10 The Radiation of Vascular Plants

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Kathleen M. Pryer

Harald Schneider

Susana Magallуn

138

Vascular plants include our major food resources in the form

of leaves, stems, roots, fruits, and seeds. They further sustain

human life by providing other essentials such as wood,

fibers, and medicines. Plants are the dominant primary producers

in terrestrial habitats, and by the process of photosynthesis,

they actively convert solar energy, water, and

carbon dioxide into carbohydrates (sugars) and oxygen,

which is vital to all living things. The rise and spread of vascular

plants resulted in a dramatic drop in atmospheric carbon

dioxide (CO2) about 400 million years ago during the

mid-Paleozoic (Algeo et al. 2001, Berner 2001, Driese and

Mora 2001, Raven and Edwards 2001). This decline in atmospheric

CO2 triggered the evolution of vascular plants

with more complex body plans, including such organs as

leaves, specialized for optimizing photosynthesis (Beerling

et al. 2001, Pataki 2002, Shougang et al. 2003). Vascular

plants therefore both caused and reacted to global changes

in their physical environment early in their evolution. The

earliest radiation of vascular plants has been interpreted as

one in which rapidly diversifying lineages colonized and

shaped different terrestrial habitats (DiMichele et al. 2001).

Repeated reciprocation between climatic change and vascular

plant radiation is noted throughout the fossil record, with

particularly marked changes in floristic patterns occurring

at the end of the Permian (Looy et al. 2001), at the Triassic/

Jurassic (McElwain et al. 1999) and Paleocene/Eocene

boundaries (Tiffney and Manchester 2001), and in the Cretaceous

(Friis et al. 2001b).

The advent of terrestrial primary producers capable of

forming a huge biomass correlates with the simultaneous

rise of terrestrial animals in the Paleozoic, including various

groups of arthropods and tetrapods (Coates 2001, Shear

and Selden 2001, Carroll 2002). For example, the first known

mites are found together with the first vascular plants in

Devonian Rhynie Chert beds in Aberdeenshire in the north

of Scotland. According to a recent molecular clock estimate,

basal groups of insects originated during the Late Devonian

(Gaunt and Miles 2002), coinciding with the diversification

of vascular plants. The wide spectrum of fossilized insects

observed in the Late Carboniferous (Labandeira 2001), including

herbivorous groups, also suggests a simultaneous

adaptive radiation of vascular plants and insects. The establishment

of vascular plants with large and complex body

plans in the Carboniferous and Permian resulted in an increased

amount and diversity of vegetative biomass that favored

the diversification of herbivorous tetrapods in the

Permian (Sues and Reisz 1998, Coates 2001). Vascular plants

are not only the major nutrient source for the consumers in

their ecosystems, but they also play an important role in symbiotic

associations with fungi (Brundrett 2002). Rhynie Chert

fossils of glomalean mycorrhizal fungi discovered in association

with preserved plant shoots exquisitely document

complex plant–fungi interactions by the Early Devonian,

suggesting that mycorrhizal associations were a critical factor

in the early and successful colonization of land by terrestrial

plants (Taylor et al. 1995, Blackwell 2000, Cairney 2000,

The Radiation of Vascular Plants 139

Hibbett et al. 2000, Redecker et al. 2000, Brundrett 2002;

see also ch. 12 in this vol.).

In this review, we summarize the results of various recent

studies that have used morphological and/or molecular evidence

to infer the phylogeny of living vascular plants, and those

that have used morphological/anatomical evidence to understand

relationships of fossil plants. These studies differ widely

in their taxon sampling, in the parts of the green branch of the

Tree of Life they focus on, and also in their methodology. It is

a challenging exercise, therefore, to distill from them not only

a summary but also a fresh look at our current understanding

of the evolution and relationships among both living and extinct

vascular plants. It should be noted at the outset that we

view the continued traditional application of several taxonomic

names and ranks, especially to fossil groups that are clearly not

monophyletic (e.g., Rhyniophyta), as hampering progress in

our understanding and discussions of vascular plant evolution.

Rather than abandon these names entirely, we retain most

of them as common names in quotation mark (e.g., “rhyniophytes”)

to clarify historical usage. In our phylogenetic figures,

we attempt to illustrate progress that has been made in discerning

the relationships of members of these groups and our best

sense of where they “fit in.” Also, where we integrate fossils

together with living taxa, we try to distinguish between stem

and crown groups (see Smith 1994:94–98). Stem groups include

taxa that are in fact part of a particular lineage but that

lack some character(s) (synapomorphy) that distinguishes the

crown group.

We were especially fortunate to be able to build on several

thorough reviews that have been published in recent

years. For additional information and different perspectives,

the reader is referred to Kenrick and Crane (1997b), Bateman

et al. (1998), Doyle (1998b), Rothwell (1999), Renzaglia et al.

(2000), Donoghue (2002), Judd et al. (2002: ch. 7), and

Schneider et al. (2002).

What Are Vascular Plants?

Vascular plants make up the bulk of all the land plant lineages.

They are a monophyletic group characterized by the

presence of specialized cells, tracheids and sieve elements,

which conduct water and nutrients throughout the plant

body and provide structural support (Kenrick and Crane

1997a, 1997b, Bateman et al. 1998, Schneider et al. 2002).

