American Journal of Botany 89(3): 506–517. 2002.

PHYLOGENETIC RELATIONSHIPS IN SELAGINELLACEAE

BASED ON RBCL SEQUENCES1

PETRA KORALL2,4 AND PAUL KENRICK3

2
Department of Botany, Stockholm University, SE-106 91 Stockholm, Sweden, and Molecular Systematics Laboratory,
Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden; and
3
Department of Palaeontology, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK

A phylogenetic framework is developed for the clubmoss family Selaginellaceae based on maximum parsimony analyses of molecular
data. The chloroplast gene rbcL was sequenced for 62 species, which represent nearly 10% of living species diversity in the family.
Taxa were chosen to reflect morphological, geographical, and ecological diversity. The analyses provide support for monophyly of
subgenera Selaginella and Tetragonostachys. Stachygynandrum and Heterostachys are polyphyletic. Monophyly of Ericetorum is
uncertain. Results also indicate a large number of new groupings not previously recognized on morphological grounds. Some of these
new groups seem to have corresponding morphological synapomorphies, such as the presence of rhizophores (distinctive root-like
structures), aspects of rhizophore development, and leaf and stem morphology. Others share distinctive ecological traits (e.g., xero-
phytism). For many groups, however, no morphological, ecological, or physiological markers are known. This could reflect patchy
sampling and a lack of detailed knowledge about many species. Despite a lengthy fossil record dating from the Carboniferous Period,
cladogram topology indicates that most of the living tropical species are probably the products of more recent diversifications. Res-
urrection plants, extreme xerophytes characterized by aridity-driven inrolling of branches and rapid revival on rehydration, have evolved
at least three times in quite different clades.

Key words: lycopod; phylogeny; rbcL; resurrection plant; rubisco; Selaginellaceae; xerophyte.

Selaginellaceae Willk. are an ancient group of lycopods
comprising some 700 living species. Most are easily recog-
nizable by their delicate dichotomously branching stems that
bear ranks of minute leaves in two distinct sizes (Jermy, 1990).
In these characteristics, the morphology of Selaginellaceae has
changed little since the group was first encountered in the fos-
sil record in the tropical wetland floras of the Carboniferous
Period (Thomas, 1992, 1997). Selaginellaceae are a cosmo-
politan family with species capable of growing under a wide
range of climate, soil, and light regimes. The group contains
frost-tolerant, arctic-alpine species, delicate terrestrial rainfo-
rest species, and physiologically robust, drought-adapted xe-
rophytes of desert scrub and heathland. Greatest diversity oc-
curs in primary tropical rainforest, and it is conceivable that
some elements of the group might have persisted in similar
environments since the Late Paleozoic. Recently, we devel-
oped an outline phylogeny for living Selaginellaceae based on
rbcL gene sequences (Korall, Kenrick, and Therrien, 1999).
Here, we build on this previous molecular work to develop a
more detailed phylogenetic framework for the family.
Previous systematic studies divided Selaginellaceae into nu-
merous groups (Spring, 1850; Braun, 1857; Baker, 1883; Hi-
eronymus, 1901; Walton and Alston, 1938; Jermy, 1986; So-
ják, 1992), and we follow the classification of Jermy (1986).
Jermy recognized one genus (Selaginella Pal. Beauv.) con-
taining five subgenera: Selaginella (2 species), Ericetorum Jer-
1
Manuscript received 3 May 2001; revision accepted 11 October 2001.
The authors thank S. Stefanovic (University of Washington, Seattle) for
providing some important DNA extracts for this analysis, J. Therrien (Uni-
versity of Kansas, Lawrence) for providing an rbcL sequence, the many other
people who have contributed material to this study, and Catarina Rydin and
Torsten Eriksson for comments on the manuscript. This work was financially
supported by the Swedish Natural Science Research Council (NFR research
grants to Paul Kenrick: B-AA/BU 10728-301, and to Paul Kenrick and PO
Karis: B 1393/1999), and Helge Ax:son Johnsons Stiftelse (grant to Petra
Korall).
4
Author for reprint requests (e-mail: petra.korall@botan.su.se).
my (3 species), Tetragonostachys Jermy (;50 species), Stach-
ygynandrum (Pal. Beauv.) Baker (;600 species), and Heter-
ostachys Baker (;60 species). Our preliminary molecular phy-
logeny based on a representative sample of 18 species revealed
that Selaginellaceae constitutes a monophyletic group and that
the morphologically distinctive subgenus Selaginella is sister
group to a clade comprising all other species (Korall, Kenrick,
and Therrien, 1999). In addition, the large subgenus Stachy-
gynandrum was shown to be polyphyletic with some members
paraphyletic to Tetragonostachys, Ericetorum, and Heteros-
tachys. Tetragonostachys and Ericetorum are monophyletic,
but monophyly of Heterostachys was untested.
Here we extend our phylogenetic data set of rbcL gene se-
quences from 18 to 62 species. Our sample includes a broad
and representative selection of diversity, adding up to almost
10% of living species. In particular, we have focused on im-
proving our sample of Stachygynandrum, choosing species
from all continents and a wide range of environments. Taxon
choice has been tailored to investigate the relationships of xe-
rophytic species, and we have included four resurrection plants
as well as other drought-tolerant forms. Taxa have also been
chosen to reflect the morphological diversity within the group,
focusing on those features that have been used by previous
authors to define groups. In addition to characters of leaf,
branch, and root, we have paid particular attention to stele
morphology, sporangial arrangement, and megaspore wall
structure. We have been careful to select characteristics that
are observable in fossils, with the long-term aim of calibrating
our phylogenetic tree.
MATERIALS AND METHODS
Nomenclature—Taxonomy and nomenclature at the species level follow
Alston, Jermy, and Rankin (1981) and Stefanovic, Rakotondrainibe, and Badré
(1997) where applicable; otherwise Reed (1965–1966) is followed.
Choice of species—Ingroup—Choice of ingroup was based on previous
taxonomic work (Baker, 1883; Hieronymus, 1901; Walton and Alston, 1938;

