Botanical Journal of the Linnean Society, 2010, 163, 305–359. With 16 figures
Phylogenetics and classification of the pantropical fern
family Lindsaeaceae
SAMULI LEHTONEN1*, HANNA TUOMISTO1, GERMINAL ROUHAN2 and
MAARTEN J. M. CHRISTENHUSZ3
1
Department of Biology, University of Turku, FI-20014, Finland
Muséum national d’Histoire naturelle, UMR CNRS 7205 ‘Origine, Structure et Evolution de la
Biodiversité’, 16 rue Buffon CP39, F-75005 Paris, France
3
Department of Botany, The Natural History Museum, Cromwell Road, London SW7 5DB, UK
2
Received 19 February 2010; revised 3 May 2010; accepted for publication 2 June 2010
The classification and generic definition in the tropical–subtropical fern family Lindsaeaceae have been uncertain
and have so far been based on morphological characters only. We have now studied the evolutionary history of the
Lindsaeaceae by simultaneously optimizing 55 morphological characters, two plastid genes (rpoC1 and rps4) and
three non-coding plastid intergenic spacers (trnL-F, rps4-trnS and trnH-psbA). Our data set included all genera
associated with Lindsaeaceae, except Xyropteris, and c. 73% of the currently accepted species. The phylogenetic
relationships of the lindsaeoid ferns with two enigmatic genera that have recently been included in the Lindsaeaceae, Cystodium and Lonchitis, remain ambiguous. Within the monophyletic lindsaeoids, we found six wellsupported and diagnostic clades that can be recognized as genera: Sphenomeris, Odontosoria, Osmolindsaea,
Nesolindsaea, Tapeinidium and Lindsaea. Sphenomeris was shown to be monotypic; most taxa formerly placed in
that genus belong to the Odontosoria clade. Ormoloma is embedded within Lindsaea and therefore does not merit
recognition as a genus. Tapeinidium is sister to a clade with some species formerly placed in Lindsaea that are
morphologically distinct from that genus and are transferred to Osmolindsaea and Nesolindsaea, proposed here as
two new genera. We do not maintain the current subgeneric classification of Lindsaea itself, because neither of the
two generally accepted subgenera (Lindsaea and Odontoloma) is monophyletic, and most of the sections also appear
unnatural. Nesolindsaea shows an ancient biogeographical link between Sri Lanka and the Seychelles and many
of the main clades within Lindsaea have geographically disjunct distributions. © 2010 The Linnean Society of
London, Botanical Journal of the Linnean Society, 2010, 163, 305–359.
ADDITIONAL KEYWORDS: lindsaeoids – Nesolindsaea – Osmolindsaea – phylogeny – pteridophytes –
sensitivity analysis.
INTRODUCTION
The fern family Lindsaeaceae comprise c. 200 species
and are distributed widely in the tropics, with several
species extending into the subtropics in temperate
South America, East Asia and New Zealand (Kramer,
1957a). Early on, lindsaeoid ferns were considered a
part of Davalliaceae (Presl, 1836; Fée, 1852; Christensen, 1938) and were later placed in Dennstaedtiaceae (Holttum, 1947; Tryon & Tryon, 1982; Kramer
*Corresponding author. E-mail: samile@utu.fi
& Green, 1990). The name Lindsaeaceae was proposed by Pichi-Sermolli (1970).
Early molecular systematic studies placed Lindsaeaceae as sister to a clade uniting Dennstaedtiaceae
and Pteridaceae (Hasebe et al., 1994; Wolf, Soltis &
Soltis, 1994) and hence supported the recognition of
Lindsaeaceae as a separate family. The six traditionally recognized lindsaeoid genera are Lindsaea
Dryand. ex Sm. (c. 165 spp.), Odontosoria Fée (c. 12
spp.), Ormoloma Maxon (1 or 2 spp.), Sphenomeris
Maxon (c. 11 spp.), Tapeinidium (C.Presl) C.Chr. (c.
18 spp.) and Xyropteris K.U.Kramer (1 sp.). Results of
molecular studies have also led to the expansion of
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
305
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S. LEHTONEN ET AL.