Land plants are typified by an alternation of generation

phases, whereby heteromorphic haploids (gametophytes)

and diploids (sporophytes) alternate throughout the plant’s

life cycle (Kenrick 1994, 2000, 2002b, Mable and Otto 1998,

Renzaglia et al. 2000). The gametophytes of nonvascular land

plant lineages (mosses, liverworts, and hornworts) are the

dominant or more visible phase that bears a comparatively

tiny sporophyte with a single sporangium. The recent confirmation

of Charales as the green algal lineage most closely

related to land plants (Karol et al. 200l) supports the view

that a dominant gametophyte phase is the plesiomorphic

(ancestral) condition, whereas a predominant sporophyte

phase, which is found in vascular plants, is derived (Mable

and Otto 1998, Kenrick 2000). The gametophyte phase is diminutive

in vascular plants compared with the highly branched

sporophyte that bears more than a single sporangium (polysporangiate).

Figure 10.1 contrasts these major differences in

morphology and life cycle between nonvascular and vascular

plants. Observations from the fossil record (Kenrick 2002b)

the reconstruction of life cycle evolution based on living taxa

(Schneider et al. 2002: fig. 17.2a) converge on a scenario suggesting

that over time there was a trend from a short-lived

sporophyte phase (“bryophytes”) to one whereby both the

gametophyte and sporophyte phases were essentially codominant

(putatively isomorphic in “rhyniophytes”) and that eventually

the sporophyte phase came to dominate the life cycle in

vascular plants. Heterosporous lineages (those that produce

two spore types), and especially seed plants, demonstrate this

trend most clearly, with the gametophyte phase becoming

extremely reduced both in size and in duration.

Unequivocal evidence for the earliest polysporangiate

plants dates back to the Rhynie Chert beds of the Late Silurian.

Representatives such as Aglaophyton (fig. 10.2 inset),

Horneophyton, and Rhynia all had simple and diminutive

body plans with dichotomously branched axes and no roots

or leaves (Kenrick and Crane 1997a, 1997b, Crane 1999,

Edwards and Wellman 2001). The erect axes were terminated

by round or ovoid sporangia and possessed water-conducting

cells that were either unthickened and unornamented (e.g.,

Aglaophyton) or well-developed tracheids (e.g., Rhynia) organized

in centrarch protosteles (protoxylem is centrally located

in the vascular cylinder and xylem maturation is centrifugal—

toward the periphery of the axis. These plants are often referred

to as “rhyniophytes,” and they were never very diverse

either in species number or in morphology and quickly became

replaced by plants with a more complex organization.

The descendants of these “rhyniophytes” diversified rapidly

in the Early Devonian, resulting in a split into two major groups

(fig. 10.2), the lycophytes (Lycophytina) and the euphyllophytes

(Euphyllophytina). The primary feature that unites

these two groups to distinguish them from the “rhyniophytes”

is the differentiation of the plant body into aerial (shoot) and

subterranean (root) components (Gensel and Berry 2001,

Gensel et al. 2001, Schneider et al. 2002), which argues for a

single origin of roots rather than several independent origins

(Raven and Edwards 2001, Kenrick 2002a).

Lycophytes and Zosterophytes (Lycophytina)

The earliest lycophyte lineages diversified in the Early Devonian

and are referred to here as “protolycophytes”

(fig. 10.3), plants characterized by mostly dichotomously

branching axes that are either naked or covered by spiny

appendages. The aerial axes mostly possess an exarch pro140

The Relationships of Green Plants

tostele (protoxylem is located at the edge of the vascular

cylinder and xylem maturation is centripetal—toward the

center of the axis) and bear dorsiventral sporangia (often

kidney-shaped) that open into two equal-sized valves via

transverse dehiscence. These sporangia are laterally inserted

either on terminate or nonterminate axes (Kenrick and Crane

1997a). Zosterophytes [eg., Zosterophyllum (fig. 10.3 inset),

Sawdonia] and prelycophytes (e.g., Asteroxylon, Drepanophycus)

were a dominant component of the landscape until

they became extinct in the Early Carboniferous. Their descendants,

which include three extant lineages of lycophytes—

Lycopodiales, Selaginellales, and Isoлtales (fig. 10.3)—bear

lycophylls, leaves that develop exclusively by intercalary

growth (Crane and Kenrick 1997, Kenrick 2002b; Schneider

et al. 2002). Intercalary growth is characterized by meristematic

activity that is not apical but rather is more diffusely

organized toward the base of the lycophylls.

These three lineages diversified in the Late Devonian and

Carboniferous and can be easily distinguished by both reproductive

and vegetative features (Kenrick and Crane 1997a,

Judd et al. 2002). The Lycopodiales are homosporous (produce

spores of a single type) and are sister to a clade of

heterosporous (producing two spore types) lycophytes,

Selaginellales and Isoлtales, which bear a sterile leaflike appendage

(ligule) on the adaxial (facing toward main axis) leaf

surface. The heterosporous lycophytes were morphologically

and ecologically diverse throughout the Carboniferous, including

arborescent forms with a unique type of secondary xylem,

such as the isoetalean lycophyte Lepidodendron (fig. 10.3, inset),

but declined drastically starting in the Upper Carboniferous

(Pigg 2001, DiMichele and Phillips 2002) and continuing

throughout the Mesozoic. Today the lycophyte representatives

that remain are diminutive in stature and diminished in diversity

(<1% of extant vascular plants).