506
March 2002] KORALL AND KENRICK—PHYLOGENY
Jermy, 1986), comparative morphology (emphasizing growth form, sporangial
arrangement, and leaf, stele, and megaspore morphology), geographical dis-
tribution, and chromosome number. A total of 62 species were chosen and 44
of the sequences analysed here were not previously published (Table 1). Spe-
cies recognition in Selaginellaceae is difficult and much effort was devoted
to accurate identification. Where necessary and whenever possible, specimens
were compared to type material, as indicated in Table 1. Most information on
sporangial arrangement (Horner and Arnott, 1963; Fraile and Riba, 1981;
Quansah, 1988), chromosome numbers (Manton, 1950; Tchermak-Woes and
Dolezal-Janish, 1959; Kuriachan, 1963; Jermy, Jones, and Colden, 1967; Löve
and Löve, 1976; Takamiya, 1993), and some data on stele arrangement (Hi-
eronymus, 1901; Mickel and Hellwig, 1969; Jermy, 1990) were taken from
the literature. Because species determination in Selaginellaceae is difficult and
herbarium and cultivated specimens often are labelled incorrectly, data culled
from the literature should be used with caution. Sporangial arrangement, rhi-
zophore development, and stele form have, as far as possible, been verified
through studies of herbarium material.
Isophyllous species were represented by the two species in subg. Selagi-
nella (S. selaginoides, S. deflexa), the three Ericetorum species (S. gracillima,
S. uliginosa, S. pygmaea), and four species of the drought-adapted Tetrago-
nostachys group (S. arizonica, S. rupestris, S. rupincola, S. sellowii).
Fifty-three anisophyllous species were chosen from Stachygynandrum (in-
cluding ten members of the series Articulatae Spring) and Heterostachys. All
growth forms (e.g., creeping, erect, twining, rosettes) and a wide range of
geographical distributions are covered (Table 1). Monostelic, bistelic, and po-
lystelic species were included (Table 1). The steles of bistelic forms are pre-
dominantly terete, whereas those of monostelic forms are elliptical to strap-
shaped. Selaginella exaltata has a unique ‘‘actino-plectostele’’ (Mickel and
Hellwig, 1969). Selaginella novae-hollandiae is quite variable in general mor-
phology and widespread in Central and South America (Alston, Jermy, and
Rankin, 1981), and we suspect that it may represent a group of closely related
species. Two morphotypes were included, one from Venezuela and one from
Ecuador. Similarly, S. pallescens has two different growth forms, rosette (a
so-called resurrection plant) and erect, and both forms were included in the
analysis.
In addition to the ten articulate species, five possibly closely related non-
articulate species were chosen (S. australiensis, S. lyalli, S. myosurus, S. po-
lymorpha, and S. sinensis). These possess at least one of the characteristics
of articulate species (i.e., single, rarely few, basal megasporangium subtended
by sterile sporophylls). Chromosome numbers are known for 24 of the species
chosen for the analysis (Table 1), x 5 8, 9, and 10 were represented, as well
as 2n 5 50–60 (S. martensii).
Outgroup—Two species of Isoetaceae, Isoetes melanopoda and I. lacustris,
were included as outgroups. The sister-group relationship between Selaginel-
laceae and Isoetaceae has been confirmed in several studies, both morpholog-
ical (Kenrick and Crane, 1997) and molecular (Kranz and Huss, 1996; Wiks-
tröm and Kenrick, 1997; Korall, Kenrick, and Therrien, 1999).
DNA extraction, amplification, and sequencing—Total DNA was extracted
from 34 specimens using the DNeasy Plant Mini Kit from Qiagen (Santa
Clarita, California, USA). Total DNA from nine species, mainly Madagascan,
was most kindly provided by S. Stefanovic (Department of Botany, University
of Washington, Seattle, Washington, USA). The rbcL sequence of the rosette
form of S. pallescens was kindly donated by James Therrien (Department of
Botany, University of Kansas, Lawrence, Kansas, USA). DNA extracts were
made from fresh material, from specimens dried in silica gel, or from her-
barium specimens. The species included in the analysis and references to
sequences taken from the literature are given in Table 1. Fragments corre-
sponding to bases 18–1383 of the rbcL gene of Marchantia polymorpha
(Ohyama et al., 1986) were amplified using the polymerase chain reaction
(PCR) and two primers (rbcL 1F corresponding to bases 1–17 and rbcL 1409R
corresponding to bases 1384–1409) (for primer sequences see Korall, Ken-
rick, and Therrien, 1999). Polymerase chain reaction was performed in 25-
mL aliquots using Ready-To-Go PCR beads from Amersham Pharmacia Bio-
tech (Uppsala, Sweden). The reactions were run in a Perkin-Elmer Thermal
OF SELAGINELLACEAE 507
Cycler with one cycle of 958C for 5 min and 30 cycles of 948C for 30 sec,
508C for 30 sec, and 728C for 2 min. A second amplification, using product
from the first PCR as template was occasionally necessary to obtain sufficient
DNA for sequencing. Two different amplification strategies were used: high
amounts of DNA template (15 mL) and only 15 PCR cycles, or nested PCR,
where one internal primer was used in combination with one of the amplifi-
cation primers. Nested PCR was the most successful method, and allowed us
to obtain sequences from poor-quality or old material, such as S. pilifera
collected in 1907. The Thermo Sequenase Fluorescent Sequencing Kit from
Amersham Pharmacia Biotech (Uppsala, Sweden) was used to sequence dou-
ble-stranded PCR products for the rbcL gene. Samples were electrophoresed
on 6% Pharmacia Long Ranger acrylamide gels on an Amersham Pharmacia
Biotech (Uppsala, Sweden) automated ‘‘ALF-express’’ sequencer. All species
were sequenced in both directions using six different primers (Korall, Kenrick,
and Therrien, 1999). Sequences were assembled and edited using the Staden
Package (Staden, 1996). All sequences are deposited in EMBL.
A smaller partial PCR product was obtained for four species (S. willdenovii,
S. myosurus, S. plana, and S. helvetica). In these cases an internal primer was
used in combination with one of the amplification primers. The length of the
resulting sequences varied between 677 and 985 base pairs.
Phylogenetic analysis—Visual alignment of the rbcL sequences was un-
problematic because of the absence of insertions and deletions. The data ma-
trix contained 1299 characters corresponding to bases 83–1382 of the rbcL
gene of Marchantia polymorpha (Ohyama et al., 1986). Parsimony analyses
of the data were performed using PAUP* 4.0 (Swofford, 2000). Analyses
used the heuristic search option and the settings were random-sequence ad-
dition with 500 replicates, tree bisection-reconnection (TBR) branch swap-
ping, collapse of zero length branches, and MULTREES on. An equal weight-
ing scheme was employed with no transition-transversion bias (Albert and
Mishler, 1992). In all analyses, trees were rooted using both Isoetes species.
Support for individual clades was assessed using the decay index (Bremer,
1988; Donoghue et al., 1992) and bootstrap values (Felsenstein, 1985). Decay
indices were calculated using AutoDecay 4.0.2 (Eriksson, 1999) and PAUP*
4.0 (Swofford, 2000). PAUP* 4.0 settings used during decay analyses to find
the tree length of constrained trees were: heuristic search with 200 replicates
of random addition sequence, TBR branch swapping, collapse of zero length
branches, random sequence addition with one replicate, and MULTREES off.
Bootstrap values were calculated using PAUP* 4.0 by performing 30 000 rep-
licates with the following options selected: heuristic search, TBR branch
swapping, collapse of zero length branches, random sequence addition with
one replicate, and MULTREES off.
RESULTS
Of 1299 characters, 566 were phylogenetically informative
for parsimony. An heuristic search yielded 1355 equally most
parsimonious trees of 2403 steps, consistency index (CI) 5
0.375, retention index (RI) 5 0.758, uninformative characters
excluded. The strict consensus tree is shown in Fig. 1. Clades
are referred to throughout the text by the outermost (top and
bottom) species of the clade as they are found in Figs. 1 and
2. Note that the circumscriptions are dependent on how the
tree is drawn and are only relevant when compared to Figs. 1
and 2.
Results are consistent with monophyly of Selaginellaceae
(Fig. 1). Within this clade, subg. Selaginella is monophyletic
(decay index 54; bootstrap 100%) and sister group to a poorly
supported clade comprising all other species, which we term
the ‘‘rhizophoric clade’’ (decay index 2; bootstrap ,50%).
The rhizophoric clade (Fig. 1) is divided into two subclades,
here termed clades A (S. sellowii/S. australiensis) and B (S.
tamariscina/S. denticulata). Clade A contains both isophyllous
and anisophyllous species and has low support (decay index
2; bootstrap ,50%). Several of the basal nodes within clade
TABLE 1. Taxa included in analysis, with references to previously published sequences, and notes on distribution, stele arrangement, and chromosome number. 508
Taxa Chromosome
(!) 5 compared to type material Subgenus/series Geographical distribution Stele arrangementa numbera

