Download A phylogenetic analysis of the land plants

RiologicalJoumalafthe LinneanSouety, 13: 225-242. With 5 figures
May 1980
A phylogenetic analysis of the land plants
LYNNE R. PARENTI"
Department of Ichthyology, Amer%cunMuseum
Central Park West at 79th Street, New York
NY 10024, U.S.A.
of Natural History,
Accepted for publication January 1980
Phylogenetic systematics (cladistics)is a theory of phylogeny reconstruction and classification widely
used in zoology. Taxa are grouped hierarchically by the sharing of derived (advanced) characters.
The information is expressed in a cladogram, a best estimate of a phylogeny. Plant systematists
generally use a phenetic system, grouping taxa on overall similarity which results in many groups
being formed, at least in part, on the basis of shared primitive characters.
The methods of phylogenetic systematics are used to create a preliminary cladogram of land
plants. The current classificationof land plants is criticized for its inclusion of many groups which are
not monophyletic.
Objections to the use of phylogenetic systematics in botany, apparent convergences within major
groups and frequent hybridization, are shown to be invalid. It is concluded that cladistic analysis
presents the best estimate of the natural hierarchy of organisms, and should be adopted b y plant
systematists in their assessment of plant interrelationships.
KEY WORDS:- cladistics - land plant classification - land plant interrelationships
systematics - plant systematics.
- phylogenetic
CONTENTS
. . . . . . . . . . . . .
. . . . . . .
. . . . . . .
Conclusion . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . .
References . . . . . . . . . . . . . .
Introduction
A cladistic analysis of land plants
Objections to cladistic analysis
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
. . . 225
. . . . 228
. . . . 240
. . .
24 1
. . . 24 1
. . . 242
INTRODUCTI0N
Previously published classifications of the land plants (Embryophyta or
Embryobionta) and their accompanying evolutionary diagrams have been
proposed as attempts at naming so-called natural groups and placing such
groups in some ancestor-descendant position relative to each other (e.g.
Cronquist, 197 1; Foster & Gifford, 1974). One classification and scheme of interrelationships of land plants that is widely accepted by plant systematists is that of
* Also at: Department of Biology, The City College, City University of New York, Convent Avenue and 138th
Street, NewYork, NY 10031, U.S.A.
0024-4066/80/090225
+ I8 S02.00/0
225
8 1980 The Linnean Society of London
L. R. PARENTI
226
Cronquist (197 l ) , see Fig. 1 . Based explicitly on a concept of overall similarity, it
is the classification of an evolutionary taxonomist (in the sense of Mayr, 1965)
for, in describing the ongoing work of plant taxonomists, Cronquist (197 1 : 80)
states: “The development of a natural system, in which plants are classified
according to the totality of their similarities and differences, has occupied the
MAGNOLIOPHYTA
I
1
PI NOPHYTA
Gnet icae
I
I
-1
RHYN IOPHYTA
I
‘i
BRYOPHYTA
Anthocerotopsida
Marchantiopsida
Embryobionta
Thallobionta
CHLOROPHYTA
C harophyceae
1
Chlorophyceae
T
I SCHIZOPHYTA I
Figure I , A classification and largely phenetic diagram ofplants. (After Cronquist, 197 1 :82, fig. 6.2).
LAND PLANT PHYLOGENY
22 7
attention of post-Linnean (and some pre-Linnean) taxonomists to this day, and
it is not satisfactorily completed.”
The purpose of the present paper is not to assess how well botanists have done
in their attempts to produce a natural classification, but to propose an alternative method of analysis in their systematic work. In light of zoologists’ recent
discoveries of the usefulness of cladograms as expressions of estimates of the
phylogenies of groups of animals (as presented by Hennig, 1950, 1966, and
modified by many subsequent authors, including Brundin, 1966, 1968; Nelson,
197 1, 19721, and their usefulness for making testable hypotheses about a group’s
distributional history (as in Platnick 8c Nelson, 19781, it seems desirable and even
necessary for such cladograms to exist for plants. It is desirable in the sense that
groups would be defined genealogically and the concept of closeness of
relationship would be presented as the groups’ inferred descent from a common
ancestor as determined by the sharing of specialized characters by all members of
the group (Hennig, 1950). I t is necessary if we are to use plant distributions to
infer general biogeographic patterns (e.g. Platnick & Nelson, 1978; Rosen, 1978).
Also, i t is a way we can adopt a common universal language, a necessity if we
wish to understand the phylogenetic hypothesis underlying classifications.
Cronquist’s ( 197 1) classification is used as a basis for criticism since it deals with
the land plants as a whole, even though other and more recent, largely phenetic
analyses of groups of plants exist (see Kubitski, 1977).This classification was also
chosen since both a diagram (Fig. 1) and written classification (Table 1) were
presented.
In the current classification (Fig I), many of the large divisions of the
Embryophyta, for example the Bryophyta, are not monophyletic in the sense that
each group does not include all the descendents, and only the descendents, of a
single hypothesized stem species. Perhaps more importantly, the question of the
interrelationships of many of these named taxa has all but been ignored. Thus,
four major groups of embryophytes, the ferns (Polypodiophyta), the naked ferns
(Psilotophyta), the club-mosses (Lycopodiophyta) and the horsetails
(Equisetophyta)are depicted in Fig. 1. as derivatives of the Rhyniophyta, primitive
fossil land plants, with no indication that this is equivalent to a statement that their
interrelationships are unresolved, and encourage further investigation. Similarly,
the Lyginopteridopsida is depicted as the ancestor of the flowering plants
(Magnoliophyta),with other gymnosperm (Pinophyta)groups presented as other
lineages at different hierarchical levels; the consequence of this practise is that the
figured dendrogram and the written formal classification (Table 1) are not
equivalent. The diagram and formal classification purport to be summaries of the
same information about the same group of plants. However, if we compare a
cladogram of the relationships expressed in Cronquist’s diagram (as shown in Fig.
