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Cladistic Analysis of the Hornworts (Anthocerotophyta)

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Cladistic Analysis of the Hornworts (Anthocerotophyta) J. Hattori Bot. Lab. No. 74: 105- 119 (Nov. 1993) CLADISTIC ANALYSIS OF THE HORNWORTS (ANTHOCEROTOPHYTA) JAAKKO HYV0NEN1 and SINIKKA PIIPPa2 ABSTRACT. A cladistic analysis of the genera of Anthocerotophyta is presented. The analysis was based on forty characters and included all nine genera currently accepted in the group. Only one most parsimonious tree was found. According to the results, the hornworts are treated as two orders: Anthocerotales Limpricht and Notothylales Hyvonen and Piippo, ord. nov. (merely with Notothylas Sull. ). Anthocerotales comprises two families: Anthocerotaceae Dum. (Anthoceros L. emend. Prosk., Folioceros Bharadw., Leiosporoceros Hassel, Mesoceros Piippo, Phaeoceros Prosk., and Sphaerosporoceros Hassel), and Dendrocerotaceae (Milde) Hassel (with Dendroceros Nees and Megaceros Campbell). INTRODUCTION The relationship of the hornworts (Anthocerotophyta) to other land plants has been a controversial issue (Crandall-Stotler 1984, Schofield 1985, Schuster 1984, 1992, Mishler & Churchill 1985). It has been claimed that they represent a totally indepen­ dent lineage from all other living land plants (Schuster 1984, 1992) or they may be included in a clade together with liverworts, mosses and tracheophytes (Mishler & Churchill 1985). The latter view assumes that they share a common ancestor with the mosses and all other land plants excluding the liverworts. Mishler and Churchill ( 1985) presented a cladistic analysis supporting this view, and their results were chosen as a starting hypothesis for our analysis. Further support for this view has lately come also from nucleotide-sequence data (Mishler et al. 1992). The monophyly of the hornworts as a whole has generally been accepted, a view supported by several synapomorphies documented by Mishler and Churchill (1985) and Hassel de Menendez (1988). Traditionally the hornworts have been treated under a single family, Anthocerotaceae. Muller (1951 - 58) treated Notothy/as Sull. in its own family. This same traditional trend has been continued by Schuster (1987, 1992) and Hasegawa (1988), Schuster keeping all the genera in the one and same family, but under different subfamilies (see Table 1), Hasegawa treating them under three families. Schuster ( 1992) has a reservation about Anthocerotaceae: "The family includes all extant Anthocerotales except (possibly) for Notothylas". Schuster (1987, 1992) did not treat all the genera. In contrast to other workers (see below, and Table 1), he continues to treat Anthoceros L. emend. Poosk as Aspiromitus Steph., and Phaeoceros Prosk. as Anthoceros, and he includes Leiosporoceros Hassel under the latter as well. Dendroceros 1 Jaakko Hyvonen, Department of Botany, P. 0 . Box 47 (Hameentie 153B), FIN-00014 University of Helsinki, Finland. 2 Sinikka Piippo, Botanical Museum, P. 0 . Box 47 (Hameentie 153B), FIN-00014 Uni­ versity of Helsinki, Finland. 0 O'- Table 1. Classidication of Anthocerotophyta by different authors. Hasegawa 1988 Hassel de Menendez 1988 Schuster 1992 Pippo 1993 Hyvonen & Pippo 1993 ANTHOCEROTALES ANTHOCEROTALES ANTHOCEROTALES ANTHOCEROTALES Anthocerotaceae Anthocerotaceae An thocerotaceae Anthocerotaceae Anthocerotaceae Anthoceros Anthoceros Subfam. Anthoceros Anthoceros ( + Subg. Folioceros) Sphaerosporoceros Anthocerotoideae Mesoceros Folioceros Phaeoceros Aspiromitus Phaeoceros Leiosporoceros ( + Subg. Leiosporoceros) Notothyladaceae Anthoceros Sphaerosporoceros Mesoceros Megaceros Subfam. ( + Subg. Leiosporoceros) Phaeoceros c- Notothyladoideae Subfam. Foliocerotaceae Sphaerosporoceros :i: I>endrocerotaceae Notothy/as I>endrocerotoideae Folioceros ~ 0 Dendroceros Subfam. Dendroceros I>endrocerotaceae :i. o::i Phaeocerotoideae Megaceros Leiosporotaceae Dendroceros £ Notothyladaceae Phaeoceros Subfam. Leiosporoceros Megaceros r Notothylas N otothyladoideae ",,. FOLIOCEROTALES Notothy/as I>endrocerotaceae NOTHOTHYLALES z <'.' Foliocerotaceae Dendroceros Notothyladaceae -.J Fo/ioceros Megaceros Notothylas ""' LEIOSPOROCEROT ALES Notothyladaceae Leiosporocetaceae Notothylas Leiosporoceros I>ENI>ROCEROT ALES I>endrocerotaceae Dendroceros Megaceros "" w"" J. HYVONEN & S. PIIPPO: Cladistic analysis of the hornworts 107 A Fig. I. A. The cladogram of the genera of Anthocerotae according to Mishler and Churchill (1985) and B. according Hassel de Menendez (1988) . Data supported the distinction of only four clades, not seven as in the original figure. Nees, Megaceros Campbell, and Notothylas are in Anthocerotaceae but in different subfamilies. Hasegawa (1988) has five genera: Anthoceros (incl. Folioceros Bharadw.), Phaeoceros (incl. Leiosporoceros) and Megaceros Campbell in Anthocerotaceae, and Dendroceros Nees and