Ingroup (Selaginella)
S. acanthostachys Baker ! Stachygynandrum S. America polystelic unknown
S. alopecuroides Baker ! Stachygynandrum Borneo monostelic, elliptical unknown
S. apoda (L.) Fern.b Stachygynandrum N. America monostelic, elliptical 2n 5 18
S. arizonica Maxonb Tetragonostachys N. America monostelic, terete unknown
S. articulata (Kunze) Spring Stachygynandrum/Articulatae S. & C. America polystelic unknown
S. australiensis Baker ! Stachygynandrum Australia monostelic unknown
S. bombycina Spring !b Stachygynandrum S. & C. America monostelic unknown
S. brooksii Hieron. Stachygynandrum Bomeo monostelic, elliptical 2n 5 18
S. deflexa Brackenridgeb Selaginella Hawaii unknown unknown
S. denticulata (L.) Springb Stachygynandrum Mediterranean monostelic, elliptical 2n 5 18
S. diffusa (C. Presl) Springb Stachygynandrum/Articulatae S. & C. America bistelic, terete unknown
S. digitata Spring Stachygynandrum Madagascar monostelic unknown
S. erythropus (Mart.) Spring ! Stachygynandrum S. America monostelic, elliptical 2n 5 20
S. exaltata (Kunze) Springb Stachygynandrum/Articulatae S. & C. America actino-plectostele unknown
S. firmuloides Warb. Stachygynandrum New Caledonia monostelic, elliptical unknown
S. flabellata (L.) Spring Stachygynandrum Grenada (Lesser Antilles) monostelic 2n 5 20
S. flagellata Spring Heterostachys Mexico to S. America monostelic unknown
S. fragilis A. Braun Stachygynandrum/Articulatae S. America monostelic unknown
S. frondosa Warb. Stachygynandrum SE Asia monostelic, elliptical unknown
S. gracillima (Kunze) Springb Ericetorum Australia, Tasmania solenostele unknown
S. haematodes (Kunze) Springb Stachygynandrum S. & C. America monostelic 2n 5 20
S. helioclada Alston ex Alston Stachygynandrum Madagascar unknown unknown
S. helvetica (L) Spring Stachygynandrum E. Europe & N. Asia monostelic 2n 5 18
S. imbricata (Forssk.) Spring Stachygynandrum E. Africa & Arabia monostelic unknown
AMERICAN JOURNAL

S. kerstingii Hieron. ! Stachygynandrum New Guinea monostelic, terete 2n 5 16

OF

S. kraussiana (Kunze) A. Braunb Stachygynandrum/Articulatae S. & E. Africa and widely introduced bistelic, terete 2n 5 20
S. lepidophylla (Hook. & Grev.) Springb Stachygynandrum S. USA, C. America monostelic unknown
S. lingulata Spring ! Stachygynandrum/Articulatae S. & C. America bistelic unknown
S. longiaristata Hieron. Stachygynandrum SE Asia monostelic, elliptical unknown
S. longipinna Warb. Stachygynandrum Australia monostelic, elliptical unknown
BOTANY