21, with a cladogram of the information contained in the formal classification (as
shown in Fig. 31, we see that their contradictions are many. Are the green algae
(Chlorophyceae and Charophyceae) a group, and if so, are the two classes more
closelyrelated to the land plants or to the rest of the plants commonly known as the
algae and fungi? The formal classification (Table 1) and its cladistic information
(Fig. 3), clearly indicate that these groups (2a and 2b) are to be considered merely
as two more groups of algae. With Cronquist’s diagram (Fig. 1) and the cladistic
information contained in it (Fig. Z), this question is still not resolved. The
Chlorophyceae is shown to be no more closely related to the algae and fungi than
L. R. PARENT1
228
Table 1. The classification of plants, from Cronquist (197 1 : 85-86)
Subkingdom
Division
Class
Class
Division
Class
Class
Division
Class
Division
Class
Division
Class
Class
Division
Class
Class
Class
Class
Division
Class
Class
Class
Division
Class
Class
Division
Class
Class
Class
Class
I.
1.
la.
Ib.
2.
2a.
2b.
3.
3a.
4.
4a.
5.
5a.
5b.
6.
6a.
6b.
6c.
6d.
7.
7a.
7b.
7c.
8.
8a.
8b.
9.
9a.
9b.
9c.
9d.
Thallobionta
Schizophyta
Schizomycetes
Cyanophyceae
Chlorophyta
Chlorophyceae
Charop hyceae
Euglenophyta
Euglenoph yceae
Cryp top hyta
Cryptop hyceae
P yrrophyta
Desmoph yceae
Dinophyceae
Chrysophyta
Chloromonadoph yceae
Xanthophyceae
Chrysophyceae
Bacillariophyceae
Phaeophyta
Isogeneratae
Heterogeneratae
Cyclosporae
Rhodophyta
Bangiophyceae
Florideaphyceae
Fungi
Myxom ycetes
Phycomycetes
Ascomycetes
Basidiornycetes
Subkingdom
Division
Class
Class
Class
Division
Class
Division
Class
Division
Class
Class
Division
Class
Class
Class
Division
Class
Division
Subdivision
Class
Class
Class
Subdivision
Class
Class
Subdivision
Class
Division
Class
Class
11.
10.
IOa.
lob.
10c.
11.
Ila.
12.
12a.
13.
13a.
13b.
14.
14a.
14b.
14c.
15.
15a.
16.
16a.
16al.
16a2.
16a3.
16b.
16bl.
16b2.
16c.
16cl.
17.
17a.
17b.
Embryobionta
BryOPhYta
Anthocerotopsida
Marchantiopsida
Bryopsida
Rhyniophyta
Rhyniopsida
Psilotophyta
Psilotopsida
Lycopodiophyta
Lycopodiopsida
Isoetopsida
Equisetophyta
H yeniopsida
Sphenoph yllopsida
Equisetopsida
Polypodiophyta
Polypodiopsida
Pinophyta
Cycadicae
Lyginopteridopsida
Bennettitopsida
Cycadopsida
Pin icae
Ginkgoopsida
Pinopsida
Gneticae
Gnetopsida
Magnoliophyta
Magnoliopsida
Liliopsida
to the land plants; and, the Charophyceae is depicted as a derivative of the
Ch lorophyceae.
This depiction of land plant interrelationships as poorly known is not based
on a lack of data, on an inability to assess primitive or derived characters, or on a
lack of concern by botanists. It is a result of plant systematists working toward an
artificial system based on a concept of overall similarity (the sum of all known
primitive and derived traits) rather than on a strictly genealogical one which
incorporates only shared derived characters, In fact, it has been just this reliance
on the sum of all evidence that has led Cronquist (1971 :676-677): to state, after
listing characters of the flowering plants: “One of the greatest difficulties in the
use of these characters is that some sort of change has occurred repeatedly in
different groups (parallelism) so that sharing of one or a few advanced characters
is no guarantee of relationship.” Surely no character comes with a guarantee,
but if we call a character advanced, in a cladistic classification by definition we
mean that it is uniquely derived and suggests a closer affinity among those taxa
that share it.
A CLADISTIC ANALYSIS O F LAND PLANTS
The advantage a formal cladistic analysis of land plants has over the current
methods becomes apparent when one compares these largely phenetic classi-
229
LAND PLANT PHYLOGENY
SCHIZOPHYTA - 1
RHODOPHY TA - 8
PHAEOPHY T A - 7
CHRY SOPH Y T A- 6
PY RROPHY TA-5
CRY PTOPH Y TA- 4
EUGLENOPHYTA-3
///
CHLOROPHYCEAE -2a
-CH AROPHY CEAE -2b
MARCH ANT I0P S IDA -10 b
BRYOPSIDA-10c
RHYNIOPHYTA-11
LYCOPODIOPHYTA- 13
EQU ISETOPHYTA- 14
P S I LOTOPHYTA-12
LYGINOPTER IDOPSIDA-16al
BENNETT I TOPSIDA-16a2
CYCADOPS I DA-16a3
MAGNO L I0PH Y TA 17
-
GNETICAE - 1 6 ~
P I N ICAE-16b
POLY PODIOPHYTA -15
Figure 2. Cladogram of the relationships, as expressed in Fig. 1 of the indicated monophyletic
groups. Numbers following taxa are the same as for those in Table 1 .
fication schemes with a cladistic (genealogical) classification, as presented in
Fig. 4. This cladogram resolves many of the cases of unknown relationship, as
pointed out above. A well-constructed cladogram is preferred over the phenetic
classification if it can present tentative solutions to these problems.
Attempts at more rigorous techniques to classify taxa are not new to botany.
