Chapter 9 Phylogeny of Angiosperms Angiosperms form the most dominant group giosperms dominate all major terrestrial veg- of plants with at least 253,300 species etation zones, account for the majority of pri- (Thorne, 2007), a number much greater mary production on land, and exhibit bewil- than all other groups of plants combined to- dering morphological diversity. Unfortu- gether. Not only in numbers, angiosperms nately, much less is known about the origin are also found in a far greater range of habi- and early evolution of angiosperms, result- tats than any other group of land plants. The ing in a number of different views regarding phylogeny of angiosperms has, however, their ancestors, the earliest forms and been a much-debated subject, largely be- course of evolution. The origin of an- cause of very poor records of the earliest an- giosperms may be conveniently discussed giosperms. These earliest angiosperms prob- under the following considerations. ably lived in habitats that were not best suited for fossilization. Before trying to What are Angiosperms? evaluate the phylogeny, it would be useful Angiosperms form a distinct group of seed to have an understanding of the major terms plants sharing a unique combination of char- and concepts concerning phylogeny in gen- acters. These important characters include eral, and with respect to angiosperms in carpels enclosing the ovules, pollen grains particular. germinating on the stigma, sieve tubes with companion cells, double fertilization result- ing in triploid endosperm, and highly reduced ORIGIN OF ANGIOSPERMS male and female gametophytes. The an- The origin and early evolution of an- giosperms also have vessels. The pollen giosperms are enigmas that have intrigued grains of angiosperms are also unique in botanists for well over a century. They con- having non-laminate endexine and ectexine stituted an ‘abominable mystery’ to Darwin. differentiated into a foot-layer, columellar The mystery is slowly being ‘sleuthed’ and layer and tectum (tectum absent in at the present pace of Sherlock Holms’ re- Amborellaceae). The angiosperm flower typi- search, it may be no more mysterious cally is a hermaphrodite structure with car- within the next two decades than for any pels surrounded by stamens and the latter other major group. With the exception of co- by petals and sepals, since insect pollina- nifer forest and moss-lichen tundra, an- tion prevails. Arbuscular mycorrhizae are 266 Plant Systematics Table 9.1 Geological time scale. Time Era Period Epoch Stage _________________________________________________________________________________________________ m years (mya) __0.01__ Quaternary Holocene __2.5 __ ________ Pleistocene_______________________________________ __7 __ Cenozoic Pliocene __26 __ Miocene __38 __ Tertiary Oligocene __54 __ Eocene __65 _________________________________________ Palaeocene________________________________________ __74 __ Maestrichtian __83 __ Campanian __87 __ Santonian __89 __ Upper Coniacian __90 __ Turonian __97 __ __________________________________________________ Cenomanian _ __112__ Cretaceous Albian __125__ Aptian __132__ Mesozoic Barremian __135__ Lower Hauterivian __141__ Valanginian __146__ _______________________________________________________________Berriasian___ Upper Jurassic Middle __208__ _________________________ Lower___________________________________________ Upper Triassic Middle __235__________________________________________ Lower____________________________________________ __280__ Permian___________________________________________________________________ __345__ Carboniferous______________________________________________________________ __395__ Devonian__________________________________________________________________ __430__ Palaeozoic Silurian____________________________________________________________________ __500__ Ordovician_________________________________________________________________ __570__________________Cambrian_________________________________________________________________ __2400_ Precambrian Algonkian__________________________________________________________________ __4500_ Archaean also unique to angiosperms (except anemophily. In spite of these and other ex- Amborellaceae, Nymphaeales and ceptions, this combination of characters is Austrobaileyales). The vessel elements of an- unique to angiosperms and not found in any giosperms typically possess scalariform per- other group of seed plants. forations. There may be individual exceptions to What is the age of most of these characters. Vessels are absent in some angiosperms (Winteraceae) while Angiosperms? some gymnosperms have vessels (Gnetales). The time of origin of angiosperms is a mat- The flowers are unisexual without perianth ter of