Figure 1. Phylogenetic relationships within leptosporangiate ferns according to Schuettpelz et al. (2008).
the family to include two enigmatic genera. These are
Lonchitis L., which was earlier placed in Dennstaedtiaceae (e.g. Tryon & Tryon, 1982), and Cystodium
J.Sm., previously considered to belong to the tree fern
family Dicksoniaceae (Korall et al., 2006; Schuettpelz
& Pryer, 2007). However, a separate family Lonchitidaceae has also been proposed for the genus Lonchitis
on the basis of morphological differences with lindsaeoid ferns (Christenhusz, 2009).
In a recent synopsis of fern phylogenetics,
Schuettpelz & Pryer (2008) recognized Saccoloma
Kaulf. (the sole genus of Saccolomataceae) as the
sister lineage of Lindsaeaceae (Fig. 1). Earlier,
however, Saccoloma has been placed as sister
lineage to all other Polypodiales (Pryer et al., 2004;
Korall et al., 2006; Perrie & Brownsey, 2007).
Schneider et al. (2004) resolved Lonchitis as the
sister of other Polypodiales and Saccoloma as the
sister of Lindsaeaceae (which then excludes Lonchitis). Although the hypothesized phylogenetic relationships between these groups differ among
studies, there is a consensus that Lindsaeaceae are
one of the early-diverging lineages from the main
stock of polypod ferns. The Early Cretaceous fossil
remains with characteristic root anatomy (i.e. a
sclerenchymatous outer cortex combined with an
innermost cortical layer six cells wide) confirm a
minimum age of c. 99 My for the lindsaeoid ferns
(Schneider & Kenrick, 2001). Based on likelihood
analyses, Pryer et al. (2004) estimated that lindsaeoids diverged c. 133 Mya.
Generic delimitation on morphological grounds has
been difficult within Lindsaeaceae. The lack of
obvious morphological discontinuities led Tryon &
Tryon (1982) and Kramer & Green (1990) to consider
Sphenomeris congeneric with Odontosoria, but this
classification has been criticized (Barcelona, 2000)
and was not followed by Smith et al. (2006, 2008).
Tapeinidium moorei (Hook.) Hieron. has been especially difficult to place and it has been included in
Lindsaea, Odontosoria and Sphenomeris.
In general terms, Lindsaea is characterized by sori
that open towards the margin and have the indusium
attached to the disc (Dryander, 1797). Ormoloma is
characterized by the combination of simply pinnate
lamina and strictly uninerval sori and Odontosoria
and Sphenomeris by their cuneately–dichotomously
divided lamina with apical sori and large spores.
Tapeinidium has only a slight adaxial sulcation of the
axes and pinnate leaf architecture, with the sori on
lateral lobes, and Xyropteris differs in having continuous sori and basally auriculate pinnae. Lonchitis is
morphologically clearly different from the other
genera as it has sori in the sinus and succulent,
dorsiventral, hairy rhizomes. Saccoloma has stout
erect rhizomes and marginal cup-shaped sori,
whereas Cystodium in many respects resembles a
small tree fern, which explains its previous placement
in Dicksoniaceae.
The systematics of lindsaeoid genera has been
extensively studied by Kramer (1957a, b, 1967a, b,
c, 1970, 1971a, b, c, 1972a, b, 1988, 1989a, b, 1991;
Kramer & Tindale, 1976). Kramer subdivided the
largest genus, Lindsaea, into two subgenera based
on rhizome anatomy (Kramer, 1967b). Subgenus
Lindsaea included species with an essentially terrestrial, short to moderately long creeping rhizome
with radially symmetric steles, and subgenus Odontoloma included species that are usually epiphytic
and have long creeping rhizomes with strongly dorsiventral steles (Kramer, 1967b). The subgenera
were further divided into 17 sections in subgenus
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
PHYLOGENETICS OF LINDSAEACEAE
Lindsaea and six sections in subgenus Odontoloma
(Kramer, 1957a, 1967b, 1972a). However, Kramer
(1957a, 1967b, 1971a) clearly defined all these sections as paraphyletic entities, thus his classification
was never meant to be phylogenetic in the sense of
Hennig (1966).