Wagner’s (1961) classic paper on the classification of the ferns called for an
analysis of characters as generalized or specialized. Furthermore, Wagner’s
230
L. R. PARENTI
Figure 3 . Cladograin of the relationships as expressed in the classification ofTable 1, with numbers
referring to the same groups.
procedure for reconstructing a phylogenetic tree is consistent with the phylogenetic principles of Hennig ( 1966), as pointed out by Farris, Kluge & Eckhardt
(1970).
Bremer & Wanntorp (1978) discussed generally the application of phylogenetic
systematics to botany. They included examples of the interrelationships among the
major angiosperm taxa, showing that the dicots do not constitute a monophyletic
23 I
LAND PLANT PHYLOGENY
CHLOROPHYC EAE
CHAROPHYCEAE
MARCHANTIOPSIDA
BRYOPS IDA
A N THOC E ROT 0PS IDA
R H Y N IOPHYTA
PSI LOTOPHYTA
LYCOPODIOPHYTA
EQUISETOPHYTA
POLY POD1OPHYTA
LYGI NOPT ER IDOPS IDA'
BENNETTITOPSIDA'
CYCADOPS I D A
M A G N O L IOPSlD A
17
Figure 4 Cladogram of the major groups of land plants and their closest relatives supported by the
derived characters at each node identified in Table 2. The more derived taxa occured within the higher
numbered nodes.
group, a topic taken up in some detail in the present paper, and of the effect of
cladistic analysis at the generic level.
0ther workers have either applied cladistic methodology (Praeger, Fowler 8c
Wilson, 19761, or have criticized the manner in which it has been applied (Farris
L. R. PARENTI
232
8c Kluge, 1979); however, the methodology has had a limited application in the
tield of botanical systematics. The cladogram of Fig. 4 represents the first
published attempt at applying the concepts of phylogenetic systematics
(cladistics) to the land plants as a whole, and as such, will be subject to rearrangement and refinement by future workers.
Even though many of the major groups of land plants are not monophyletic,
their names have been retained here to permit an easier understanding of the
nature of their preliminary interrelationships. In fact, the branching structure of
the cladogram suggests that the majority of the groups are not monophyletic, but
are rather grade level assemblages. That is, even though no derived character is
given to define the ferns, they are presented as primitive to the seed plants, yet
more advanced than the other land plants. It is possible that some group of ferns
is more closely related to the seed plants than to other ferns; however, this
problem is only considered in the treatment of the Bryophyta and Pinophyta.
In addition to more complete interrelationships of members of the groups
being presented, a striking difference between the cladogram (Fig. 4)and Fig. 1 is
that, in the cladogram, ancestors (taxa at nodes) are not recognized. This is true
whether the taxa being analysed are fossil o r recent. Recent taxa are not
recognized as ancestors of other recent taxa because contemporaneous taxa
cannot logically be ancestral to each other (see Patterson 8c Rosen, 1977, for a
complete discussion). Therefore, Cronquist’s Pinophyta (here Pinicae, Lyginopteridopsida, Bennettitopsida, Cycadopsida and Gneticae) is not depicted as the
ancestor of the Magnoliophyta. Instead, the group of the Pinophyta which shares
derived characters with the Magnoliophyta is treated as a distinct group, the
Gneticae (minus Ephedra) and presented as the sister taxon of the flowering
plants. Stated another way, the Gneticae and Magnoliophyta are hypothesized to
share a comtnon ancestor not shared by other Pinophyta.
Furthermore, contrary to Sporne (19761, the inclusion of fossil taxa is not
considered critical in deciding if a character is primitive or derived. Characters or
character complexes recognized as being unique are assessed as derived. The
Table 2. Derived characters (listed in Table 3) for each node in the cladogram of
Fig. 4. (see text for discussion)
Node
1
2
3
4
5
6
7
8
9
10
II
12
I3
14
15
16
17
Name of inclusive taxa
Derived characters
Chlorophyta and Embryophyta
Unnamed group
Embryophyta
Unnamed group
Unnamed group
Vascular plants
Unnamed group
Unnamed group
Unnamed group
Unnamed group
Seed plants
Unnamed group
Unnamed group
Unnamed group
Unnamed group
Magnoliophyta
Liliopsida
A2, 02, C2
D2, E2
F2, G I , H2,XZ
I2
G2, E3
52, K2, G3
L2, M2
Q2, (W2)
L3, M3, N 2 ( o r N 3 )
L4, M4
P2, T2, R2
v3
0 2
0 3 , V4, W3
D3, J3. K3, R3, U2, V5
S2, V6
N4, P3, V7
LAND PLANT PHYLOGENY
233
Table 3. Characters and their primitive and derived states*
Character
States
A. Plastid pigments
B. Storage olstarch in chloroplasts
C. Cell wall components
D. M ulticellular gametangia
( 1 ) absent (2)present
( 1 absent (2) present
E. Apical meristeins
F. Altc.rnation ot generations
G . Development ofsporophyte
H. Sporangia
1. Stomatrs and guard cells
J . Xylen1
K. Phlocin
L. Position ofsporangia
M . Leavrs on sporophyte
N . Slelar patter11
0 . Pollc11 tube
P. Colylrdons
Q. Roots
R. Integument around ovule
s. Ovary
T. Rrtention orspores in
nirgasporangiuin
U . Origin ol'teinale gametophyte
V. Sporophylls
W. Secondary growth
( 1 ) absent (2)present
( 1 ) absent (2)present
(3) archegoniurn lost
(l)absent(2)present
(3) present in sporophyte
( I ) isomorphic (2)heterornorphic
( I ) dependent o n gametophyte
( 2 )elaborate sporophyte, reduced garnetophyte
( 3 )sporophyte physiologically independent at
maturity
( 1 ) unicellular (2)multicellular
( 1 ) absent ( 2 )present
(I)absent (2) present
(3) present with vessels
(l)absenr(2)prese1it
( 3 )present with companion cells
(1) terminal on an axis
( 2 )distributed randomly on short branches
(3)localized on lower branches
( 4 ) present generally on lateral appendages
( 1 ) absent (2)microphyllous and veinless
( 3 ) rnegaphyllous with branching venous system
( 4 ) Divided into blade and petiole
( 1 ) protostele (2) siphonostele
(3) dictyosrele (4) atactostele
( 1 ) absent (2) present
(31 present with loss of motile gametes
( 1 ) many (2) two (3)one
( 1 ) absent (2)present
( 1 ) absent (2)single layer (3) double layer
( 1 ) absent (2)present
not retained (2) retained
( I ) rnonosporic ( 2 ) tetrasporic
(1) absent ( 2 ) present
(3) megasporophylls and microsporophylls
aggregated into compact terminal strobili
(seed and pollen cones)
(4) seed cone compound
( 5 ) pollen cone compound
( 6 ) differentiated into sepals and petals
( 7 ) reduced number due to fusion
( 1 1 absent
(2) division of an incomplete ring of
vascular cambium
(3)division o f a complete ring of
vascular cambium
( 1)
X. Centrioles during somatic
cell division
( 1 1 fbrrned (2)not rormed
.:' State ( 1 ) is the primitive state of the character as considered in the present paper; (2)is the derived state. For
transition series with more than two states, the further derived states ofthe character are listed as states (3),(4) etc.
