Early Lycophyte Evolution

25 Pages·2001·12.7 MB·English

by  Patricia G Gensel

American
Fern
Journal 91(3):74-98
(2001)
Early Lycophyte
Evolution
Patricia Gensel
G.
Department NC
of Biology, University of North Carolina, Chapel 27599
Hill,
Christopher M. Berry
Department
of Earth Sciences, Cardiff University, Cardiff, CFlO 3YE, Wales, United Kingdom
Abstract
known
have
phylls, the longest history of any group of vascular land The
plants. early evolution of the
group reviewed
is concentrating on the Late Silurian and Devonian record of Lycopsida and Zos-
terophyllopsida. and
Distinct root-like shoot-like axes in zosterophyllopsids and lycopsids
are
first
recorded in the Early Devonian and can be compared development
to the later of pseudobipolar
growth
of tree-shaped lycopsids with upward-growing
trunks and branch systems and downward-
growing rooting systems. The development
of stigmarian
rootlets postdates the evolution of pseu-
dobipolar growth, recorded Middle
first in the Devonian, according to current evidence. Other
important events in early lycophyte evolution during the Devonian include changes mor-
in leaf
phology, modification of sporophylls, and
the eventual appearance
of the lycopsid
strobili.
What
a Lycophyte and When
is did Lycophytes Appear?
The =
lycophytes
club mosses and
related plants) are regarded as a distinct
(
lineage of vascular plants with long
a evolutionary
history. Considerable
di-
much
versity evident
is for of their existence, although only 7+ one
four
(or
if
accepts
either 011gard's Wagner and
(1987] or
Beitel's (1992) splitting of Ly-
copodium
into several genera) herbaceous
genera
are recognized today
[Lyco-
podium
(and
segregates), Phylloglossum, and
Selaginella, Club mosses
Isoetes).
have
long been
defined
as plants with microphyllous
leaves, axillary or adax-
borne
ially reniform sporangia with
dehiscence along and
their distal margin,
mostly exarch xylem
maturation; such now
plants are included
in the class
Lycopsida
("lycopsids") by Kenrick and
Crane
(1997). Extinct taxa attributed
to Zosterophyllopsida
(and
possibly including
barinophytes) considered
are
closely
related
to lycopsids,
either
as ancestral or sister taxa (Gensel, 1992;
Hueber,
1992; Bateman,
1992; Kenrick and
Crane,
being
1997), similar in spo-
rangium
shape and xylem
attributes but from
differing lycopsids in lacking
and
leaves
leaf-borne
sporangia. Additionally they have
vascularized sporan-
^
gial stalks
(Fig.
l).
Redefinition of
"lycophytes" and
"lycopsids".—
Several workers emphasize
(M
ck and Many
Crane,
1997).
demonstrate
that Ivnnnbvt.
J
Kranz and
recent, extensive
morphological
phylogenetic
and
analysis of living extinct
monophyly
plants,
supported, and
is zosterophylls and
lycopsids
are inter-
preted two
as classes in a larger group, subdivision Lycophytina
This
(Fig.
1).
GENSEL & BERRY: EARLY LYCOPHYTE EVOLUTION
75
Anisophyton
t
Kontona
t
r*- Crenabcaulis
t
^ Sawdoniaceae
Serrulacautis
t
Deheubarthia
t
Sawdonia
t
Tttfinkopfiyton
t
Sawdoniales
\ Bartnop^yton alroiiHorme
t
obscumm
darmoptiyton Barinophytaceae
f
Protoberinophyion
t
^ Zosterophyltopsida
- |— Euphyilophylina
u ^^ ' Hsoaf Hsuaceae
1Lycophytina '
.