S. lyallii (Hook. & Grev.) Spring Stachygynandrum Madagascar polystelic 2n 5 18

S. martensii Spring Stachygynandrum Mexico & C. America monostelic, elliptical 2n 5 50–60
S. moellendorffii Hieron.b Stachygynandrum SE Asia monostelic 2n 5 20
S. moratii Rauh & W. Hagemann Stachygynandrum Madagascar unknown unknown
S. moritziana Spring ex Klotzsch !b Heterostachys S. America monostelic unknown
S. myosurus (Sw.) Alston Stachygynandrum W. tropical Africa monostelic 2n 5 18–20
S. novae-hollandiae (Sw.) Springc Heterostachys S. & C. America monostelic, terete unknown
S. novae-hollandiae (Sw.) Springd Heterostachys S. & C. America monostelic, terete unknown
S. pallescens (C. Presl) Springe Stachygynandrum S. & C. America monostelic, elliptical 2n 5 20, 22
S. pallescens (C. Presl) Springf Stachygynandrum S. & C. America monostelic, elliptical 2n 5 20, 22
S. pervillei Spring Stachygynandrum Madagascar monostelic unknown
S. pilifera A. Braun Stachygynandrum S. USA & N. Mexico monostelic 2n 5 20
S. plana (Desv.) Hieron. Stachygynandrum SE Asia, introduced in the New World polystelic 2n 5 20
S. polymorpha Badré Stachygynandrum Madagascar polystelic unknown
S. pulcherrima Liebm. ex E. Fourn. !b Stachygynandrum Mexico monostelic, elliptical 2n 5 20
S. pygmaea (Kaulf.) Alston Ericetorum South Africa, Australia solenostelic unknown
S. radiata (Aubl.) Spring Heterostachys S. America monostelic unknown
S. remotifolia Spring Stachygynandrum/Articulatae E. & SE Asia monostelic 2n 5 20
[Vol. 89
 March 2002]

TABLE 1. Continued.

Taxa Chromosome
(!) 5 compared to type material Subgenus/series Geographical distribution Stele arrangementa numbera

S. rupestris (L.) Springb Tetragonostachys N. America monostelic, terete 2n 5 18

S. rupincola Underw.b Tetragonostachys S. USA monostelic, elliptical unknown
S. selaginoides (L.) Linkb Selaginella Circumboreal monostelic, terete 2n 5 18
KORALL

S. sellowii Hieron. Tetragonostachys Cuba, Mexico, S. America monostelic unknown

S. sericea A. Braun Stachygynandrum/Articulatae S. America bistelic, terete unknown
AND

S. simplex Baker ! Heterostachys S. America unknown unknown

S. sinensis (Desv.) Spring Stachygynandrum China monostelic unknown
S. stauntoniana Spring ! Stachygynandrum E. Asia monostelic, elliptical unknown
S. suavis (Spring) Spring Stachygynandrum/Articulatae S. America bistelic, terete unknown
S. sulcata (Desv.) Spring Stachygynandrum/Articulatae S. America bistelic 2n 5 20
S. tamariscina (Beauvais) Spring Stachygynandrum E. Asia, northern parts of SE Asia monostelic, elliptical 2n 5 20
S. uliginosa (Labill.) Springb Ericetorum Australia, Tasmania solenostelic 2n 5 18
S. umbrosa Lemaire ex Hieron. Stachygynandrum S. America monostelic, elliptical 2n 5 20
S. willdenovii (Desv.) Baker Stachygynandrum SE Asia, introduced in New World tropics polystelic, elliptical 2n 5 18
Outgroup
Isoetes lacustris L.b Europe unknown 2n 5 110g
Isoetes melanopoda (Gay & Durieu) ex. Durieuh USA unknown 2n 5 22g
KENRICK—PHYLOGENY

a See text for references.

OF

b Previously published sequences: Korall, Kenrick, and Thierren (1999).

c Collected in Venezuela.
d Collected in Ecuador.
e Rosette form.
f Erect form.
g Musselman and Heafner (1997).
h Previously published sequences: Manhart (1994).
SELAGINELLACEAE
509
510 AMERICAN JOURNAL OF BOTANY [Vol. 89

Fig. 1. Strict consensus of 1355 equally most parsimonious trees, consistency index 5 0.375, retention index 5 0.758. Support values above branches
denote decay indices and below branches bootstrap values (a dash indicates a bootstrap value less than 50%). Branches with bootstrap values $80% are thicker.
Support values with arrows pointing to nodes denote values on these nodes when S. sinensis and S. australiensis are excluded from the analysis. All species
not labeled with subgenus (first column) are classified in subg. Stachygynandrum. Note that series Articulatae is found within Stachygynandrum. 1The rosette
form of S. pallescens. 2The erect form of S. pallescens. 3Specimen collected in Venezuela. 4Specimen collected in Ecuador.
March 2002] KORALL AND KENRICK—PHYLOGENY OF SELAGINELLACEAE 511