234
L. R. PARENT1
general condition among the land plants is initially assessed as primitive;
however, such a condition may be derived, and this can only be determined if it is
correlated with other derived characters.
A large number of the characters discussed by Cronquist (1971) and Foster &
Gif’ford (1974) have been analysed to determine their distribution among the
land plants and to assess for each which states are primitive and which are
derived, in order to create the preliminary cladogram of the major groups
presented here (Fig. 4). The derived characters found in those plants above each
node are listed in Table 2. The characters and their primitive and derived states
are listed in Table3.
The characters for each node are found in that state in all plants above it, or in
some further derived state, thus describing a transition series. Assuming that
evolution involves the transformation of characters from one state to another, a
transition series is the hypothesized dequence of transformation of character
states for a given character (Hennig, 1966).
Listed for node 1 are those derived characters found in the Embryophyta and
the two classes of green algae. These are the sharing of plastid pigments, or
proportions of such pigments, found in no other plants (chlorophyll b,
phytochrome, carotenoids a and b with carotene a present in the highest
proportions, and xanthophylls, principally lutein); unique storage of starch
within the chloroplast; and unique components of the cell wall (including
polyphenols, cellulose, hemicelluloses and hydroxyproline (Cronquist, 197 1 :
140ff., 28 Iff.; Bremer & Wanntorp, 1979b, unpublished data). These characters
support the idea that the green algae are more closely related to the embryophytes
than to any other algal or fungal group. Surely, then, we cannot consider the
Chlorophyceae to be in any way ancestral to the Fungi and other algal groups, as
indicated in Fig. 1 .
The green algae itself is a paraphyletic group as evidenced by the fact that the
Charophyceae may be interpreted as being more closely related to the land
plants than the Chlorophyceae. A monophyletic group, in the sense of Hennig,
contains all the descendents, and only the descendents, of a common ancestor.
Members of a monophyletic group share uniquely derived characters. A
paraphyletic group, on the other hand, contains members who share primitive
characters. Both the Charophyceae and land plants possess multicellular
gametangia, and are capable of developing apical meristems (Cronquist, 197 1 :
160, 2821, thus, together they form a monophyletic group. Members of the
Chlorophyceae have either one or both of the latter two mentioned characters,
indicating that they are more closely related to the Charophyceae-Embryophyta
group than to the rest of the algae, and that the Chlorophyceae is not likely to be
a monophyletic group.
The association of the green algae and the land plants would require a formal
recognition of such a taxon by giving it a name, such as the ‘Chlorobionta’, also
suggested by Bremer 8c Wanntorp ( 1 979b, unpublished data). The Thallobionta,
the group to which the green algae now belong, is now a paraphyletic group; i.e.
based on a set of primitive ‘non land-plant’ characters such as leaves and roots
absent, etc.
The Embryophyta is a well-defined taxon whose outstanding derived features,
listed for node 3, may be explained as follows. All land plants exhibit a
heteromorphic alternation of haploid and diploid generations, as opposed to an
LAND PLANT PHYLOGENY
235
isomorphic alternation in most of the green algae. The sporophyte always begins
its development within the tissue of the gametophyte. The mode of cell division is
unique in that n o centrioles are formed during somatic cell division. In addition,
the sporangia are multicellular rather than unicellular.
The Bryophyta, liverworts and mosses, are depicted in Fig. 1 as being primitive
to the rest of the land plants. A preliminary analysis also agrees with this diagram
by indicating that the bryophytes d o not constitute a monophyletic group.
Cronquist assesses the Anthocerotopsida as being more closely related to the rest
of the land plants than to either the Marchantiopsida or Bryopsida, which are
indicated as sister taxa primitive to all other land plants. Therefore, in the
cladogram of Fig. 4,the term Bryophyta, which does not indicate a monophyletic
group, is not used, and the three groups are treated separately.
Critical to an understanding of the relationships of these three groups to each
other and to the vascular plants in general is a sound interpretation of‘ the
phylogenetic significance of the relative size of the sporophyte and gametophyte
in each of the groups. In all vascular plants the sporophyte is the conspicuous
generation, and is fully independent of the gametophyte at maturity. In general,
bryophytes have a large gametophyte and much smaller sporophyte. In the
Anthocerotopsida, however, the sporophyte is much more elaborate than in the
Bryopsida o r Marchantiopsida. Also, both the Anthocerotopsida and Bryopsida
have stomates on their sporophytes, an advanced character that they share with
the vascular plants. Cronquist, in summarizing his viewpoint on this problem,
states (197 1 : 304-305): “ I t has traditionally been thought that the bryophytes
represent a more or less direct link between the green algae and the vascular
plants, and that the evolution of the land plants from the green algae follows a
course of progressive elaboration of the sporophyte accompanied by a reduction
of the gametophyte. The more general view today is that the bryophytes are
derived from the green algae through pre-rhyniophyte ancestors in which both
the gametophyte and the sporophyte were green and physiologically independent.. . One of the most convincing bits of evidence pointing to the
derivation of the bryophytes from ancestors with more complex sporophytes is
the presence of stomates on many bryophytic sporophytes in which they have
little or no functional importance. The stornatal apparatus is a complex
evolutionary adaptation. . . It is not likely that such a mechanism would arise in
advanced of the need.”