“Trimerophytes” and

Euphyllophytes (Euphyllophytina)

Euphyllophytes are the sister group to the lycophytes. Although

the euphyllophytes encompass an astonishing morphological

diversity, they all share several features in common,

Figure 10.1. Comparison of alternation of generation phases between representative “bryophyte”

and tracheophyte life cycles to illustrate the evolutionary transition from a dominant autotrophic

gametophyte and a nutritionally dependent monosporangiate sporophyte in “bryophytes” to a

dominant autotrophic polysporangiate sporophyte in tracheophytes. In ferns, the gametophytes

are independent of the sporophytes; in seed plants, the microgametophytes are independent but

the megagametophytes are retained on the sporophyte. Figure modified from Singer (1997).

moss life cycle

bryophyte

gametophyte = dominant phase

sporophyte = monosporangiate

tracheophyte

sporophyte = dominant phase

sporophyte = polysporangiate

Meiosis

Spores

(1n)

Protonema

Sporangium

fern life cycle

Meiosis

Fertilization

Fertilization

Sporophyte

(2n)

Sporophyte

(2n)

Sporangium

(2n)

Spores

(1n)

Spore

germination

Sporophyte

(2n)

Gametophyte

(1n)

Gametophyte

(1n)

Sperm

(1n)

Sperm

Root

Roots

Rhizome

Sori

Scrus

Indusium

Archegonium

Archegonium

Egg

Egg (1n)

Embryo

(2n), young

sporophyte)

Gametophyte

(1n)

Gametophyte

(1n) Gametophyte

(1n)

Leafy

gametophyte

Leaf

Antheridium

Sperm

Egg

Archegonium

The Radiation of Vascular Plants 141

such as sporangia that terminate some lateral branches

(figs. 10.2 and 10.4), a distinctively lobed primary xylem strand

(Stein 1993, Kenrick and Crane 1997a) and a 30-kilobase

chloroplast inversion (Raubeson and Jansen 1992a). Early

members of the euphyllophyte lineage, such as Psilophyton

(fig. 10.4 inset), are referred to as “trimerophytes” and were

homosporous and leafless plants restricted to the Devonian.

They exhibited pseudomonopodial branching (overtopping)

resulting in a differentiation of the shoot system whereby one

axis is dominant with indeterminate growth (main axis continues

to grow) and the lateral axes were determinate (terminated

by sporangia). Later during the evolution of this lineage

the determinate axes were transformed into euphylls—leaves

that develop with an apical and/or marginal meristem resulting

in a gap being formed in the stele (stem vascular cylinder)

above the point of leaf insertion (Schneider et al. 2002), which

argues for a single origin of euphylls, rather than several independent

origins (Boyce and Knoll 2002). Therefore, as early

as the Devonian there was a major transition from vascular

plants without leaves to those that possessed euphylls (Beerling

et al. 2001, Shougang et al. 2003).

During the evolution of the Euphyllophytina there was a

split in the early-mid Devonian into two major clades, monilophytes

and lignophytes (Pryer et al. 2001). The monilophytes

(= Infradivision Moniliformopses, sensu Kenrick and Crane

1997a; Judd et al. 2002: ch. 7) include horsetails, eusporangiate

and leptosporangiate ferns, and whisk ferns (Psilotum and

relatives). The lignophytes include all seed plants and their

closest relatives (Doyle 1998b). The ancient radiation of these

two divergent lineages gave rise to what now is 99% of extant

vascular plant diversity.

Monilophytes

The monilophytes comprise five major extant lineages (fig.

10.5A): Equisetopsida (horsetails), Polypodiidae (leptosporangiate

ferns), Psilotidae (whisk ferns), Marattiidae (marattiaceous

ferns), and Ophioglossidae (moonwort ferns).

Previous assessments of relationships among these lineages

were contradictory and often placed one or more of them as

sister to the seed plants, implying that vascular plant evolution

had proceeded in a progressive and steplike fashion.

Recent recognition that these lineages are clustered together

in a single clade that is sister to seed plants has helped to stabilize

this pivotal region of the vascular plant phylogeny

(Kenrick and Crane 1997a, 1997b, Nickrent et al. 2000,

Renzaglia et al. 2000, Pryer et al. 2001, Rydin et al. 2002).

Among the extant monilophytes, the earliest-diverging

lineages are those with the poorest fossil record—the Psiloti-

Figure 10.2. Vascular plant phylogeny: relationships of early polysporangiate taxa. Gray triangles

indicate extant lycophyte and euphyllophyte crown groups; shaded box highlights extinct (†)

“rhyniophyte” stem group with some representative taxa. Critical synapomorphies are indicated

on the branches. Phylogeny based largely on Kenrick and Crane (1997:129, fig. 4.31) and Meyer-

Berthaud and Gerrenne (2001). Inset, Sketch of a representative early Devonian “rhyniophyte,”

Aglaophyton: A, dichotomously branched creeping and erect axes, the latter terminated by ovoid

sporangia; B, tiny central strand of unthickened water-conducting cells. Plant drawing from

Fischer et al. (1998).

142 The Relationships of Green Plants

dae and Ophioglossidae (fig. 10.5B)—eusporangiate ferns

(produce thick-walled sporangia containing numerous

spores) with such radically different phenotypes that their

recognition as sister taxa became apparent only after the accumulation

of data from a number of molecular markers

(Nickrent et al. 2000, Pryer et al. 2001). Morphological characters

that support this relationship are exceedingly difficult

to discern given the extreme simplification that one observes

in both their vegetative and reproductive structures. However,

these two monilophyte lineages share a reduction in root

systems, whereby Ophioglossidae have no root hairs and

Psilotidae have lost roots altogether, with both lineages relying

on endomycorrhizal associations for nutrient absorption

(Schneider et al. 2002).

How the remaining lineages of extant monilophytes

(Equisetopsida, Polypodiidae, and Marattiidae) are related to

one another is still unclear. Extant Equisetopsida (15 species;

Des Marais et al. 2003) and Marattiidae (300 species;

Hill and Camus 1986) are relatively species poor, but both

these groups have very rich fossil records in the Late Paleozoic

and Early Mesozoic (fig. 10.5B; Bateman et al. 1998,

Rothwell 1999, Liu et al. 2000, Berry and Fairon-Demaret

2001). In contrast, the Polypodiidae have had a rich fossil

record from the Late Paleozoic until the Recent period, with

extant taxa numbering greater than 10,000 species (Collinson

1996, Skog 2001). Polypodiidae share the notable characteristic

of being leptosporangiate—having sporangia with a

wall that is a single cell layer thick and containing relatively

few meiospores (<1000, usually 64).