Fig. 2. Phylogram showing one of the most parsimonious trees. Taxa in boldface are isophyllous. Stele arrangement is shown as: one circle 5 monostelic;
two circles 5 bistelic; three ellipses 5 polystelic; * 5 actino-plectostele; ? 5 stele type unknown.
512 AMERICAN JOURNAL
A are also weakly supported, leaving three major well-sup-
ported groups: (1) the isophyllous subg. Tetragonostachys,
which is monophyletic with very strong support (decay index
44; bootstrap 100%); (2) a group of articulate species (all Ar-
ticulatae except S. exaltata) (decay index 12; bootstrap 96%);
and (3) a very strongly supported clade comprising the three
species in Ericetorum and three Madagascan species (S. lyallii,
S. moratii, and S. polymorpha) (decay index 21; bootstrap
100%). However, monophyly of Ericetorum is not supported.
Also of interest is the sister-group relationship between S. lep-
idophylla (resurrection plant) and the moss-like xerophytes in
Tetragonostachys, which has moderate support (decay index
4; bootstrap 70%). Other notable groupings in clade A include
species with rhizophores emerging from the upper surface of
branches, here termed the ‘‘dorsal rhizophoric clade.’’ This
group includes Articulatae, Tetragonostachys, and their re-
spective sister taxa: S. myosurus and S. lepidophylla (decay
index 2; bootstrap ,50%). Also, there is weak support for
monophyly of Articulatae (decay index 2; bootstrap ,50%).
Clade B comprises only anisophyllous species (decay index
3; bootstrap 76%), and it contains several well-supported sub-
clades (Fig. 1). There is strong support for a cosmopolitan
clade (Asia, North America, Africa/Madagascar) of drought-
adapted species (S. tamariscina/S. imbricata, decay index 43;
bootstrap 100%). This predominantly xerophytic group is sis-
ter to a clade containing all other species: S. apoda/S. denti-
culata. Some of the subsequent nodes are weakly or moder-
ately supported, leaving two strongly supported major nodes:
A clade of southeast Asian and Australian species, S. longi-
pinna/S. alopecuroides (decay index 4; bootstrap 97%), and a
clade of European, Madagascan, and Asian species, S. plana/
S. denticulata (decay index 17; bootstrap 100%). In addition,
a poorly supported clade of Central and South American hu-
mid tropical species is found, S. pallescens/S. novae-hollan-
diae (decay index 1; bootstrap ,50%). Species with dimorphic
sporophylls (Heterostachys sensu Jermy, 1986) form a poly-
phyletic assemblage. Neither the two geographic variants of S.
novae-hollandiae nor the two morphologically different forms
of S. pallescens were resolved as monophyletic.
DISCUSSION
Systematics—Despite its large size (700 species), only a
handful of taxonomic groups are widely recognized within Se-
laginellaceae. Of the groupings that have been established
based on morphological criteria, rbcL data corroborate the is-
ophyllous subg. Selaginella and Tetragonostachys. Likewise,
the anisophyllous series Articulatae (subg. Stachygynandrum),
excluding S. exaltata, has strong support. Monophyly of the
drought-adapted, mainly North American Tetragonostachys
has been supported previously by two molecular studies that
sampled most species of the group (based on rbcL and the
nuclear ribosomal internal transcribed spacer region [ITS];
Therrien, Haufler, and Korall, 1999; Therrien and Haufler,
2000). In previous systematic treatments, major divisions of
the family have often been based on one or more morpholog-
ical features, such as leaf dimorphism (isophylly/anisophylly),
phyllotaxy, and growth form. The rbcL data suggest that sev-
eral of these key characters have evolved iteratively, implying
that these groups are polyphyletic or paraphyletic. It should be
noted, however, that earlier classifications are in most cases
not phylogenetically based systems and were thus not neces-
sarily intended to reflect evolutionary relationships (exceptions
OF BOTANY [Vol. 89
include Soják, 1992). Of the groups recognized by Jermy
(1986), the rbcL tree indicates that Stachygynandrum and Het-
erostachys are polyphyletic. Whether Ericetorum is monophy-
letic or not cannot be deduced from this study. Of the groups
recognized by Soják (1992) the genera Selaginella (5 subg.
Selaginella of Jermy, 1986) and Bryodesma (5 subg. Tetra-
gonostachys of Jermy, 1986) are monophyletic, but the large
genus Lycopodioides Boehm (5 subgenera Ericetorum, Stach-
ygynandrum, and Heterostachys of Jermy, 1986) is paraphy-
letic to Bryodesma.
Perhaps the most surprising aspect of our analysis is the
large number of new and well-supported groupings not pre-
viously recognized on morphological grounds. These clades
range enormously in size from those containing perhaps a
handful of species to others with many hundreds. Examples
of these include S. remotifolia/S. fragilis, S. pygmaea/S. gra-
cillima, S. sinensis/S. australiensis, S. tamariscina/S. imbri-
cata, S. apoda/S. denticulata, S. longipinna/S. alopecuroides,
and S. plana/S. denticulata. One of these groupings shares the
distinctive ecological trait of being xerophytic (S. tamariscina/
S. imbricata), but the other clades do not appear to be sup-
ported by any obvious characters. This may reflect a poor un-
derstanding of the comparative morphology, ecology or phys-
iology of species in this large and diverse family. It may also
be an artifact of limited sampling because the rbcL data sample
;10% of living species diversity. There is certainly a need to
reevaluate these species groups from other perspectives. The
taxonomic status of various groups is discussed in more detail
below.
New groups—Our previous molecular analysis (Korall, Ken-
rick, and Therrien, 1999) identified a clade with a conspicuous
morphological marker, which we have called the rhizophoric
clade (Fig. 1). All species in this group bear a distinctive and
unique root-like structure termed the rhizophore (Fig. 3C and
F), which is lacking in the two species of subg. Selaginella.
Another morphological character supporting the rhizophoric
clade is the decussate arrangement of sporophylls. Bootstrap
support for this clade is very low. Within the rhizophore bear-
ing group, a basal dichotomy gives rise to two major clades:
clade A (poorly supported) with both isophyllous and aniso-
phyllous species and clade B (moderate support) with only
anisophyllous species (Fig. 1). The exclusion of two species
with exceptionally long branches (S. sinensis and S. austral-
iensis), strengthens support for these three clades (see below
‘‘branch lengths, pseudogenes, and morphotypes’’).
All species in the poorly supported dorsal rhizophoric clade
(Fig. 1) also possess a conspicuous and unique morphological
marker. Instead of developing from the lower surface of the
stems, the rhizophore develops from the upper surface (surface
bearing small leaves) and loops over the branch to grow down-
wards (Fig. 3C). This distinctive form of development is well
documented in Articulatae (e.g., S. kraussiana), but has not
been recognized previously as a synapomorphy of a larger
group. Dorsal rhizophores have been reported for two species
of Tetragonostachys (S. densa Rydb. in Webster and Steeves
[1963], S. wallacei Hieron. in Webster and Steeves [1964]),
and we have observed this developmental pattern in an addi-
tional ten out of ;50 species in this group. Observations of
herbarium and living material show that dorsal rhizophores
also occur in the resurrection plant S. lepidophylla and in S.
myosurus.
The well-supported S. remotifolia/S. fragilis clade contains
March 2002] KORALL AND KENRICK—PHYLOGENY OF SELAGINELLACEAE 513