However, a scheme of interrelationships agreeing more or less with the
traditional viewpoint, as expressed in the cladogram of Fig. 4, is more
parsimonious than one in which bryophytes with stomates and moderate
sporophytes are considered to be retaining primitive characters. This is also
supported by the fact that both the Anthocerotopsida and the vascular plants
have a meristematic region in the sporophyte.
One character which conflicts with this scheme is the presence of granular
chloroplasts in both the Bryopsida and vascular plants. The Anthocerotopsida
have the apparently primitive structure of one chloroplast per cell with a
pyrenoid. However, among the plants possessing stomates, the Bryopsida shares
granular chloroplasts, while the Anthocerotopsida shares an elaborate
sporophyte and reduced gametophyte, plus a meristematic region in the
sporophyte, with the vascular plants. We may make a decision concerning these
relationships if we invoke the principle of parsimony. It is not assumed that
12
236
L. R . PARENT1
evolution follows the most parsimonious course. However, an hypothesized
phylogeny should give the most parsimonious explanation of all data, since, by
definition, it requires that we make the fewest assumptions about character
transformations.
The unique characters which define the rest of the Embryophyta, the group
commonly known as the vascular plants, are the presence of xylem and phloem,
and the physiological independence of the sporophyte from the gametophyte at
maturity (Cronquist, 197 1 : 307 ff.).
The Rhyniophyta of Fig. 1 is composed of various primitive fossil land-plant
genera o fdoubtful affinities. They range in complexity from the rootless, leafless,
dichotomously branching stems with terminal sporangia as in the Silurian
Cooksonia and Devonian Rhynia, to the Devonian Asteroxylon which has microphyllous leaves (without vascular tissue), a layer of phloem surrounding a central
strand of xylem, and sporangia borne singly o n short projections from the stem
and scattered among the leaves. The rhizome also has slender branches which are
repeatedly forked, and may be true vascular roots.
The placement of the genus Asteroxylon within node 8 o n the cladogram is
dependent upon the interpretation of the anchoring structures of the genus as
true roots. Psilotophytes have rhizomes which are undifferentiated from the
stem. In Asteroxylon, the rhizomes have slender branches which themselves are
further branched. I t is assumed that these structures served in anchoring and
absorbing. They are hypothesized to have been at least more differentiated than
the rhizomes of the psilotophytes. If we do not wish to call them true roots, then
they may be called a stage in the transition series from the rhizomes as in
psilotophytes to the roots which are differentiated from the stem in higher
plants.
It must be emphasized that the statement that two structures are homologous
is an hypothesis (Wiley, 1975). That Asteroxylon has true roots may be refuted or
supported by additional information from the same or different system. Only by
pointing out such derived similarities do we encourage the further investigation
of this structure.
Transition series, as defined previously, within several character complexes, as
analysed below, allow for a preliminary reorganization of the rest of the named
taxa into a scheme of interrelationships.
The sporangium of land plants is primitively terminal on the branching axis,
and unprotected. It becomes progressively more protected and also restricted to
the lateral appendages, the most derived form being seen in the flowering plants in
which the sporangia are located in specific structures called flowers.
In Rhyniophyta, minus Asteroxylon, the sporangia are borne terminally o n an
axis. All those plants above node 7 o n the cladogram have a more specialized,
much less random arrangement of the sporangia. They are not terminal o n an
axis, and are primitively borne o n specialized very short lateral appendages in the
leafaxil, as in the psilotophytes (Cronquist, 197 1 : 308 if.).This group of plants is
well-defined by the fact that ‘leaves’ on the sporophyte (primitively microphyllous and without a complex venous system) are present in all members.
The Lycopodiophyta and Equisetophyta are depicted in Fig. 1 as being no
more or less closely related to the rest of the land plants than the other
rhyniophyte derivatives. However, in these two taxa, the ferns, and the seed
LAND PLANT PHYLOGENY
23 1
plants, true vascular roots are present, suggesting they all share a common
ancestor.
In the Equisetophyta, the ferns and the seed plants, the sporangia are localized
and found on complex branches with the sporangia often fused to the leaves.
Steles in all are primitively siphonostelic; that is, there is a central core of pith in
the stem.
The many types of stelar patterns within the land plants obscures the
relationship of one type to another. The most primitive type of stele within
vascular plants is the protostele; that is, a central strand of xylem is surrounded
by a sheath of phloem. There is no pith. I t is characteristic of primitive land
plants such as Rhynia . In psilotophytes and lycopodiophytes, the stele is generally
actinostelic; in cross-section the xylem is star-shaped, and there is no pith.
In all taxa above node 9, there is a pith in the centre of the stem; that is, the
stelar pattern within these plants is primitively siphonostelic. The siphonostelic
pattern is modified in Equisetophyta, most ferns, cycads, conifers, and
angiosperms into the dictyostelic pattern (or some further modification of it).
The primary vascular tissue is interrupted by leaf and branch gaps and forms a
ring of vascular bundles.