Continued emphasis on increasing the availability of

molecular markers will likely improve resolution among

these deep branches in the monilophyte clade. However, it

Figure 10.3. Vascular plant phylogeny: relationships of lycophytes. Phylogeny based largely on

Kenrick and Crane (1997a:129, fig. 4.31) and Meyer-Berthaud and Gerrienne (2001); extinct taxa

are indicated with a dagger (†). Early in the evolution of the lycophyte lineage there was a

transition to sporangia that had a dorsoventral organization and that opened with transverse

dehiscence. The crown group of lycophytes shares a single origin of leaves (lycophylls) that

develop by an intercalary meristem. Bottom inset, Sketches of a representative early Devonian

lycophyte, Zosterophyllum: A, dichotomously branched axes, erect axes bearing lateral dorsoventral

sporangia; B, Tiny central vascular strand (protostele) composed of tracheids. Plant drawing

from Arens et al. (1998a). Top inset, Lepidodendron, typical arborescent lycopsid. Plant drawing

from Arens et al. (1998b). Taxonomic issues: Hsua = “rhyniophyte” sensu Banks (1975, 1992) =

putative zosterophyte sensu Kenrick and Crane (1997a); Nothia = “rhyniophyte” sensu Banks

(1975, 1992) = putative zosterophyte sensu Kenrick and Crane 1997a); Barinophyton = incertae

sedis sensu Banks (1975, 1992) = zosterophyte sensu Kenrick and Crane (1997a); Cooksonia =

“rhyniophyte” sensu Banks (1975, 1992) = polyphyletic, with some species part of Lycophytina

stem group sensu Kenrick and Crane (1997a).

The Radiation of Vascular Plants 143

will also be critical for future studies to incorporate morphological

data from fossil members pertinent to this clade if we

really are going to improve our understanding of the evolution

of monilophyte lineages through time and clarify ideas

concerning homology. These include arborescent relatives

of Equisetopsida, such as Archaeocalamites and Calamites

(fig. 10.5A); fossil relatives of Marattiidae, such as Psaronius

(fig. 10.5A), which was an important tree-fern-like component

of Carboniferous landscapes; and extinct Polypodiidae,

such as Botryopteris, which although less abundant and more

diminutive (Bateman et al. 1998, DiMichele et al. 2001), were

opportunistic and scandent members of the terrestrial ecosystem,

much as their living relatives are today.

As to the relationships of other fossil monilophytes of

the Devonian with highly divergent morphologies, such

as “iridopterid” (Ibykya), “cladoxylopsid” (Calamophyton,

Pseudosporochnus), and “zygopterid” ferns (Rhacophyton),

much work remains to be done (Bateman et al. 1998,

Rothwell 1999, Berry and Farion-Dermaret 2001). These

fossil plants have been discussed as relatives to horsetails

and ferns in the broad sense, but with no clear picture

emerging as to which are stem group or crown group members

(fig. 10.5A). Integrating these taxa into a phylogeny of

living members will certainly improve our understanding of

evolutionary transitions in morphology in this group.

Within the leptosporangiate ferns (Polypodiidae), our

knowledge of extant fern relationships has dramatically improved

over the last 10 years (Hasebe et al. 1995, Pryer et al.

1995, 2001, Schneider 1996, Wolf et al. 1998). A few highlights

include the determination that Osmundaceae is the

earliest-diverging leptosporangiate family; gleichenioid and

dipteroid ferns together with Matonia are a monophyletic

early-diverging group and not, as was once thought, a paraphyletic

grade of basal ferns; the heterosporous ferns

(Marsileaceae and Salviniaceae) are sister group to a large

dade of derived homosporous ferns that includes tree ferns

and the species-rich “polypodiaceous” ferns; the most derived

lineage of ferns including dennstaedtioid, ptendoid,

dryopteridoid, and polypodioid ferns, once thought to be

polyphyletic (Smith 1995), are now known to be monophyletic.

Extant lineages differ enormously in their diversity and

history, including their time of origin, time of greatest diversity,

and time of decline (fig. 10.5B). Osmundaceous ferns,

the most basal lineage of leptosporangiate ferns, are a small

group today, but they were highly diverse from the Permian

and throughout the Mesozoic until they began to decline in

the Upper Cretaceous (Skog 2001). Other basal Polypodiidae

lineages, such as the gleichenioid and schizaeoid ferns, followed

a similar pattern (fig. 10.5B). In stark contrast, the

clade of ferns (Polypodiales; fig. 10.5B) with the greatest diversity

today (>80% of all extant leptosporangiate ferns)

might have originated as early as the Cretaceous (Skog 2001;

but see Collinson 1996) and has diversified throughout the

Cenozoic (Collinson 2001). The origin and diversification

pattern observed in this clade of ferns parallels that observed

in the angiosperms, albeit at a relatively smaller scale

Figure 10.4. Vascular plant phylogeny. Relationships of “trimerophytes” and euphyllophytes (= monilophytes + lignophytes).

Phylogeny based largely on Kenrick and Crane (1997a:240, fig. 7.10) and Meyer-Berthaud and Gerrienne (2001). Extinct (†) taxa are

in shaded boxes. The transition to “trimerophytes” is marked by a change to pseudomonopodial branching, whereby a main indeterminate

axis develops and overtops lateral determinate axes. Euphyllophytes share a common origin of leaves (euphylls) that develop

by an apical and/or marginal meristem, a 30-kilobase inversion in the chloroplast genome organization, and a distinctively lobed

primary xylem strand. Inset, sketch of Psilophyton shows sterile axes with forked tips and fertile lateral axes terminated by sporangia.