Fig. 3. Morphology of Selaginella. (A–C) Selaginella arizonica (subg. Tetragonostachys). (A) Habit, note the incurling vegetative branch tips. (B) Close-
up of vegetative branch showing uniform spirally arranged leaves. (C) Close-up of branch dichotomy showing rhizophore originating on the dorsal side of the
branch. (D–F) Selaginella martensii (subg. Stachygynandrum). (D) Habit. (E) Close-up of upper side of vegetative branch showing dimorphic leaves, decussately
arranged in four rows. (F) Close-up of branch dichotomy showing rhizophore originating on the ventral side of the branch. Drawing by Pollyanna von Knorring.

all of the articulate species sampled, except S. exaltata. In
1850, Spring incorporated all species with articulations into a
widely recognized and predominantly South American group
called Articulatae (Braun, 1865; Hieronymus, 1901; Walton
and Alston, 1938). Articulations are small swellings of the
stem that occur below dichotomies. Somers (1978) listed sev-
eral additional morphological features found in this group.
Distinguishing features include (1) dorsal rhizophores, (2) a
single, basal megasporangium (rarely two) associated with
several enlarged sterile sporophylls, (3) large megaspores, and
(4) unique microsporangia. Monophyly of Articulatae is con-
sistent with the strict consensus tree (Fig. 1), but has very low
support. Although the articulations seem to be a synapomor-
phy of the group, many of the characteristics documented by
Somers (1978) have also been reported for nonarticulate spe-
cies (e.g., the dorsal rhizophores). It seems likely, therefore,
that a more detailed study of Articulatae and close relatives
will show that some of the putative characteristics of the group
are in fact synapomorphies of a series of more inclusive
clades.
The South American articulate species (S. sericea/S. fragil-
is) form a well-supported subclade that is sister to a clade
containing the only two Old World articulate species sampled
(i.e., S. kraussiana, S. remotifolia; Somers, 1978). These two
species are very similar in morphology and growth form and
have been considered geographic variants of a single species
514 AMERICAN JOURNAL
(S. kraussiana; Baker, 1884). Differences in stele and leaf
shape (P. Korall, personal observations; Hieronymus, 1901;
Somers, 1978) together with 91 base-pair differences in the
rbcL sequences support their treatment as distinct species.
Whereas S. remotifolia is strictly confined to the Old World
(parts of east and southeast Asia), the distribution of S. kraus-
siana spans both New World and Old World (parts of Africa,
South America). Alston, Jermy, and Rankin (1981) point out
that the general assumption is that S. kraussiana has been in-
troduced into South America by humans. In addition to S.
kraussiana there is at least one other Articulatae species in
Africa. Selaginella grallipes Alston differs markedly in gross
morphology from the creeping S. kraussiana and S. remotifolia
and more closely resembles the scandent South American S.
exaltata (Moran and Smith, 2001). Including S. grallipes in
the analysis might help elucidate the weakly supported rela-
tionships between basal Articulatae species and close relatives.
The strongly supported S. pygmaea/S. gracillima clade does
not possess any obvious unique morphological synapomor-
phies. Morphologically, the three Madagascan species (S. lyal-
lii, S. moratii, S. polymorpha) and Ericetorum (S. gracillima,
S. uliginosa, S. pygmaea) are quite dissimilar. Ericetorum con-
tains small, isophyllous plants that inhabit temperate heathland
in Australia and South Africa. Selaginella pygmaea and S.
gracillima are annuals. In contrast, S. lyallii, S. polymorpha,
and S. moratii are tall plants (up to 80 cm height; Stefanovic,
Rakotondrainibe, and Badré, 1997) with frondose branches in
the upper part, anisophyllous, and tropical. The rbcL sequenc-
es of the three Madagascan species differ in only one or two
base pairs, and although the species are very similar in mor-
phology, Stefanovic, Rakotondrainibe, and Badré (1997) con-
sider them to be different species.
The very large pantropical S. apoda/S. denticulata clade
contains almost half of the 62 species included in the analysis.
All have dimorphic leaves and are members of either Stach-
ygynandrum or Heterostachys. Most species are confined to
the humid tropics. One exception is the sister species to the
rest of the group, S. apoda, which grows in moist, temperate
environments in North America. It is likely that this clade
includes many unsampled species from the humid tropics of
southeast Asia and South America. The restricted geographic
distribution and the relatively small differences in branch
lengths (Fig. 2) among species within some subclades is con-
sistent with comparatively recent speciation events.
Morphological characters previously used as diagnostic
features in classifications—The presence or absence of leaves
of two distinctive sizes (leaf dimorphism or anisophylly) has
been used as a criterion for subdividing the family (see Spring,
1850; Baker, 1883; Hieronymus, 1901; Thomas and Quansah,
1991), but our study shows that isophylly has a complex evo-
lutionary history. Anisophylly is characteristic of the subgen-
era Heterostachys and Stachygynandrum (Fig. 3D–F), whereas
Tetragonostachys (Fig. 3A–C), Selaginella, and Ericetorum
are isophyllous (Fig. 2). Outgroup comparison with Isoetaceae
indicates that leaves of one size is the plesiomorphic state for
the family. The isophyllous states of Tetragonostachys and
Ericetorum are most parsimoniously interpreted as reversals,
but because most basal nodes have low support the possibility
that isophylly is a retained plesiomorphic state and that ani-
sophylly has originated several times cannot be ruled out.
OF BOTANY [Vol. 89
A resupinate strobilus, one that exhibits sporophyll dimor-
phism with the smaller sporophylls borne in the same plane
as the larger vegetative leaves, was used to characterize the
polyphyletic subg. Heterostachys. Five resupinate species were
included in the analysis (Fig. 1). Although they all appear in
clade B, the rbcL data indicate that the evolution of resupinate
strobili involved parallelisms and/or reversals. In a future
study, it would be interesting to include S. bemarahensis S.
