosperms to associate with the granular Ben- above Nymphaeales and monocots linked
•
difte^
minimal
nettitales-Pertfoxy/orc-Gnetales Given the
clade, with gran- toiochiaceae (Fig. 6c).
unwarran
ular Magnoliales attached between the latter and ences in parsimony, would be
it
W0
should
columellar angiosperms. Figure 5
conclude that the tree in
&
Although Donoghue
these results cast doubt on previous strongly preferred over those in
.
& AlihjjJ
inferences regarding the origin of angiosperms, the (1989a) or Doyle Donoghue (1992).
ia^
Magno
change from the previous situation less radical the away from a basal position of ^
is shift
than as
it seems. Essentially the same alternative re- may represent real progress, reflecting i
charac
lationships recognized as almost equally parsimo- the removal of previous biases in exine
GNETRL ANGIOSPERMS
Exine
3 steps
unordered
spongy
I
honeycomb
granular
columellar
uncertain
Sporophylls
steps
unordered
Mega comp
I
mcom
Msim
both simple
a B
* 0.
Q »
Z
u
</> </>
O
*
(•5
UJ 3Isu
ft-
Zj
0. uj O u o 3 Q_ UJ U I E
a a CD CL CJ CO CD "Z Q.
a
E3
E3 E3
spongy
honeycomb
granular
columellar
uncertain
Figure
6 nine-angiosperm data set: (a)
found with the
Representative one step less parsimonious (one-off*) trees
„ 7 r &
Donoghue
*u_ _•_. r , . i xm i:_i_ u„„„i ;„ -ngiosperms, as in Doyle
neo-englerian
tructure character; (b)
with
sporophyll character; (c)
the
Ji^J^. M
-S^P^ms linked with fW«-.„ „„j anH Nvmnhaeales basal in anciospenns, in tree* based or.
>
428 Annals of the
Missouri Botanical Garden
GNETRL HNGIOSPERMS
If
r
3
o — a
^ a.
u a
CD
<•>
a.
3
X u u u U 0. U I 3 z I
nan
LJ <_) (J3 an CD uj o. a:
a a a a a
Phullotaxy
4 steps
unordered
spiral
198
Treelength:
opposite
|
distichous
equivocal
Figure 7. Representative tree (of 1675) found when angiosperms and Gnetales are forced together and Chl—o-
ranthaceae are forced to the base of angiosperms, showing distribution of the phyllotaxy character. This tree is six
steps less parsimonious than the shortest trees. Abbreviations as in Figures and 5.
1
may
much
it be as a function of the smaller number globose pollen with reticulate sculpture and a ver-
among
of taxa and the omission of connecting groups. rucate sulcus. Similarly, Piperales are nested
Despite these ambiguities, experiments with other paleoherbs based on herbaceous habit, di>
al-
ternative topologies do provide some stronger re- tichous leaves, palmate venation, and globose pol-
The
most Chloranthaceae
sults. interesting experiments concern Of homologies of
len. the potential
nodes
proposed links between Gnetales and Chlorantha- and Gnetales, opposite leaves and two-trace
ceae. Trees with angiosperms angiosperms in trees
forced together with are unequivocally primitive in
Gnetales using the constraints option in PAUP are Figure since they also occur in Austro-
like 7,
have
only two steps longer than the shortest trees, but baileya. However, compound strobili would
Chloranthaceae equally
are not basal in angiosperms, as to be lost below Austrobaileya, so it is
might be expected from their gnetalian features; parsimonious to assume that this feature originated
Gnetales.
instead, angiosperms are arranged as in the most independently in Chloranthaceae and
are
parsimonious The Chloranthaceae
trees (Fig. 5). shortest trees with Other "gnetalian" features of
'**
Chloranthaceae basal in angiosperms and angio- problematical morphologically and were thcl
f
sperms microsporophy Is,
linked with Gnetales unknown whorled
(Fig. 7) are six steps scored as (e.g.,
con-
are
longer than the shortest trees. Similarly, in the neo- one ovule per carpel). As a result, they
and
englerian Chloranthaceae
trees (Fig. 6b), anthophytes are not ar- sistent with a link between
suM
ranged in such a way that the similarities between Gnetales when Chloranthaceae alone are
"
*
attra
Gnetales and Chloranthaceae are homologous; in- tuted for angiosperms, but they do not
*
*
stead, angiosperms are linked with Bennettitales, Chloranthaceae to the base of angiosperms
*
and Finally,
Magnoliales are basal in angiosperms. nine angiosperm taxa are included.
all »
The reason Gnetales in
that trees of the type in Figure 7 though Chloranthaceae are like
Gneta
are so unparsimonious, even though more like
Chlorantha- respects, Magnoliales are
*
ceae are associated with Gnetales when they are others leaves without chloranthoid teeth;
(e.g.,
structw^
the only angiosperms exine
in the analysis, presumably shaped granular
is pollen; tectate,
^
analy"
that Chloranthaceae are "screened off' from hav- The strongest conclusion of these
m
ing an influence on the position of angiosperms by that both angiosperms and Gnetales are °^,
being Figure
linked with Austrobaileya and other groups, groups. In the tree shown in
letic . •
an
based on such nine
features as laterocytic stomates and are unambiguously supported by