Plant drawing from Arens et al. 1998c).

144 The Relationships of Green Plants

The Radiation of Vascular Plants 145

(H. Schneider, E. Schuettpelz, K. M. Pryer, R. Cranfill,

S. Magallуn, and R. Lupia, unpubl. obs.).

Lignophytes

The lignophytes (Doyle and Donoghue 1986, Rothwell and

Serbet 1994, Bateman et al. 1998, Doyle 1998b) include all

plants that reproduce via seeds (spermatophytes), together

with their immediate “seed-free” precursors (fig. 10.6). Spermatophytes

are the only living lignophytes, and with more

than 260,000 species, they constitute the most diverse group

of extant plants. The overwhelming majority of this diversity

belongs to angiosperms (flowering plants), which produce

their seeds enclosed within carpels (modified leaves).

The remaining spermatophytes are “gymnosperms,” represented

by four extant lineages (fig. 10.6): Cycadophyta

(cycads, ~130 species), Gnetophyta (gnetophytes or gnetales,

~70 species), Ginkgophytes (Ginkgo biloba, a single living

species), and Coniferophyta (conifers, ~550 species). All

“gymnosperms” produce naked seeds, that is, not enclosed

within a carpel.

Lignophytes share the capability of forming wood by

means of a bifacial cambium—a region of persistent cell division

in their stems that produces secondary phloem toward

the outside and secondary xylem toward the inside. At maturity,

these secondary xylem cells form wood. Lignophyte

precursors share a tetrastichous branch arrangement and a

distinctive form of protoxylem ontogeny (= Infradivision

Radiatopses, sensu Kenrick and Crane 1997a; Schneider et al.

2002; fig. 10.6). Pertica, formerly regarded as a “trimerophyte”

(sensu Banks 1975, 1992), and Tetraxylopteris, a “progymnosperm,”

have been tentatively identified as lignophyte precursors

(Kenrick and Crane 1997a; fig. 10.6). The earliest

lignophytes had a gymnospermous wood-producing stem

anatomy, and some were large trees. Unlike gymnosperms,

however, these woody plants did not produce seeds, but rather

were free-sporing. Collectively, these plants are known as

“progymnosperms” and were important components of the

mid-Paleozoic vegetation (Meyer-Berthaud et al. 1999). Early

representatives of this group, such as the Middle Devonian

(Eifelian) Aneurophyton, produced a single type of spore

(homospory). Younger “progymnosperms” produced two

different types of spores (heterospory), microspores and

megaspores, which gave rise to microgametophytes/sperm

cells and megagametophytes/egg cells, respectively. The megagametophyte

and microgametophyte phases of the life cycle

of these fossils are believed to have been retained within the

walls of the megaspore and the microspore, respectively (endospory),

which is the condition observed in all known living

heterosporous plants. The heterosporous “progymnosperms,”

including the Late Devonian Archaeopteris (fig. 10.6, inset), are

considered to be the closest relatives to the seed plant lineage

(spermatophytes).

Although heterospory evolved several times in different

tracheophyte lineages, only in the lineage leading to spermatophytes

was it accompanied by a sophisticated suite of innovations

and modifications involving the structure and function

of megagametophytes, microgametophytes, and associated

sporophytic tissues, giving rise to the complex structures that

are seeds (Bateman and DiMichele 1994). The fossil record

indicates that the series of steps leading from heterospory to

seeds occurred a single time in the evolution of plants (Crane

1985, Doyle and Donoghue 1986, Nixon et al. 1994, Rothwell

and Serbet 1994). Several Late Devonian (Fammenian) reproductive

structures, such as in Elkinsia and Archaeosperma (fig.

10.6), exhibit some of the early steps in the evolution of the

seed, but lack several critical attributes found in later forms.

These structures consisted of an unopened (indehiscent) megasporangium

that retained within its walls a single functional

megaspore with an endosporic megagametophyte. Partially

fused protective lobes of sporophytic origin (integumentary

lobes) enveloped the indehiscent megasporangium, thereby

retaining the megasporangium on the sporophyte parent plant.

Subsequent spermatophyte lineages had seeds with a

completely fused envelope (integument) that enclosed the

Figure 10.5. Vascular plant phylogeny: relationships of ferns and horsetails (monilophytes). (A) Phylogeny based largely on Pryer

et al. (2001) and Kenrick and Crane (1997a). The monilophytes share the positional and ontogenetic characteristic of having their

protoxylem confined to the outer lobed ends of the xylem strand (“necklacelike,” L. moniliformis). The greatest species diversity

within the monilophytes (~12,000 species) is found in the Polypodiidae clade, which shares the derived leptosporangiate condition:

thin-walled sporangia that produce a low number of spores (generally 64). Sketch of representative extinct crown group

monilophytes: left inset, Psaronius, Pennsylvanian marratialean “tree fern.” Plant drawing from Arens et al. (1998d): right inset,

Calamites, Carboniferous arborescent relative of the modern horsetail, Equisteum. Plant drawing from Arens et al. (1998e) By

integrating extant taxa (Pryer et al. 2001) together with their fossil (†) relatives (Kenrick and Crane 1997a, Berry and Fairon-Demaret

2001, Meyer-Berthaud and Gerrienne 2001) in this phylogeny, we hope to demonstrate that much of the morphological diversity

that once existed in this clade is not represented in studies that consider only the living taxa. The representative fossils (†) encompass

several groups: “cladoxylopsids” (Calamophyton, Pseudosporochnus), “iridopterids” (Hyenia, Ibyka), “sphenophylls” (Sphenophyllum,

Bowmanites), “zygopterids” (Rhacophyton, Zygopteris), and Stauropteris. (B) Phylogeny of extant monilophytes (Pryer et al. 2001)

plotted onto a geological time scale (Geological Society of America 1999) to illustrate the diversification of leptosporangiate ferns

through time (Skog 2001). Dashed lines indicate ghost lineages—lineages without a corresponding fossil record (a striking example

is the branch that unites Psilotidae and Ophioglossidae); continuous lines indicate congruence between fossil record and phylogeny.