The typical monocot stele has vascular bundles scattered throughout the
parenchyma; it is atactostelic. In such a stem there is no well-defined pith. This is
interpreted as an advanced stelar pattern. Therefore, the transition series of these
four patterns would be from the primitive complete vascular ring (protostele), to
a ring with pith (siphonostele), to an interrupted ring (dictyostele) forming
vascular bundles, to a complete scattering of the vascular bundles (atactostele).
There are other types of steles within the land plants; however, many unique
forms undoubtedly define small groups of plants and cannot be readily
incorporated into a transition series which would define relationships among all
the plants.
The stelar pattern and further derived state of leaves having a branching
venous system constitutes support for the hypothesis that the taxa included above
node 9 form a more advanced group of land plants.
The true ferns (Polypodiophyta) and the seed plants are related to each other
on the cladogram in the same manner as in Cronquist’s diagram (Fig. 1 ) . This
association may be formally defined by the characters listed for node 10 which
follow.
The leaves are megaphyllous, and, in addition to having a branching venous
system, are differentiated into blade and petiole. The sporangia of these plants
are generally associated with lateral appendages. Thus, the states of leaf
characteristics used in this analysis may be represented in a transition series as
follows: leaves on the sporophyte present or absent; if present, megaphyllous
with a branching venous system or primitively microphyllous with no veins; if
megaphyllous, divided into blade and petiole or primitively undivided. The
presence of leaves is used to unite the land plants above node 7. Megaphyllous
leaves are present in all the land plants above node 9. Megaphyllous leaves
differentiated into blade and petiole unite all taxa above node 10 into a
monophyletic group.
The seed plants, commonly known also as the gymnosperms and angiosperms,
form a well-defined group. Their shared derived characters, listed for node 11,
include the formation of true seeds and a unique heterospory (true seeds are
238
L. R. PARENTI
formed as a result of the retention of spores within the ovule, and are distinguished from other such retention of spores by having a dormancy period.
The megaspore completes its development into the female gametophyte while
enclosed within the megasporangium. After fertilization, the embryo sporophyte
begins its development while still enclosed within the female gametophyte.); the
development of a new structure, a single, presumably protective layer around the
ovule, called an integument; and, a reduced number of cotyledons (Cronquist,
197 1: 382 ff.).
As for the Bryophyta, the main groups of seed plants (Pinophyta) will be
treated separately since Cronquist plainly indicates (Fig. 1) that they do not
constitute a distinct lineage. The two fossil groups, Lyginopteridopsida and
Bennettitopsida, are placed o n the cladogram using the data available o n their
anatomy and certain assumptions about their physiology.
The seed plants, except the Lyginopteridopsida, have megasporophylls and
microsporophylls, those leaves associated with the megasporangium and the
microsporangium, aggregated into structures which cover the seed and pollen,
respectively. Each such structure is called a strobilus in the Cycadopsida and
Bennettitopsida, a cone in the Pinicae and Gneticae, and a flower in the
Magnoliophyta. Thus, these three structures are considered to be homologous.
The complex nature of the cone obscures its relationship to the stobilus and the
Rower (see Florin, 1944a,b). However, the possession of such a complex
structure is a derived character used to unite the plants above node 12 into a
monophyletic group.
The living cycads, and Ginkgo, have a primitive pollen tube; its function is the
absorption of food materials. At fertilization, the base of the tube bursts releasing
flagellated male gametes, any of which may enter an archegonium and fertlize the
egg.
The pollen tubes of the Pinicae, Gneticae and Magnoliophyta carry nonflagellated male gametes directly to the archegonium or embryo sac. The Pinicae
and Gneticae also possess a compound seed cone comparable to an inflorescence
in the angiosperms.
These three groups and Ginkgo, except for even more derived angiosperm
groups such as the monocots, exhibit secondary growth achieved by the division
of a complete ring of vascular cambium (Cronquist, 197 1 :402 ff.). This differs
from the secondary growth of the fossil lycopod group, Lepidodendrales, which
often has an incomplete ring (Cronquist, 197 1 : 336). Thus, Ginkgo may best be
described as more closely related to these three groups than to the cycads.
Within this group, the Gneticae and Magnoliophyta form a subgroup in which
both have a second integument around the ovule, vessels in the xylem,
companion cells in the phloem, and compound strobili comparable to inHorescences for both the seed and pollen cones in the Pinicae. Also, both the
Gneticae (minus Ephedru) and the flowering plants do not have an archegonium,
the loss of which may be interpreted as a derived character uniting the two into a
monophyletic group. This is further supported by the fact that Gnetum and
Welwitschia have a female gametophyte which is tetrasporic in origin, a condition
limited within the seed plants to these two genera and certain angiosperms
(Foster & Gifford, 1974:542). (Ephedru is better represented as more closelyrelated
to the Gneticae and Magnoliophyta).
LAND PLANT PHYLOGENY
239
This scheme rejects the contention of many authors that the seed plants should
be represented as two distinct lines of evolution, one a cycadophytine line
including cycads, Bennettitopsida, Lyginopteridopsida, Cneticae and
angiosperms, and the other a pinophytine line including Ginkgo, taxads and the
conifers. It is true, for example, that the strobilus of Cycus resembles a primitive
flower more than any other conifer cone; however, the scheme presented here is
based on the contention that this resemblance is primitive and that there are
several derived characters that indicate the conifers, flowering plants and the
Cneticae are more closely related to each other than each is to the other
cycadophytines, or any other group of plants.
The flowering plants have a number of derived characters which define them
as a monophyletic group. Included are the development of an ovary, a portion of
the newly formed carpel which partially or completely encloses the ovule and
young seeds; and the development of sporophylls into specialized sepals and
petals.
In the Pinophyta of Fig. 1, the ovules and seeds are exposed, a clearly primitive
condition. They also have a multicellular female gametophyte consisting of up to
several thousand cells. These develop into the food storage tissue of the seed. The
female gametophyte of flowering plants is very reduced and does not function for
food storage.