Stefanovic and Rakotondrainibe and S. marinii S. Stefanovic
and Rakotondrainibe. These species have resupinate strobili,
but the rhizophores are dorsal (Stefanovic and Rakotondrain-
ibe, 1996), which implies a phylogenetic position closer to
Articulatae and Tetragonostachys.
Stele morphology has been used as a basis for recognizing
groups within Selaginellaceae (Hieronymus, 1901), and this
characteristic is documented for most species (Fig. 2, Table
1). It is clear from Fig. 2 that the bistelic condition has evolved
at least once among the articulate species and that the polys-
telic condition has arisen independently at least four times, in
S. lyallii and S. polymorpha, in S. articulata, in S. acanthos-
tachys and in S. willdenovii and S. plana. A solenostele is
reported as characteristic of Ericetorum (Jermy, 1986).
Several studies have shown that distinctive patterns of spo-
rangial arrangement exist in Selaginella (e.g., Horner and Ar-
nott, 1963; Fraile and Riba, 1981; Quansah, 1988). Major
trends that have been recognized include the organization of
sporangia into rows (two rows of microsporangia and two
rows of megasporangia) and the restriction of megasporangia
to a zone at the base of the strobilus. The only pattern that
seems always to be consistent within species is the presence
of a single (rarely two) basal megasporangium (Fraile and
Riba, 1981; Quansah, 1988). This arrangement has been used
as a feature unifying the articulate species (Somers, 1978), but
is also found in other taxa. This was recognized by Hierony-
mus (1901) who included sporangial arrangement as a diag-
nostic character in his classification by dividing the large sub-
genus Heterophyllum (corresponding to Stachygynandrum and
Heterostachys together) into Oligomacrosporangiatae (few
megasporangia per strobilus) and Pleiomacrosporangiatae
(many megasporangia per strobilus). Included in our analysis,
in addition to the articulate species, are S. myosurus, S. aus-
traliensis, S. lyallii, and S. polymorpha and S. sinensis. Our
results show that species with a single basal megasporangium
are all found in clade A, but that this characteristic does not
uniquely circumscribe a distinct clade.
Branch lengths, pseudogenes, and morphotypes—With
566 phylogenetically informative characters for 62 taxa, the
rbcL gene has a very high level of variation in Selaginellaceae,
and this is distributed unequally within the family (Fig. 2).
The branches in clade A are longer (more substitutions) than
those in clade B, and this phenomenon has the potential of
causing analytical problems. Long branches can cause spuri-
ous groupings (Felsenstein, 1978), but this is mainly a problem
when they are connected by short internodes. This pattern is
not seen in our tree (Fig. 2) in which internodes are of a
similar length to terminal branches for the most part. The
branches leading to S. sinensis and S. australiensis are excep-
tional even for Selaginellaceae and have led to unstable to-
pologies. Under some ingroup/outgroup combinations, these
two species have even grouped with seed plants in the Gne-
tales, also a group with an exceptionally long branch in rbcL
data sets. Because of this problem we acknowledge the pos-
March 2002] KORALL AND KENRICK—PHYLOGENY
sibility of spurious groupings, but we suspect that this is not
a major problem because many groupings within the tree are
comparatively stable and well supported, both in terms of
bootstrap support and decay index. Furthermore, if S. sinensis
and S. australiensis are excluded from the analyses, the same
topology is found and support for the basal nodes increases.
The support for the rhizophoric clade, clade A, and clade B,
rise from bootstrap values/decay indices of ,50%/2 to 94%/12,
,50%/2 to 85%/7, and ,50%/3 to 91%/4, respectively. In
view of the branch lengths, it is particularly important to test
the rbcL gene tree through the development of a parallel data
set based on additional genes.
Our laboratory data indicate the possible existence within
Selaginellaceae of a pseudogene that is shorter than the func-
tional rbcL gene. Double PCR products were amplified in six
of the included species (S. acanthostachys, S. arizonica, S.
novae-hollandiae [from Venezuela], S. remotifolia, S. rupin-
cola, S. sellowii), and multiple products were observed in one
species (S. plana). Pseudogenes of rbcL have previously been
found in both chlorophyllous and parasitic angiosperms and in
red algae (see Sennblad, Endress, and Bremer, 1998, and ref-
erences therein). Because no attempts to sequence the shorter
fragments have been made, we cannot exclude the possibility
that the fragments are amplifications of unrelated parts of the
genome.
The rbcL sequences revealed problems in the species delim-
itation of S. novae-hollandiae. Two morphotypes of S. novae-
hollandiae were included in the analysis. These specimens col-
lected from Venezuela and Ecuador were not resolved as a
monophyletic group (Fig. 1) and the rbcL sequences differ in
27 base pairs. Analyzing the data set with a constraint that
forced the two taxa together produced trees five steps longer
than the most parsimonious trees. These results are consistent
with the presence of more than one species in S. novae-hol-
landiae. Similarly, the rbcL data show that the rosette and
erect forms of S. pallescens differ in nine base pairs and that
they are closely related but not a monophyletic group (Fig. 1).
In this case, a constraint yields trees only two steps longer
than the most parsimonious trees. This might also constitute
grounds for considering the separation of rosette and erect
forms at the species level. Interspecific variation in the rbcL
gene of Selaginellaceae has not previously been examined, but
studies on ferns show that within-species variation is low: only
0–2 base-pair differences are commonly found between indi-
viduals considered to belong to the same species (Hauk, 1995;
Yatabe, Takamiya, and Murakami, 1998). Our results indicate
that species diversity may be underestimated in the family and
reflect the need of a thorough revision of the family at the
species level.
Origins of Selaginellaceae—The earliest fossil evidence of
Selaginellaceae comes from the tropical wetland floras of the
Carboniferous Period (Visean Epoch, 333–350 million years