|
Gossttngia
— t
Lycopsida
Eulraohe<^hytes
\
Go&stinQiaceae
- Zosterophyllopsida
-^
Cooksonia cambrensrs Zosterophynum tfivgricatum
t
f
J^- f^enatm f Zosterophyttum fertlte t
Tracheophyta
Uskiefta t ZosterophyHom tianoveranum
\ t
*- Yuma
fle£>yc/Ma
\ t
+-
SartHmania
\ Discalis
t
^
Cooksonia pertonn
t
Zosterophyttum Oeciduum
t
^
Cooksonia cahdonica
t
Hupefzia
Rhyntopsida
Asteroxyton
f
Lycopsida
Baragwanattiia
t
Lycophytina Drepanopnycus
\
\
Rhyniophylina sensu Banks
3|e
tiothiS^
sensu Banks
Zosterophyllophytina
Acfoketophyion
t
A sensu Banks
Ttirnerc^hylina
Zosterophyttum myretonianum
t
Gumuia
t
Hwat
Hickiingta
t
Psifoptjyton
t
A B
# Zosteroptiylkiphytina sensu Banks
consensus showing relationships among several polysporangiophyte taxa and
trees
Fig. Strict
1.
conducted by Kenrick and Crane A) Adapted from
among lycophytes according to analyses (1997).
Kenrick and Crane, 4,31. B) From Kenrick and Crane, fig. 5.25, with permission. Zosterophyl-
fig.
lopsida and Lycopsida are highlighted. See text for discussion. Not all taxa discussed in the text
because of differences in preservation and therefore absence of characters for
are included, partly
some
taxa.
237-238) by the following synapomorphies: **more
group defined
larger is [p.
lum
sporangium margin, conspicuous cellular thickening
hiscence along distal
on
along sporangial dehiscence line, sporangia short, laterally inserted stalks,
Within
from
and
clade largely consisting of lycopsids, a large
Zosterophyllopsida, a
the
Zosterophyllopsida sensu Kenrick and Crane
taxa.
IB) are defined by only two synapomorphies, namely circinate growth and a
Among
unresolved
two-rowed arrangement of sporangia. the single
unique,
excluded from Zosterophyllopsida sensu stricto are several plant genera
taxa
among
placed the zosterophylls, several species
originally
[Rebuchia, Discalis)
—
AMERICAN FERN VOLUME NUMBER
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91
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lyretonian
forms
plants traditionally considered zosterophylls The
as paraphyletic. incomplete
among
data the taxa analyzed characters employed, and
for all lack of reso-
lower
lution at levels in the cladogram, indicates further investigation of char-
and
acters character homologies needed. Thus
these conclusions should be
is
regarded with caution
until additional data are available.
Kenrick and Crane
second
(1997) define the clade, the Lycopsida
IB),
[Fig.
by synapomorphies
the of microphylls, xylem
stellate strand, vascularized
leaves, sporophylls (close association of sporangium and and
loss of spo-
leaf),
rangial vasculature. Lycopsida includes clade composed
a of three possibly
transitional genera, Asteroxylon, Drepanophycus, and
Baragwanatbia, and
a
second
larger clade of plants traditionally considered The
as lycopsids.
first
composed
clade
is of taxa that do not possess of the characters
all definitive
of lycopsids Asteroxylon and Drepanophycus
have
cauline sporangia with
a
vascularized and Asteroxylon
stalk, lacks full vascularization of lateral ap-
pendages. Neither has sporangium mem-
a associated with
a occurs
leaf, as in
bers of the lycopsid clade and most probably Baragwanathia
in (Hueber,
1992).
—The
APPEARANCE
occurrence of the genus Baragwanathia
in the pre-
sumed
late Silurian (Ludlow;
Garratt et al, 1984; Rickards, 2000) of Victoria,
Australia suggests
a possible pre-Devonian
diversification of lycophytes. Zos-
terophylls also are recorded from
these but
strata, detailed descriptions are
lacking (Tims and Chambers, Most
1974). other occurrences
of late Silurian
much
plant remains
are smaller and
in size simpler in organization than
either
Baragwanathia An
or Zosterophyllum
(Fig. interesting exception
2). the as-
is
semblage
of zosterophylls and
related plants fi^om well-dated Ludlow
late
stra-
ta of Bathurst Island (Kotyk new
et al., in prep.). These forms support an early
diversification of the lycophyte
lineage.