Thickened areas only generally approximate the relative diversity of groups through time.

146 The Relationships of Green Plants

Figure 10.6. Vascular plant phylogeny: relationships of seed plants and the extinct “progymnosperm,”

“pteridosperm,” and derived “trimerophyte” stem group lineages. Phylogeny based

primarily on Kenrick and Crane (1997a). Members of this clade share the positional and ontogenetic

characteristic of having protoxylem with multiple strands occurring along the midplanes of

the lobed primary xylem ribs, corresponding to the “radiate protoxylem” group of Stein (1993)

(= Infradivision Radiatopses in Kenrick and Crane 1997a). The greatest species diversity within

this clade is found in the angiosperms (~260,000 species), which share several derived characters,

including a carpel that encloses the seed and highly reduced male and female gametophytes.

Critical synapormophies (e.g., secondary xylem, heterospory, seed, sealed micropyle) are plotted

onto the topology at positions we believe best reflect our current understanding of the evolution

of these features. A “seed” is a complex structure and is defined here as a megasporangium

containing a single functional megaspore enclosed in one or more integuments of sporophytic

origin. Inset, Sketch of representative extinct “progymnosperm”: Archaeopteris. Plant drawing

from Arens et al. (1998f). Relationships among all five major extant seed plant lineages remains

elusive with no consensus as to the closest relative to the angiosperms. The figure attempts to

illustrate that taking into account all the lineages (extinct and extant) that produce naked seeds

(“gymnosperms”) as a whole, results in “gymnosperms” being a paraphyletic assemblage,

regardless of how the modern groups turn out to be related (i.e., even if all four living lineages are

a monophyletic sister group to the angiosperms). Extinct (†) lineages interspersed among the five

extant lineages of seed plants represent such groups as Bennettitales, Pentoxylales, Caytoniales,

Corystospermales, and Cordaitales.

The Radiation of Vascular Plants 147

megasporangium except at its apex, where a small opening

remained. Through this aperture (the micropyle), pollen

grains entered the pollen chamber and released either sperm

cells or formed pollen tubes to establish contact with the

megagametophyte and, eventually, with the egg cells. The

earliest seeds with a completely fused integument and a welldefined

micropyle are known from the lowermost Carboniferous

(e.g., Stamnostoma; Long 1960). Spermatophyte

diversity increased dramatically during the Carboniferous,

giving rise to several lineages with fernlike foliage, collectively

known as “pteridosperms” or “seed ferns” (fig. 10.6). These

plants encompass an extremely broad array of seed morphology

and reproductive biology, but they all have seeds with a

micropyle that did not seal following pollen grain capture.

How “pteridosperm” lineages are related is incompletely

understood (fig. 10.6); however, it appears that the earliestdiverging

lineages were composed of forms such as

Lyginopteris, in which pollen reception involved sophisticated

elaborations of the megasporangium wall apex, but in later

forms, such as in Medullosa and Callistophyton, the function

of pollen reception was taken up by the micropyle formed by

the integuments. The Mesozoic “glossopterids” are putative

“pteridosperms,” although some authors have indicated that

they may be more closely allied with members of the seed plant

crown group (Doyle 1998b, Willis and McElwain 2002).

Plants in which the micropyle became sealed after pollen

grain capture gave rise to the clade that includes the five

major groups of living spermatophytes, as well as many other

lineages that are now extinct (fig. 10.6). Included among

these are some Mesozoic plants that various authors have

previously called “seed ferns.” In this chapter, we restrict the

use of “seed ferns” to seed plants without a sealed micropyle;

therefore, taxa previously regarded as “seed ferns” that have

a sealed micropyle, such as the Caytoniales, no longer fit this

definition and are regarded here as part of the seed plant

crown group. Discerning relationships among major living

spermatophyte clades and their extinct relatives has proven

to be extremely problematic, due, at least in part, to the old

age of most of the lineages involved (except probably for the

angiosperm crown group), and to the scant proportion of

overall spermatophyte diversity represented by the living

members. The use of morphological and molecular data in

phylogenetic studies has resulted in dramatically different

views. Morphological studies benefit from incorporating information

about extinct clades but are affected by the problematic

interpretation of homologies for insufficiently known

characters. Molecular studies are severely impacted by the

relatively meager taxonomic representation of overall spermatophyte

diversity that is provided by living representatives.

Analyses of morphological data have recognized a clade

(the anthophytes) that includes angiosperms and gnetophytes,

together with the extinct Bennettitales and Pentoxylales (Crane

1985, Doyle and Donoghue 1986, Rothwell and Serbet 1994).