considerable debate. For many years, in several Amentiferae, which also exhibit the earliest well-documented angiosperm Phylogeny of Angiosperms 267 fossil was considered to be the form-genus other fossil pollens from the Jurassic age at- Clavitopollenites described (Couper, 1958) tributed to Nymphaeaceae ultimately turned from Barremian and Aptian strata of Early out to be gymnosperms. Cretaceous (Table 9.1) of southern England In the last few years Sun et al., (1998, (132 to 112 mya-million years), a 2002) have described fossils of Archaefructus monosulcate pollen with distinctly sculptured from Upper Cretaceous (nearly 124 mya) of exine, resembling the pollen of the extant China, with clearly defined spirally arranged genus Ascarina. Brenner and Bickoff (1992) conduplicate carpels enclosing ovules, a fea- recorded similar but inaperturate pollen ture not reported in earlier angiosperms. grains from the Valanginian (ca 135 mya) of The fruit is a follicle. This is considered to the Helez formation of Israel, now consid- be the oldest record of angiosperm flower. ered to be the oldest record of angiosperm Several vegetative structures from the fossils (Taylor and Hickey, 1996). Also found Triassic were also attributed to angiosperms. in Late Hauterivian (Brenner, 1996) of Is- Brown (1956) described Sanmiguilea leaves rael (ca 132 mya) were Pre-Afropollis (mostly from the Late Triassic of Colorado and sug- inaperturate, few weakly monosulcate), gested affinity with Palmae. A better under- Clavitopollenites (weakly monosulcate to standing of the plant was made by Cornet inaperturate), and Liliacidites (monosulcate, (1986, 1989), who regarded it as a presumed sexine similar to monocots). From Late primitive angiosperm with features of mono- Barremian have been recorded Afropollis and cots and dicots. Although its angiosperm ve- Brenneripollis (both lacking columellae) and nation was refuted by Hickey and Doyle Tricolpites (the first appearance of tricolpate (1977), Cornet (1989) established its an- pollen grains) giosperm venation and associated reproduc- The number and diversity of angiosperm tive structures. Our knowledge of this con- fossils increased suddenly and by the end of troversial taxon, however, is far from clear. the Early Cretaceous (ca 100 mya) period Marcouia leaves (earlier described as major groups of angiosperms, including her- Ctenis neuropteroides by Daugherty, 1941) are baceous Magnoliidae, Magnoliales, Laurales, recorded from the Upper Triassic of Arizona Winteroids and Liliopsida were well repre- and New Mexico. Its angiosperm affinities sented. In Late Cretaceous, at least 50 per are not clear. cent of the species in the fossil flora were Harris (1932) described Furcula from the angiosperms. By the end of the Cretaceous, Upper Triassic of Greenland as bifurcate leaf many extant angiosperm families had ap- with dichotomous venation. Although it peared. They subsequently increased expo- seems to approach dicots in venation and nentially and constituted the most dominant cuticular structure, it has several non-an- land flora, continuing up to the present. giospermous characters including bifurcat- The trail in the reverse direction is in- ing midrib and blade, higher vein orders with complete and confusing. Many claims of an- relatively acute angles of origin (Hickey and giosperm records before the Cretaceous were Doyle, 1977). made but largely rejected. Erdtman (1948) Cornet (1993) has described Pannaulika, described Eucommiidites as a tricolpate di- a dicot-like leaf form from Late Triassic cotyledonous pollen grain from the Jurassic. from the Virginia-North Carolina border. It This, however, had bilateral symmetry in- was considered to be a three-lobed palmately stead of the radial symmetry of angiosperms veined leaf. The associated reproductive (Hughes, 1961) and granular exine with gym- structures were attributed to angiosperms nospermous laminated endexine (Doyle et but it is not certain that any of the repro- al., 1975). This pollen grain was also discov- ductive structures were produced by the ered in the micropyle of seeds of the female plant that bore Pannaulika. Taylor and cone of uncertain but clearly gymnosper- Hickey (1996), however, do not accept its mous affinities (Brenner, 1963). Several angiosperm affinities, largely on the basis 268 Plant Systematics of the venation pattern, which resembles was made by Martin et al., (1989) using nine more that of ferns. Much more information angiosperm sequences from gapC, the is needed before the Triassic record of an- nuclear gene encoding GADPH (cytosolic giosperms can be established. glyceraldehydes-3-phosphate dehydroge- Cornet (1996) described Welwitschia like nase). The observed number of fossil as Archaestrobilus cupulanthus from the