Possible precursors.—
Most
polysporangiate
plants with branched
plants
(i.e.
sporophytes) with round
reniform
to sporangia
referred rhynioph-
to either as
yte?, cooksonioid, or rhyniophytoid
(Taylor, 1988; Hueber,
1992) represent
possible
close
relatives or precursors
to the lycophytes but
currently there are
no
obvious
candidates. Outline drawings
(Fig. of several Late Silurian and
2)
small
—
and
X - «**^-»-"-'- LJiAi^^vu %j.±±\^ iiAvju,t^o UA LAciiioLjtJllljt;. 1 null ollldll
simple
size, construction,
lack of anatomical
and
preservation,
firagmentary
make
preservation more
precise
inference
impossible, but those with globose-
reniform may
sporangial
construction
represent
likely candidates lycophy-
for
earliest
Island
which
resembles
a pseudomonopodial
Cooksonia
or very simple Zosterophvl-
r
/
lum ^ i-
2
n.
ffip.
some
the plexus
of
latest Silurian-earliest Devonian
rhyniophytoids
(but their rela-
GENSEL & BERRY: EARLY LYCOPHYTE EVOLUTION
77
plants (A
Silurian -
1)
C
x3
A
Lochkovian O)
plants
(J -
J
^
x4
x18
oo
*
contains cryptospores
oo dyads
^
obligate tetrad
®
miospores
trilete
N
—
A
and Devonian meso- and
Selected Silurian earliest megafossils. Pridoli plants.
Fig. 2. late I)
B— E—
A) from Cai et al. (1993); D] from Fanning et al. (1991); G) from Edwards (1996). H) from
—
Kotyk (1998). from Basinger et al, (1996). O). Lowermost Devonian plants from Edwards
I) J
(1996).
by
tionship these simple plants thus far is not extensively tested cladistic
to
When
Renalia and Cooksonia were
precursors.
represent likely
analyses), also
Kenrick and Crane, they formed
phylogenetic analyses of part
included in the
and were
basal polytomy of the polysporangiophytes interpreted
of the large
stem-lineage zosterophylls. Further investigation of these early
as possible
needed.
plants
is
AMERICAN FERN VOLUME NUMBER
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3 (2001)
The
present contribution notes major advances and addresses
several areas
of concern in regard to early lycophyte evolution and diversification, including
maj
phyte
structures.
Current Data on
Zosterophylls
As
a probable sister group[s) or stem group(s} to lycopsids, zosterophylls
may
taxa
ome
alter conceptions of relationships between zosterophylls and lycopsids nor aid
Th
fying ordinal or familial delimitation within zosterophylls.
main
by two
genera, Saivdonia ornata 3A) and
(Fig. Oricilla bilinearis 3C).
(Fig.
Differences include sporangium and
orientation presence/absence of emer-
gences (multicellular appendages). The Sawdonia and
clade (Kenrick Crane's
Sawdoniaceae) more
exhibits upright orientation of sporangia and emergences
of varying morphology and arrangement, while and
the Oricilla clade (Kenrick
Crane's Gosslingiaceae) naked and
exhibits axes sporangia attached
stalks per-
pendicular The
to the axis. Zosterophyllum depicted 3B
in Fig. exhibits heli-
similar
and
Beyond these two well- supported now have new
clades, w^e considerable
in-
some
formation about more
of the basal lineages, discussed
next.
which
Plants appear very similar Zosterophyllum
to (Fig. SB], except that
sporangia more
are scattered and borne on many
longer than
stalks in previ-
ously described Zosterophyllum
found
species, are in Pragian deposits of Chi-
na and
Bathurst Canadian
Island, Arctic Archipelago These do
(Kotyk, 1998).
not
quite existing generic or species delimitations, but they become more
fit as
completely known,
they might
aid in a better understanding of the genus Zos-
terophyllum
or closely The
allied taxa. separation of several Zosterophyllum
species
into separate clades Kenrick and
in Crane's analysis based mostly
is
on symmetry
of sporangial arrangement and
presence/absence
of circinate ver-
nation. However,
these
characters are not easy to evaluate and their coding
may
not them
reflect that data about are incomplete; most
particularly, several
taxa lacked anatomy.
