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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 . 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