The Liliopsida, or monocotyledons, exhibit advanced states of characters
found in the rest of the flowering plants. The stelar pattern is unique in having
the vascular bundles completely scattered. The number of cotyledons is reduced
to one. The number of floral parts (sepals, petal, etc) is reduced, mainly by a
fusion of parts.
Thus, the monocotyledons appear to be a monophyletic group. The
Magnoliopsida, or dicotyledons, on the other hand, is not monophyletic on the
basis of having two or more cotyledons and many floral parts, the main
characters by which the taxon is currently defined. These are primitive characters
for flowering plants.
If the dicotyledons do not constitute a monophyletic group, do we wish to
retain this category in a classification of land plants? The basis of cladistic
classification is the naming only of monophyletic groups, and if followed strictly,
calls for the disbanding of the group Magnoliopsida into monophyletic groups
which can be related in increasing levels of generality to each other and to the
Liliopsida.
Bremer & Wanntorp (1978) have expressed the same opinion about the
classification of the angiosperms, and recommend that the group be classified
cladistically.
Monophyletic groups, such as the ‘Chlorobionta’ (Embryophyta and
Chlorophyta) may be so renamed when they are more formally defined. I t is a
common practise of cladists to give monophyletic groups the same rank as their
sister taxa to facilitate the reconstruction of a cladogram from a classification (see
Nelson, 1973; also for other discussions of cladistic classification see Farris,
1976; Patterson & Rosen, 1977). However, no further recommendations for a
reclassification of the land plants will be made at this time, although, it is evident
that such a reclassification would reflect more explicit statements about plant
interrelationships like the one presented here.
240
L. R. PARENT1
OBJECTIONS TO CLADISTIC ANALYSIS
An objection made frequently by both zoologists and botanists is that plants
cannot be analysed by cladistic methods because plants hybridize regularly in
nature (McNeill, 1976). However, this objection does not preclude a cladistic
analysis of plants for several reasons.
If we find three apparently closely related species, for example, two with
a diploid chromosome number of 2n, and the third with a diploid chromosome
number of 4x1, we may whish to say that the 4n species arose by hybridization
between the other two. If, however, we do not know if a plant is of hybrid origin
(e.g. intentionally produced crop plants), we must treat it and its suspected parent
species as three unique taxa, each of which may be recognized by its defining,
spcialized characters. A specialized character of an allopolyploid, for example, is
its unusual chromosome number.
After finding three such taxa in the field and knowing nothing else about them,
we could construct a cladogram of their interrelationships as an unresolved
trichotomy (Fig. 5A). This presents no less information than if we wished
immediately to assume the 4n population was a hybrid, and diagrammed the
interrelationships as in Fig. 5B. Having the 4n taxon straddle the two 2n taxa
actually includes an assumption about the 4n taxon for which we may have no
evidence (see Bremer 8c Wanntorp, 1979a, for analternative viewpoint). It may also
divert taxonomist’s attention from the problem by assuming that it is solved.
Further investigation may show, in fact, that the 4n taxon shares a derived
character with one of the 2n taxa and is therefore more closely related to that 2n
taxon than to the other (as in Fig. 5C). Without such additional information, we
can do no better than to produce an unresolved trichotomy. However, see Rosen
( 1979) for a discussion of proposed hybrid origin when biogeographic
information is included. A cladogram is a statement of inferred interrelationships of taxa based on an analysis of primitive and derived characters. Such
inferences are based on the fact.that it is more parsimonious to assume that two
groups sharing a specialization both acquired it from a common ancestor, rather
than independently. Stated another way, a cladogram is not a phylogeny; it is a
best estimate of a phylogeny. Regardless of any interbreeding now or in the past,
the gymnosperms and angiosperms, for example, may be inferred to be more
closely related to each other than either is to any other group of land plants
because of their many shared derived characters.
C
Figure 5. Hypothetical cladograms of inferred hybrid and parental species.
LAND PLANT PHYLOGENY
24 I
Two major points are being made here. The first is that polyploidy, or any
other proposed intermediate condition, by itself is no guarantee that hybridization has occurred (see Neff & Smith, 1979).The second is that even if hybridization has played a large role in the evolution of the land plants, we can always
represent their interrelationships by grouping taxa on the basis of their sharing
specialized characters.
Another objection to the use of cladistic methods in plant systematics is that
there are so many apparent convergences among the major groups of land plants
that it is impossible to determine relatedness on the basis of shared derived
characters (Stace, 1978).A previous quote states Cronquist’s view on the problem
of parallelism; is that, it obscures true relationships. However, it is only after a
cladogram is constructed that we can assess the nature of the alleged
convergences and parallelisms. For example, the lycopod Seluginellu has an
embryo which has two ‘cotyledons’. It has been stated that a reduction in the
number of cotyledons to two is an advanced character within the seed plants. If
so, should Seluginella be placed within node 11 on the cladogram of Fig. 4 ? I t
should not because it does not have an integument, it is not siphonostelic or
megaphyllous, etc. Therefore, in light of all available evidence we may say that a
reduction of cotyledons to two was arrived at independently in the seed plants
and the lycopods. Upon further investigation we may find that the ontogeny of
the reduction of cotyledon number is different in these two taxa. This would
further support the hypothesis that the two are not closely related. Conversely,
we may find further evidence which supports the relationship between the two,
and then we may question the other data. In any case, the cladistic analysis of a
group of taxa is one way in which we may identify mistakes we have made in
describing characters and hypo thesizing their homologies.
CONCLUSION
I t is concluded that cladistic methodology can and should be used to estimate
phylogenies of the land plants. Objections to using the methodology are based
on misunderstandings of the methods and their goals. A cladogram itself is not a
phylogeny; it is a hierarchical expression of interrelationships based on levels of
generality of attributes observed in nature. But, it may be taken as the current
best estimate of the single real phylogeny on the assumption that nature itself is
structured hierarchically as a result of the genealogical process. It is also tested by
the discovery of additional derived characters; therefore, a given cladogram is
potentially rejectable in favor of another that new data show to be more
parsimonious. Current traditional attempts at reconstructing phylogenies, like
all taxonomic schemes, zoological and botanical, dependent on a concept of
overall similarity, lack refutibility, rigorous definitions of groups, and precise
statements about the nature of group interrelationships.