document
It is difficult to the presence or (known) ab-
sence
of
circinate vernation (and true terminations). The character "symmetry
may
of sporangial arrangement"
be
difficult to ascertain because determining
sporangia
if are helically arranged or are subopposite in two rows
difficult
is
A
in compression
remains. two-rowed
pattern could be produced by widely
a
spaced, very simple
helix coupled with
twisting of either sporangial stalks or
axis
new
indicate these Zosterophyllum and
species
other Zosterophyllum-\ike
may
plants represent stem
zosterophylls for which only a few distinguishing
characters
are present.
GENSEL & BERRY: EARLY LYCOPHYTE EVOLUTION
79
mm
mm
5 1
-I
mm
5
-^0
c
mm
1
mm
mm
2
-1
-1
1
D
Selected putative basal lycophytes or zosterophyllopsids. A, Cj Representatives of Zos-
Fig. 3.
terophyllopsida sensu Kenrick and Crane. A) Sawdonia ornota (Dawson) Hueber, based on spec-
imens from Gaspe. C) OriciUa bilinearis Gensel, redrawn from Gensel (1982], B) Depiction of a
Zosterophyllum with helically arranged sporangia, a stem group taxon according to Kenrick and
carvata Gerrienne from the Early Devonian of Belgium. Note thickening
Crane D] Gosferia
(1997).
near base of sporangium. Redrawn from Gerrienne (1991). E) Ensivalia deblondii Gerrienne, a
probable zosterophyllopsid from the Early Devonian of Belgium, F) Faironella valentula Gerrienne,
uncertain, from the Early Devonian of Belgium. Sporangium is borne inside a recurved,
affinity
redrawn from Gerrienne
(1996).
thickened spiny structure. E, F)
AMERICAN FERN JOURNAL: VOLUME NUMBER
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Another possible basal taxon, Gosferia curvata Gerrienne (1991, 1999), from
Devonian Belgium, unique having
the Early of in long, basipetally recurving
is
each terminated by reniform sporangium The
stalks, a (Fig. 3D). closest simi-
some
larity of this plant to unidentified zosterophyll-like plants in China
is
and and some The
Bathurst Island Silurian-Pragian rhyniophyte-like
to plants.
occurrence of a swelling near the sporangium base where attaches the
to
it
known
some Drepanophycus
stalk also of interest; similar swellings are in
is
and Edwards, and KauJanglophyton
species (Li 1995) in (Gensel, pers, obs.].
What unknown
any
represents in of these plants currently (but see below).
is
it
Ensivalia deblondii Gerrienne (1996a) from the Early Devonian of Belgium
has spiny, anisovalvate sporangia terminating stout The abaxial sporan-
stalks.
valve enlarged and which more smooth
gial spiny, inside of the
is delicate,
Odonax
adaxial valve rests (Fig. 3E). borealis Gerrienne (1996b), also from
New
Belgium, and some unnamed from Devonian
zosterophylls the Early of
Brunswick
also exhibit modification of the sporangium/stalk in the form of
enlargement of either stalk or distal sporangium valve and presence of emer-
which
gences, features perhaps help protect the sporangium.
Further evaluation of the variability of emergence types (see Gensel, 1992
and Kenrick and Crane, 1997 examples) among needed
for zosterophylls
as
is
well perhaps, homologies
as, clarification of the of different types of emer-
gences. For example, in Nothia aphylla (Lyon, 1964] El Saadawy and Lacey
(1979), the so-called emergences are produced by raised areas of axial tissue
and
(cortex epidermis), from expansion
resulting of existing with
cells, api-
cally located stomata (Kerp Are
et ah, 2001). these structures truly emergences
do
or they represent short, discontinuous ridges of the stem? The unusual
prismatic emergences of Serrulacaulis (Berry and Edwards, 1994) and those
now
known
to occur in Bothurstia (Kotyk and Basinger, 2000) also add
to
diversity of those structures but do not provide any homology
further of
tests
between
emergences and
microphylls.