As a result, the idea that, among living spermatophytes, angiosperms

and gnetophytes are most closely related (anthophyte

hypothesis, fig. 10.7A) prevailed for more than a decade

(Donoghue and Doyle 2000). However, increasing evidence

from studies based on molecular data has now rejected the

phylogenetic closeness between angiosperms and gnetophytes

(Donoghue and Doyle 2000), although, at this writing, none

of these studies have yet converged on an alternative, wellsupported

scheme of relationships among the living major

clades of spermatophytes. The conflict spans not only analyses

based on morphological versus molecular data, but also

analyses based on different types of molecular data and on

different approaches to analytical methods and taxon sampling

(e.g., Sanderson et al. 2000, Magallуn and Sanderson 2002,

Rydin and Kдllersjц 2002, Rydin et al. 2002).

Several studies based on different genes and gene combinations

lace angiosperms as the sister to all other living

spermatophytes (gymnosperm hypothesis; fig 10.7B), suggesting

that angiosperms are not closely related to any one

of the extant groups of gymnosperms. Most molecular-based

studies indicate a close association between gnetophytes and

conifers, some even placing gnetophytes within conifers, thus

rendering the conifers a paraphyletic assemblage (e.g., Chaw

et al. 2000, Gugerli et al. 2001, Magallуn and Sanderson

2002, Soltis et al. 2002). The suggestions of extant gymnosperm

monophyly and conifer paraphyly are unexpected and

should be viewed as provisional. Still other studies (e.g.,

Figure 10.7. Alternative hypotheses of relationships (A, B, C)

among five major extant lineages of seed plants. The anthophyte

hypothesis places the gnetophytes as sister to the angiosperms.

This hypothesis is based mostly on morphological evidence

(Crane 1985, Doyle and Donoghue 1986), but most recent

molecular studies (e.g., Barkman et al. 2000) have not supported

any evidence for an anthophyte clade (but see Rydin

et al. (2002).

148 The Relationships of Green Plants

Graham and Olmstead 2000, Sanderson et al. 2000) have

shown that sometimes gnetophytes can be placed as sister

to all other extant seed plant groups (gnetophyte hypothesis;

fig. 10.7C).

A close proximity between gnetophytes and conifers has

been proposed previously on the basis of various anatomical

and morphological similarities (Coulter and Chamberlain

1917, Bailey 1953, Bierhorst 1971, Carlquist 1996), but the

placement of gnetophytes within the conifers has disturbing

implications from a traditional perspective on conifer evolution.

Conifers show remarkable homogeneity in their vegetative

and reproductive morphological attributes, including

a growth form that is nearly always a monopodial tree, mostly

needle-shaped leaves, gymnospermous wood, simple pollen

cones, and usually compound seed cones with a distinctive

organization, whereas gnetophytes display extraordinary

variability in each of these characters. A molecular character

often cited in support of conifer monophyly is the loss of one

of the inverted repeat (IR) copies of the chloroplast genome,

which is shared exclusively by all conifers (Raubeson and

Jansen 1992b).

Although it is certainly possible that angiosperms are not

closely related to any one lineage of living gymnosperms, it is

important to keep in mind that molecular evidence alone simply

cannot provide information regarding the relationship of

angiosperms to any of the extinct groups of gymnosperms.

Regardless of how the issue of relationships among the five

extant seed plant lineages is finally resolved, “gymnosperms”

in the broad sense, which include the early-diverging fossil

lineages, are not monophyletic (fig. 10.6). It is highly likely that

at the base of the lineage leading to modern angiosperms, there

were some gymnosperms that are now extinct.

Taken as a whole, there have been remarkable improvements

in our understanding of relationships within the major

living spermatophyte lineages. Well-supported examples

include the determination that Cycas is the sister to all other

cycads; among living gnetophytes, Gnetum and Welwitschia

are more closely related to one another than either is to Ephedra;

Pinaceae is the earliest-diverging clade among living conifers;

and Araucariaceae plus Podocarpaceae is sister to a

clade that includes Taxaceae (yew), Taxodiaceae (redwood),

and Cupressaceae (cypress) (Barkman et al. 2000, Chaw et al.

2000, Gugerli et al. 2001, Magallуn and Sanderson 2002,

Rydin et al. 2002).

A number of significant innovations originated on the

lineage leading to angiosperms, including the carpel, which

encloses the seeds, a second integumentary layer around the

seed, and an extreme reduction of the megagametophyte

(Bateman et al. 1998, 1998b, Theissen et al. 2002). Although

our understanding of relationships within the angiosperms

has improved dramatically over recent years (Qiu et al. 1999,

2000, Soltis et al. 1999, 2000; see ch. 11 in this vol.), the

nature and homology of several characters unique to angiosperms

are still unclear.

Vascular Plants, the Phylogenetic

and Genomic Revolutions, and Fossils

Our understanding of the phylogeny of vascular plants has

changed tremendously in the last 20 years due to the introduction

of molecular techniques (Soltis and Soltis 2000) into

plant sciences and the concomitant application of explicit

phylogenetic methods to both molecular and morphological

data. Before that time (and to some extent even in the

present), an Aristotelian interpretation of relationships prevailed,

one that promoted a linear and unidirectional transition

in vascular plant evolution from simple to complex

organization. For example, it was commonly thought that

the whisk fern Psilotum was a “living fossil” or remnant of

the earliest lineage of vascular plants, given its remarkable

superficial resemblance to the dichotomously branched

“rhyniophyte” fossils (Parenti 1980, Gifford and Foster 1989,

Rothwell 1996, 1999, DiMichele et al. 2001). We now know

that Psilotum is well embedded within the euphyllophytes and

that its scalelike leaves and lack of roots do not indicate an

ancient origin, but are rather the result of morphological simplification

during the evolution of these plants (Schneider

et al. 2002).

Although there has been remarkable progress in our understanding

of plant evolution, some relationships are still enigmatic.