ago [Ma]; Rowe, 1988). By the Late Carboniferous (290–323
Ma) branching stems that bore minute leaves of two distinct
sizes were widespread in coal measure floras (Thomas, 1992,
1997). These observations demonstrate that the characteristic
of leaf dimorphism appeared early on and that the family was
an important component of the humid tropical floras of the
Late Paleozoic. Selaginellaceae are predominantly forest-floor-
dwelling species, and the possession of leaves of two distinct
sizes is most probably an adaptation to poor light quality (Hé-
bant and Lee, 1984). The evolution of this characteristic broad-
OF SELAGINELLACEAE 515
ly coincides with earliest evidence for closed-canopy forest,
which was caused by the rise of tree ferns during the West-
phalian, some 303–320 Ma (DiMichele et al., 1992). The eco-
logical association between Selaginellaceae and coal measure
forests and the similarity of modern species to fossils raises
the possibility that some living tropical clades may be relicts
of these ancient Carboniferous groups (Korall, Kenrick, and
Therrien, 1999).
If elements of Selaginellaceae have persisted in tropical wet-
lands since the Carboniferous, we would expect to resolve spe-
cies from the humid tropics as a basal grade or clade within
the family, which would be paraphyletic or basal to xerophytic
and temperate clades. The results of our molecular analysis do
not, however, support this interpretation. Results document
two major clades of predominantly humid tropical species, the
S. pallescens/S. denticulata clade and a clade containing Ar-
ticulatae and its sister species, S. myosurus. The S. pallescens/
S. denticulata clade is further divided into strongly supported
Southeast Asian–Australian (S. longipinna/S. alopecuroides)
and weakly supported neotropical elements (S. pallescens/S.
novae-hollandiae). Several of the basal clades in Selaginella-
ceae are either temperate, xerophytic, or contain significant
proportions of species that fit these categories. Subgenus Se-
laginella contains the temperate/arctic alpine S. selaginoides.
In clade A, the S. pygmaea/S. australiensis clade is probably
temperate, and the Tetragonostachys plus S. lepidophylla clade
is xerophytic. Likewise, in clade B, the S. tamariscina/S. im-
bricata clade contains drought-adapted species, and the next
branch up is S. apoda, a temperate North American species.
These data show a comparatively derived position for both
major clades of humid tropical species. The cladogram topol-
ogy therefore indicates that species and species groups of the
modern humid tropics are unlikely to be relicts of Carbonif-
erous cladogenesis, but are probably of more recent origin.
How can this interpretation be reconciled with the early ap-
pearance of species with dimorphic leaves in the tropical wet-
lands of the Carboniferous Period? The relationships of the
early fossil species are currently very poorly understood. This
is mainly because many are compression fossils, and they do
not contain much information on anatomical or reproductive
structures. They are therefore relatively information poor. It is
possible that some of these early species would branch from
the stem group of the rhizophoric clade or perhaps even from
the Selaginellaceae stem group. In either case, these species
would not be expected to possess the distinctive rhizophore,
and in this context it is interesting to note that rhizophores
have not been observed in any Paleozoic fossils.
Multiple origins of resurrection plants—Although most
species diversity in Selaginellaceae occurs in primary tropical
rainforest, a substantial number of species are able to with-
stand seasonal drought or even live in very arid parts of the
world. The moss-like xerophytes (Fig. 3A–C) in Tetragonos-
tachys have been shown to be a monophyletic group (Korall,
Kenrick, and Therrien, 1999; Therrien, Haufler, and Korall,
1999; Therrien and Haufler, 2000). Physiologically, species in
this group are able to withstand prolonged desiccation, and
morphologically they exhibit adaptations to reducing water
loss by possessing small leaves with thick cuticles. In Stach-
ygynandrum, at least ten species have a rosette of branches
and during drought the branches curl inwards, forming a ball.
These are called ‘‘resurrection plants’’ and the name alludes
to their ability to revive rapidly by uncurling their branches to
516 AMERICAN JOURNAL
reform the rosette habit under more favorable moisture con-
ditions. We included four of these ten species in our analysis
in order to investigate their relationships to each other and to
Tetragonostachys. Results show that resurrection plants have
evolved at least three times in Selaginellaceae. The resurrec-
tion plant S. lepidophylla is sister to the moss-like xerophytes
of the Tetragonostachys clade. Selaginella lepidophylla also
has the distinctive rhizophore development that characterizes
the more inclusive dorsal rhizophoric clade. The resurrection
plants S. tamariscina (eastern Asia) and S. pilifera (southern
USA, Mexico) are found in a strongly supported clade with
other non-resurrection Asian (S. stauntoniana) and Madagas-
can species (S. digitata, S. helioclada, S. imbricata). All spe-
cies in this clade grow in seasonally dry areas. In contrast to
other xerophytes, the rosette form of the resurrection plant S.
pallescens is nested in a humid tropical clade. The rbcL data
therefore support diverse relationships for resurrection plants,
indicating that this response to arid conditions has evolved
iteratively in Selaginellaceae. Incurling of branches in a less
pronounced fashion is also found in other drought-adapted
species such as some species of Tetragonostachys (e.g., S. ar-
izonica; Tryon, 1955; see Fig. 3A–C), and the non-rosette-
forming species of the S. tamariscina/S. imbricata clade (S.
stauntoniana and S. imbricata; P. Korall, personal observa-
tions; S. digitata and S. helioclada; Stefanovic, Rakotondrain-
ibe, and Badré, 1997). There is evidence therefore in the mor-
phology of other species that the resurrection plants’ adapta-
tions to aridity may just be an extreme example of a more
general but less dramatic trend of branch incurling that is com-
mon in the family.
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