Some
Early Devonian which
plants in sporangia arranged an obvious
are in
may
strobilus relate to the lycophyte clade, either among zosterophylls
or
ly-
copsids. Demersatheca, based on only a few leafless fertile specimens from the
Pragian of China,
exhibits reniform sporangia deeply sunken
into the axis
(Fig.
4D) and forming
tight strobili (Li and Edwards, 1996). Other plants with
stro-
include Distichophytum and
bili Bathurstia, both
attributed to the zostero-
and some un-named
phylls,
plants of uncertain from
affinity Bathurst Island.
This morphology
blurs the distinction between zosterophyll and barinophyte
some
to extent.
Barinophytes
are defined, according Kenrick and by
to Crane, very com-
a
unbranched
pact,
strobilus, indehiscent
sporangia,
intrasporangial heterospo-
and
sporangia borne on
ry, a horizontally extended which wraps around
axis
the stem
(their "clasping" sporangium
However,
orientation).
their relation-
Barinoph)^
More
mm
plants
GENSEL & BERRY: EARLY LYCOPHYTE EVOLUTION
81
D
may
Plants from the Pragian of China that be related to lycophytes. A) Adoketophyion
Fig.
4.
subverticillatum Li and Edwards with a leaf-like appendage subtending each sporangium. Re-
drawn from Li and Edwards (1992). B, C) Eophyllophyton helium Hao, in which lobed leaf-like
structures terminate lateral axes. Globose to reniform sporangia attach on the upper surface of the
lobes. Redrawn from Hao and Beck (1993). D. Demersatheca contiguo Li and Edwards, with spo-
rangia sunken in the axes. Redrawn from Li and Edwards (1996).
Protobarinophyton, Faironella valentula Gerrienne (1996a} also of
as is interest
between and
discussion a possible link zosterophylls barinophytes.
in this as
sporangia are attached to the inside of a curved appendage (Fig, 3F), and
Its
some
while affinities presently are uncertain, it thus bears resemblance to Bar-
inophytaceae.
Adoketopbyton, a genus described from the Pragian of China by Li and Ed-
with
wards (1992), demonstrates fertile regions leaf-like structures that bear
and
Crane Kenrick
sporangia in their axils (Fig. 4A]. (1997) suggest the leaf-
became
like structures might represent sterilized sporangia that modified as a
changes developmental processes such
"leaf" as a result of in as multiplication
and Another plant from the Pragian of China, Eophyllophyton
co-option. hel-
ium (Hao) Hao and Beck (1991) has the habit of a typical Early Devonian plant,
Whereas
but bears lobed, laminate leaf-like structures (Fig. 4B, 4C). this plant
the base of the euphyllophyte clade of Kenrick and Crane, largely because
is at
AMERICAN FERN JOURNAL: VOLUME NUMBER
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Fig. Line drawing of Drepanophycus qujingensis Li and Edwards. Note cauline sporangia not
5.
associated with leaves. Redrawn from Li and Edwards
(1995).
of centrarch
its protostele, its globose-reniform sporangia are located adaxially
on and
leaves tracheids possess G-type wall thickenings those present
its like
many
and
in zosterophylls
stem-lycophytes. In our opinion, this plant pos-
an odd
sesses suite of characters basal euphyllophytes and perhaps
for
is
it
more
appropriately considered
in the context of zosterophylls lycopsids.
or
Both Adoketophyton and
Eophyllophyton
thus provide idiosyncratic evidence
development
of the of laminate appendages, but information on
their
little
homologies.