Notothylas in their own families. The analysis by Mischler and Churchill (1985) included five genera: Anthoceros (including Folioceros), Dendroceros, Megaceros, Notothylas and Phaeoceros (Fig. la). Higher ranking was not discussed by them. Hassel de Menendez (1988) accepted eight genera with Sphaerosporoceros Hassel and Leiosporoceros. Folioceros was treated as a separate genus from Anthoceros (Fig. l b, Table l ). The classification by Hassel de Menendez radically differs from those of the others, because she accepts four different orders for the hornwort genera (see Table l). The study of the New Guinean material (Piippo 1993) revealed a formerly undescribed taxon. It did not fit well in any of the known genera and thus required description of one more genus in Anthocerotophyta, Mesoceros Piippo (Piippo 1993). The relationship of this new genus to other genera of the hornworts was only briefly discussed by Piippo, and this inspired interest in analysis of the whole group, based on cladistic principles. We were also interested to find out whether the data collected could possibly offer better resolution of the whole group than formerly presented. Cladistic analysis is based solely on characters of the taxa included and totally avoids any a priori assumptions as to the evolution of the group. MATERIAL AND METHODS Nine genera currently accepted in the hornworts are included as the terminal taxa 108 J. Hattori Bot. Lab. No. 74 I 9 9 3 in the analysis. Forty characters (see below) were included in the analysis. Originally three more characters (length of capsules, form of the capsule cells, and the size of spores) were tabulated, but we were unable to code their excessive polymorphism for the use in the final analysis. Of the characters, 39 are morphological and one is ecological. Only three characters included three character states, the others being binary. In addition, six synapomorphies for the hornworts or for the clade of the land plants excluding liverworts (Mishler & Churchill 1984, 1985) were putatively included (characters 41 - 47) when the two out-groups were added to the analysis. For further discussion on these characters, see Mishler and Churchill ( 1985). The main sources for the data were Mishler and Churchill ( 1985), Hassel de Menendez ( 1986, 1988 ), and Hasegawa (1988). Study of the herbarium material concentrated on Western Mela­ nesian specimens and especially on the genera Dendroceros, Folioceros, Megaceros, Mesoceros and Phaeoceros (see Piippo 1993). The original data matrix was compiled by S. Piippo. Characters included in the analysis 1. Thallus strap-shaped (0), radiate ( l ). Dendroceros, Folioceros and Megaceros have distinctly strap-shaped thalli, even though species of Dendroceros are often richly branched; the thalli of the other genera are radiate, except Anthoceros and Phaeoceros, which have both forms. 2. Colar light green (0), dark green ( 1) . Most of the hornworts are dark-colored, often almost black, except for the light green Dendroceros, green Anthoceros and variable Notothylas. 3. Costa absent (0), present ( 1) . Distinct, but variable in width, a costa is present only in Dendroceros, which also has one-celled laminae outside the costa providing many further characters at specific level. The other genera have a pluristratose thallus throughout except perhaps on the thallus edges. 4. Costa/thallus cavernous (0), solid ( 1) . The schizogenous cavities usually serve as a good distinguishing character between the genera. The only genus showing polymorphism is Dendroceros. 5. Tubers absent (0), present ( 1). Tubers are known to occur only in Phaeoceros. 6. Rhizoids present (0), absent (1 ). Rhizoids usually occur in hornworts, but may occasionally be absent. In Dendroceros, rhizoids are few or rare. 7. Epidermal cells not distinctive from medium cells (0), two cell types present (1). Especially in Megaceros, Mesoceros and Phaeoceros the epidermal cells are smaller than medium cells. 8. Epidermal cells without trigones (0), with trigones ( 1). Only species of Dendro­ ceros have trigones in epidermal cells, which serve as good specific characters due to their different sizes, possible perforations, and position on laminae. 9. Pyrenoids in chloroplasts absent (0), present ( 1) . Pyrenoids are present in all thallus cells except in Megaceros and a few species of Folioceros (Bharadwaj 1972). 10. Apical cell of thallus hemidiscoid (0), cuneate (1). All the other hornwort genera have cuneate apical cells, except the epiphytic Dendroceros. 1. HvvONEN & S. PllPPO: Cladistic analysis of the hornworts 109 11 . Thallus does not continue its growth by the apices after fertilization (0), growth continues (I). Only in Notothylas does the thallus cease apical growth, and the developing capsule remains in an apical notch. 12. lnvolucres 2.5- 5mm (0), 1- 2.5 mm (1), 5- lOmm (2).
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