CHAPTER8 Phylogenetic Relationships of Angiosperms he angiosperms (or flowering plants) are the dominant group of land Tplants. The monophyly of this group is strongly supported, as dis- cussed in the previous chapter, and these plants are possibly sister (among extant seed plants) to the gnetopsids (Chase et al. 1993; Crane 1985; Donoghue and Doyle 1989; Doyle 1996; Doyle et al. 1994). The angio- sperms have a long fossil record, going back to the upper Jurassic and increasing in abundance as one moves through the Cretaceous (Beck 1973; Sun et al. 1998). The group probably originated during the Jurassic, more than 140 million years ago. Cladistic analyses based on morphology, rRNA, rbcL, and atpB sequences do not support the traditional division of angiosperms into monocots (plants with a single cotyledon, radicle aborting early in growth with the root system adventitious, stems with scattered vascular bundles and usually lacking secondary growth, leaves with parallel venation, flow- ers 3-merous, and pollen grains usually monosulcate) and dicots (plants with two cotyledons, radicle not aborting and giving rise to mature root system, stems with vascular bundles in a ring and often showing sec- ondary growth, leaves with a network of veins forming a pinnate to palmate pattern, flowers 4- or 5-merous, and pollen grains predominantly tricolpate or modifications thereof) (Chase et al. 1993; Doyle 1996; Doyle et al. 1994; Donoghue and Doyle 1989). In all published cladistic analyses the “dicots” form a paraphyletic complex, and features such as two cotyle- dons, a persistent radicle, stems with vascular bundles in a ring, secondary growth, and leaves with net venation are plesiomorphic within angio- sperms; that is, these features evolved earlier in the phylogenetic history of tracheophytes. In contrast, the monophyly of the monocots is supported by the synapomorphies of leaves with parallel venation, embryo with a single cotyledon, sieve cell plastids with several cuneate protein crystals, stems with scattered vascular bundles, and an adventitious root system, although several of these characters are homoplasious (see page 174). The monophyly of monocots also is supported by 18S rDNA, atpB and rbcL nucleotide sequences (Bharathan and Zimmer 1995; Chase et al. 1993, 1995a; Soltis et al. 1997, 1998). 161 162 CHAPTER EIGHT Although the “dicots” apparently are nonmonophylet- ly pinnately veined, coriaceous leaves, and paracytic sto- ic, a large number of species traditionally considered mates. Flowers typically have several to numerous parts, within this group do constitute a well-supported clade: with little or no fusion. Perianth parts are arranged spi- the tricolpates (or eudicots) (Chase et al. 1993; Donoghue rally or in whorls of three, and stamens are often lami- and Doyle 1989; Doyle et al. 1994; Soltis et al. 1997). nar. The filament is poorly differentiated from the anther, Synapomorphies of this monophyletic group include tri- and the connective tissue is often well developed. Pollen colpate pollen (or modifications of this basic pollen type), grains of Magnoliales lack a columellar exine structure. plus rbcL, atpB, and 18S rDNA nucleotide sequences. The paleoherbs include Aristolochiales, Piperales, Unfortunately, phylogenetic relationships among the Nymphaeales, and Ceratophyllales. They are usually nonmonocot, nontricolpate angiosperms are poorly herbaceous (but sometimes secondarily soft-woody) understood. These families have often been considered plants that may have adaxial prophylls (lowermost bract to represent a paraphyletic, primitive angiosperm com- of shoot). Leaves are alternate, often more or less plex, and are treated as the superorder Annonanae by palmately veined, thin-textured, and with anomocytic Thorne (1992) and as the subclass Magnoliidae by Cron- stomates. Flowers have numerous to few parts; those of quist (1981, 1986, 1988) and Takhtajan (1980, 1997). Most the perianth and androecium usually are in whorls of have ethereal oils in scattered spherical cells within the three. The filament is well differentiated from the anther, parenchymatous tissues and elongate vessel elements and the connective usually is inconspicuous. Pollen with slanted, scalariform perforation plates. Their flow- grains usually have a columellar exine. ers usually are radially symmetrical; the carpels and sta- Note that the monocots share most of the above-listed mens are usually distinct and free, and the former have a paleoherb characters. The paleoherb families (or at least poorly developed style and an elongate stigmatic region. some of them) may be closely related to monocots The pollen is usually monosulcate, and the seeds have a (Chase et al. 1993; Donoghue and Doyle 1989; Doyle et tiny embryo with copious