For example, relationships among the major seed plant

lineages, recently thought to be close to resolution (Donoghue

and Doyle 2000), are now under renewed scrutiny, and we

are almost no farther along than we were 20 years ago in

identifying the closest relatives to the angiosperms. Molecular

data appear to have rejected the anthophyte hypothesis

(fig. 10.7A)—gnetophytes sister to angiosperms—but they

continue to be ambiguous about the position of gnetophytes:

either within the putatively monophyletic extant gymnosperms

(gymnosperm hypothesis; fig. 10.7B), or sister to all other

living seed plants (gnetophyte hypothesis; fig. 10.7C;

(Goremykin et al. 1997, Doyle 1998, Barkman et al. 2000,

Frohlich and Parker 2000, Sanderson et al. 2000, Magallуn

and Sanderson 2000, Rydin and Kдllersjц 2002, Rydin et al.

2002).

Papers on vascular plant phylogeny are now being published

that include in excess of eight or more genes (Graham

and Olmstead 2000, Soltis et al. 2002), but a clear picture

of branching relationships resulting from the deep seed plant

radiation is still not emerging. Two approaches are currently

favored to resolve these persistently stubborn questions. The

first promises to take advantage of the exceptional progress

in our ability to sequence large pieces of whole genomes

under the assumption that the accumulation of large amounts

of genetic information and, in particular, data about structural

mutations within the genome may provide a breakthrough.

The second favors the integration of more than 100

years of accumulated knowledge of fossils into a modern

phylogenetic framework. Exactly how to go about doing this,

The Radiation of Vascular Plants 149

integrating data from molecules together with morphological

characters from both living and extinct taxa, is one of

the exciting challenges now facing us (Doyle and Donoghue

1987, WiIkinson 1995, Nixon 1996, Wiens 1998, O’Leary

2000, Kearney 2002). The latter approach reflects a rather

surprising renaissance in how to view morphological data in

modern phylogenetic studies. Pushed aside in the early days

of DNA sequencing, when molecules were thought to be the

holy grail for sorting out all questions on early land plant

evolution, they are now back in favor once again as a valuable

resource in more synthetic approaches. In addition, there

has been a recent notable increase in the description of exciting

new plant fossils (e.g., Sun et al. 1998, 2002, Friis et al.

2001a).

Because recent advances in our understanding of vascular

plant relationships are due mostly to the introduction of

molecular data, our interpretations are nearly exclusively

restricted to living taxa. When one stops to ponder the vascular

plant tree through hundreds of millions of years, one

is struck not only by the large number of taxa that have come

before and that are no longer extant (and that are not available

for DNA sequencing studies), but also the extent of

morphological diversity that is no longer represented in living

plants. Extinctions have wiped out major parts of whole

lineages that contributed heavily to plant diversity in the

Paleozoic and Mesozoic. For example, extant moniliophytes

consist of five distinct and ancient lineages. With the exception

of leptosporangiate ferns (Polypodiidae), these lineages

are not rich in either species number or morphological diversity.

However, some of these lineages, such as the horsetails,

were among the more diverse and dominant groups in

the Upper Paleozoic and Early Mesozoic. Although horsetails

have managed to survive until today with one speciespoor

lineage, Equisetum, other groups of monilophytes, such

as Cladoxydopsidales and Zygopteridales, have gone completely

extinct. On the surface, this would seem to support

the idea that terrestrial ecosystems have witnessed a sequential

replacement of lineages through time whereby, for example,

such groups as the lycophytes, which were dominant

in the Paleozoic, came to be superseded in diversity by the

euphyllophytes, especially seed plants (Niklas et al. 1985). This

has led to the seemingly popular notion that once such lineages

“crash”: they either go extinct or experience a prolonged

period of stasis. However, some of these “superseded” lineages

have undergone subsequent radiations, as observed in

lycophytes (Late Tertiary; Wikstrцm and Kenrick 2001) and

derived leptosporangiate ferns (Late Cretaceous-Early Tertiary;

H. Schneider, E. Schuettpelz, K. M. Pryer, R. Cranfill,

S. Magallуn, and R. Lupia, unpubl. obs.).

The recent implementation of highly sophisticated genetic

tools to study the plant genome and the expression of

its genes has generated a new breed of studies that integrate

the study of plant development with evolution (Cronk 2001,

Cronk et al. 2002, Schneider et al. 2002). This approach can

be used to explore the evolution of critical morphological

characters, such as the origin of leaves, for example, that have

been the subject of long-standing controversies (Langdale

et al. 2002, Schneider et al. 2002). Incorporating data from

fossils and plant development in integrative and comparative

studies promises to help us to overcome our currently

incomplete knowledge of vascular plant relationships

through time. The results of such studies will inform our

understanding of the evolution of these extinct taxa, will

afford us clearer insights into the morphological evolution

of extant plants, and will even permit us to interpret fundamental

changes in global ecology—including climate—

throughout the last 450 million years (McElwain et al. 1999,

Beerling et al. 2001, Berner 2001, Driese and Mora 2001,

Willis and McElwain 2002).

Acknowledgments

We thank Joel Cracraft and Michael J. Donoghue for inviting us

to participate in this symposium and for their patience and

encouragement during manuscript preparation. Support from

the National Science Foundation to the “Deep Time” Research

Coordination Network initiative has been helpful in bringing

the coauthors and others together to discuss several points

made in this chapter. K.M.P. and H.S. gratefully acknowledge

grant support from the NSF (DEB-0089909). An exceptional

website on early land plants, developed by Nan C. Arens and

Caroline Strцmberg, was useful to us (available at http://

www.ucmp.berkeley.edu/IB181/HpageIB181.html). It was the

source of several plant drawings by C. Strцmberg, reproduced

here courtesy of the University of California Museum of

Paleontology.

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