ACKNOWLEDGEMENTS
I am indebted to K. Bremer and H.-E. Wanntorp for their extensive criticism
of earlier drafts. D. B a d e introduced me to some of the problems of plant
systematics during his course in plant morphology. I thank D. E. Rosen for his
advice, encouragement and criticism, and L. Hickey, C. Humphries, M. F.
L. R. PARENT1
242
Mickevich, C. Mitter, N. A. Neff and G. Nelson for their editorial comments.
Several anonymous reviewers provided helpful suggestions.
Particular thanks go to L. F. Marcus for providing access to a text-editing
system, and R. F. Rockwell for supplying computing funds from City College, the
City University of New York for the preparation of the final draft of the
typescript .
REFERENCES
BREMER, K. & WANNTORP, H.-E., 1978. Phylogenetic systematics in botany. Taxon, 27(4): 317-329.
BREMER, K. & WANNTORP, H.-E., 1979a. Geographic populations or biological species in phylogeny
reconstruction? Systematif Zoology, 28(2): 220-224.
BREMER, K. & WANNTORP, H.-E., 1979b. Towards a Phylogenetic Clnrsijkation of Green Organisms. Unpublished
manuscript.
BRUNDIN, L., 1966. Transantarctic relationships and their significance as evidenced in midges. Kungliga
Suenska Vetenskapsakademiens Handlingar, I I : 1-4 7 2.
BRUNDIN, L., 1968. Application of phylogenetic principles in systematic a n d evolutionary theory. In T. Orvig
(Ed.),NobelSymposium 4, Current Problems in Lower Vertebrate Phlogeny: 473-495. Stockholm: Almquist &Wiksell.
CRONQUIST, A,, 197 1. IntroductotyEotany,tDld. ed. N e w York: H a v e r and Row.
FARRIS, J. S., 1976. Phylogenetic classification of fossils with recent species. Systematic Zoology, 25: 27 1-282.
FARRIS, J . S . & KLUGE, A. G., 1979. [Review ofl Cladistics and plant systematics. Systematic Zoology, 28:
400-4 1 I .
FARRIS, J . S . , KLUGE, A. G. & ECKHARDT, M. J., 1970. A numerical approach to phylogenetic systematics.
Systematic Zoology, 19: 179-189.
FLORIN, R., 1944a. Die Koniferen des Oberkarbons und des unteren Perms. Vol. 6. Paleontographica. 85 ( B ) :
365-456.
FLORIN, R., 1944b. Die Koniferen des Oberkarbons und des unteren Perms. Vol. 7 . Paleontographica, 85(E):
457-654.
FOSTER, A. S. & GIFFORD, E. M., 1974. Comparative Morphology of Vascular Plants, 2nd ed. San Francisco: W.
H. Freeman.
HENNIG, W., 1950. Grundzunge einer Theorie der phylogenetischen Systematike. Berlin: Deutscher Zentralverlag.
HENNIG, W. 1966. Phylogenetic systematics. Urbana: University of Illinois Press.
KUBITZKI, K., (Ed.). 1977. Flowering plants, evolution and classification of higher categories. Plant Systematics
and Evolution, Suppl. 1
McNEILL, J., 1976. The taxonomy and evolution of weeds. Weed Research, 16: 399-413.
MAYR, E., 1965. Numerical phenetics and taxonomic theory. Systematic Zoology, 14: 73-97.
NEFF, N. A. & SMITH, G. R., 1979. Multivariate analysis of hybrid fishes. Systematic Zoology, 28: 176-196.
NELSON, G. J., 1971. “Cladism” as a philosophy o f classification. Systematic Zoology, 20: 47 1-472.
NELSON, G. J., 1972. Phylogenetic relationships a n d classification. Systematic Zoology, 21: 227-231.
NELSON, G. J., 1973. Classification as a n expression of phylogenetic relationships. Systematic Zoology. 22:
344-359.
PATTERSON, C. & ROSEN, D. E., 1977. Review of ichthyodectiform a n d other Mesozoic teleost fishes and
the theory and practice ofclassifying fossils. Bulletin ofthe American Museum ofNatural History, I 5 7 : 1-1 70.
PLATNICK, N. I. & NELSON, G., 1978. A method of analysis for historical biogeography. Systematic Zoology,
27: 1-16.
PRAEGER, E. M . , FOWLER, D. P. & WILSON, A. C., 1976. Rates of evolution in conifers (Pinacead.
Evolution, 30: 637-649.
ROSEN, D. E., 1978. Vicariant patterns and historical explanation of biogeography. Systematic Zoology, 27:
159-188.
ROSEN, D. E., 1979. Fishes from the uplands and intermontane basins of Guatemala: revisionary studies and
comparative geography. Bulletin of the American Museum of Natural History, 162(5): 267-376.
SPORNE, K., 1976. Character correlations among angiosperms and the importance of fossil evidence in
assessing their significance. In C. B. Beck (Ed.), Origtn and Ear& Evolution ofAngiosperms: 312-329. New York:
Columbia University Press.
STACE, C. A,, 1978. Breeding systems, variation patterns and species delimitation. In H. E. Street (Ed.),Essays
in Plant Taxonomy: 56-78. New York: Academic Press.
WAGNER, W. H., 1961. Problems in the classification of ferns. Recent Advances in Botany, I : 841-844,
WILEY, E. O., 1975. Karl R. Popper, systematics, and classification: a reply to Walter Bock and other
evolutionai-y taxonomists. Systematic Zoology, 24: 233-243.