Pre-Lycopsids
L
This term has been many
applied to plants with lycopsid characters, but
lacking the consistent association of sporangium with
a leaf or lacking fully
vascularized Genera
leaves. included Drepanophycus,
are Kaulangiophyton,
Asteroxylon, and some
in Baragwanathia
instances, another
interpretation,
(for
see Hueber, They form
1992). a sister clade to other lycopsids in Kenrick and
Crane's analysis and
are treated there as a stem-based group of Lycopsida, the
Drepanophycales. However, some
aspects of remain
their structure controver-
and may
re-evaluation
sial, of these features influence their position relative
to lycopsids or the interpretation of their evolutionary
significance.
Based on
current knowledge
Drepanophycus,
of the following appears
cer-
two
tain: species of Drepanophycus,
D. qujingensis and Edwards and
Li the
type
species D. spinaeformis
(Goeppert) Hotton and
Hueber, both
Li, exhibit
rhizomatous and
aerial axes covered with
vascularized microphyllous
leaves
and
cauline sporangia and Amona
[Fig. Li Edwards, 1995:
5; Li et al. 20001.
GENSEL & BERRY: EARLY LYCOPHYTE EVOLUTION
83
vegetative remains assigned Drepanophycus, morphology
to leaf varies con-
siderably, from long and falcate to short and thorn-like. has been suggested
It
that the axes with the former represent aerial regions, those with the
latter
rhizomatous axes. Sporangia borne on comparatively short stalks (usually
among
shorter than leaves) are interspersed the microphyllous with no
leaves,
apparent association with them.
Kaulangiophyon akantha
exhibits a similar growth habit to that of Drepan-
ophycus, but with all axes covered in stout, thorn-like emergences (Gensel et
underway
aL, 1969). Studies are to test assertions that Kaulangiopbyton very
is
similar to or congeneric with Drepanophycus (Kasper, 1972; Schweitzer and
Giesen, 1980), or that Kaulangiophyton has sporangia associated with leaves
new
(Hueber, 1992). Careful examination of original Maine collections and
New
from Brunswick shows no
material indication of vascularization in the
emergences. Sporangia were originally described as cauline, terminating a
moderately long stalk and extending beyond emergences (Gensel et aL, 1969).
Hueber noted
(1992) features of the sporangial stalk that led to his hypothesis
that a leaf extends beneath the sporangium but obscured by the sporangium
is
We
and thus not visible on impression remains. note that the stalks of some
is
pad
sporangia attach to a thickened or ring of coalified material that
itself is
borne on an axial protrusion. resembles the pad at the base of sporangia in
It
A
may
Stockmansella and Huvenia. similar thickening occur in Drepanophy-
cus qujingensis. However, in contrast to Hueber's ideas, no extra appendage,
emergence, or leaf lamina has been demonstrated in attachment to this thick-
ening in Kaulangiophyton. Additional information on these and other char-
acters of Kaulangiophyton and assessment of relationships will be presented
in a later paper.
Rooting Structures Early Lycophytes
in
Information about rooting structures, other than rhizoids, in basal lycophy-
being recorded the zosterophylls Zosterophyllum, Ba-
increasing, for
tes
is
and Hsua Drepano-
thurstia, Crenaticaulis (Gensel et ah, 2001), (Li, 1992), for
phycus and Edwards, Gensel and
(Rayner, 1984; Li 1995; et ah, 2001) for the
rhyniacean Stockmansella [Taeniocrada] langii Fairon-Demaret (1985) by
Two
Schweitzer (1980). patterns are recognized by Gensel et aL (2001) and
may correlate with habit. The pattern occurs in tufted forms, such as some
first
downward
Zosterophyllum species, which produce trending axes from a cen-
Upward
appear trending axes departing from the
region that root-like.
tral
smooth
same point are interpreted as shoots. In the other pattern, slender axes
and some
depart from the rhizomatous regions, in cases divide to varying de-
bedding
These frequently across, not on, the plane. Also, they are
grees. lie
sometimes produced during the formation of K-branches as in Bathurstia and
Drepanophycus (Gensel aL, 2001). In these plants, an axis departs, then
et
One axes oriented towards the rhizome apex and
forks. of the resultant is
and emergences
appears identical to shoots the other, lacking either or leaves
and directed away from the apex, appears root-like (Figs. 6A, 6B). Based on