endosperm. al. 1994). In fact, the monocots often are considered one It is convenient to divide the families of this complex of the subgroups of paleoherbs, and the other paleo- into two groups: the magnoliids and the paleoherbs. The herbs are then referred to as nonmonocot paleoherbs. magnoliids include Magnoliales, Laurales, and Illiciales. Magnoliids traditionally have been considered to retain They are woody plants with alternate or opposite, usual- the greatest number of plesiomorphic features within the “Magnoliids” Paleoherbs Magnoliales Laurales Illiciales Tricolpates Piperales Nymphaeales Aristolochiales Monocots 1 cotyledon Parallel venation P-type plastids Loss of ethereal oils Tricolpate pollen Scattered vascular bundles (and derived types) Adventitious root system Loss of ethereal oils Anomocytic stomates 2 perianth whorls 3-merous perianth and androecium Herbs Anthers well differentiated from filaments Figure 8.1 Cladogram of major angiosperm Columellate pollen groups based on morphological characters, showing Magnoliales as sister to the remaining taxa. Note that in this and subsequent cladograms in this chap- ter, the use of quotation marks shifts, meaning that whether or not a group is seen as monophyletic can change based on the criteria (morphology, nucleotide sequence, etc.) used to create the clado- gram. (Modifed from Donoghue and Doyle 1989.) PHYLOGENETIC RELATIONSHIPS OF ANGIOSPERMS 163 “Paleoherbs” Magnoliids “Paleoherbs” “Magnoliids” Monocots Nymphaeales Aristolochiales Laurales Magnoliales Illiciales Nymphaeales Aristolochiales Illiciales (Winteraceae) Laurales Magnoliales Piperales Tricolpates Monocots Tricolpates Figure 8.2 Cladogram of major angiosperm groups based on Figure 8.3 Cladogram of major angiosperm groups based on morphological characters, showing Nymphaeales and monocots nuclear ribosomal RNA nucleotide sequences. (Modified from as sister to the remaining taxa. (Modifed from Doyle et al. 1994.) Doyle et al. 1994.) angiosperms (Cronquist 1968, 1981, 1988; Thorne 1974, atpB nucleotide sequences suggest that a clade contain- 1992; Takhtajan 1969, 1980; Dahlgren 1977, 1983). This ing Nymphaeales and magnolid families such as Illici- viewpoint has received some support from morphology- aceae and Austrobaileyaceae may be sister to the based cladistic analyses (Donoghue and Doyle 1989; Doyle remaining angiosperms, with Ceratophyllaceae placed et al. 1994; Loconte and Stevenson 1991). The magnoliids, as sister to the tricolpate clade (D. Soltis, personal com- therefore, may represent a basal paraphyletic complex munication; M. Chase, personal communication). within the angiosperms, as supported by the possibly In summary, the rooting of the angiosperm cladogram retained plesiomorphic feature of laminar anthers (Figure is equivocal. It is obvious, however, that a simplistic divi- 8.1). The noncolumellate pollen of Magnoliales may also sion of the angiosperms into monocots and dicots does be a retained plesiomorphy. Several cladistic analyses based on 18S nucleic acid sequences, however, support a rooting of the angio- sperm clade within the nonmonocot paleoherbs (Doyle “Paleoherbs” Magnoliids et al. 1994; Zimmer et al. 1989; Hamby and Zimmer 1992; Soltis et al. 1997). The paleoherbs also occupy a basal paraphyletic position in some recent analyses based on either morphology alone or rDNA combined with mor- Laurales phology (Doyle et al. 1994; Figures 8.2, 8.3, and 8.4). Nymphaeales Monocots Piperales Aristolochiales Tricolpates Illiciales (Winteraceae) Magnoliales Thus, the primitive angiosperm may have been semi- herbaceous, with alternate, more or less palmately veined leaves and anomocytic stomates. Its flowers may have been 3-merous, with six tepals (in two whorls of three), and six stamens (also in two whorls of three) that were well differentiated into an anther and filament (see also Taylor and Hickey 1996). Cladistic analyses based on rbcL sequences (Figure 8.5) support placement of most angiosperms in one of two major clades. Taxa with monosulcate pollen (mono- cots, nonmonocot paleoherbs, and magnoliids) are on one branch and tricolpates on a second (Chase et al. 1993). These analyses also suggest that Ceratophyllaceae Figure 8.4 Cladogram of major angiosperm groups based on may represent the sister group to all other angiosperms. both morphology and nuclear ribosomal RNA. (Modified from Finally, recent analyses based on 18S rDNA, rbcL, and Doyle et al. 1994.) 164 CHAPTER EIGHT Monosulcates Figure 8.5 Cladogram of major angiosperm groups based on rbcL nucleotide sequences. (Modified from Chase et al. 1993.) “Paleoherbs” “Magnoliids” not accurately reflect phylogenetic history. At this time, the monophyly of only two major angiosperm clades— the monocots and tricolpates