Lindsaeoid ferns have been poorly sampled in previous molecular studies. For example, Pryer et al.
(2004) only included one lindsaeoid species and
Schuettpelz & Pryer (2007) five. Here, we present the
first comprehensive analysis of the phylogenetic relationships within Lindsaeaceae. Our analysis is based
on simultaneous optimization of morphological and
molecular evidence and it includes 165 of the 249
lindsaeoid taxa (species, subspecies and varieties)
recognized by Kramer (1957a, b, 1967a, b, c, 1970,
1971a, 1972a, b, 1988, 1989a, b, 1991) and Kramer &
Tindale (1976), with an additional five lindsaeoid taxa
not recognized by Kramer and five outgroup taxa. On
the basis of the results, we propose a new generic
classification for the family.
MATERIAL AND METHODS
TAXON
SAMPLING AND MORPHOLOGICAL DATA
For this study, we aimed to sample as many taxa of
Lindsaeaceae as possible. Our molecular sampling
includes large numbers of silica-dried material collected by us (mostly from the Neotropics) or provided
by colleagues (mostly from the Palaeotropics). In
addition, many taxa were sampled using existing
herbarium specimens deposited at AAU, BISH, BM,
CAY, L, MO, P, TUR, U, US and Z (herbarium acronyms according to Thiers, 2010). We successfully
sampled 195 specimens representing 175 taxa. All
eight genera placed in the family by Smith et al.
(2008) were included in our analyses, except the
monotypic Xyropteris, for which DNA amplification
failed. The sampling covered c. 71% of the generally
accepted taxa of Lindsaea (76% of the species), 50% of
the taxa of Tapeinidium (56% of the species), 56% of
the taxa in the Sphenomeris-Odontosoria group (74%
of the species), both Ormoloma spp. accepted by
Kramer (1957a), one of the two Lonchitis spp. and the
sole Cystodium sp. Overall, we obtained c. 69% taxon
sampling and 73% species sampling within the family
in the broad sense. In addition, two Saccoloma spp.
representing the closely related Saccolomataceae
were included.
The uncertainty concerning the closest relatives of
the lindsaeoid ferns may cause problems for the
rooting of the tree. Depending on the study, either
Saccoloma (Pryer et al., 2004; Korall et al., 2006;
Perrie & Brownsey, 2007), Lonchitis (Schneider et al.,
2004) or the Saccoloma–Lonchitis–Lindsaeaceae
307
(Schuettpelz & Pryer, 2007) clade is the sister lineage
of all other polypod ferns. The analysis by Schuettpelz
& Pryer (2007) was based on the largest number of
data (rbcL, atpB and atpA assembled for 400 leptosporangiate ferns) and therefore can be considered
the most reliable hypothesis presented to date. We
based our outgroup selection on this hypothesis and
rooted our tree with a dennstaedtioid polypod,
Pteridium pinetorum C.N.Page & R.R.Mill. (northern
bracken, Dennstaedtiaceae), a member of the
proposed sister lineage to the Lindsaeaceae–
Saccolomataceae clade.
We identified the sequenced specimens by comparing them with c. 4000 herbarium specimens. Whenever type material or digital type images were
available, they were used to verify the correct application of names. In other cases we named the specimens by following the specimen lists, keys and
descriptions provided in the numerous publications
of Kramer (e.g. Kramer, 1957a, 1967a, b, c, 1970,
1971a, b, c, 1972a, b, 1989a, 1991; Kramer & Tindale,
1976). Many of the sequenced specimens had been
identified to species and annotated by K. U. Kramer
himself, but even then we verified the consistency of
identifications.
We coded a total of 55 morphological characters for
the studied taxa (Appendices 1 and 2). The characters
were either novel or adapted from Pryer, Smith &
Skog (1995), Stevenson & Loconte (1996) or Barcelona
(2000). Spore characters were mostly coded according
to information given in the literature (Kramer, 1957a,
1967a, b, c, 1970, 1971a, b, 1972a, b, 1989a, 1991;
Kramer & Tindale, 1976; Kramer & Green, 1990), but
most of the other characters were coded by direct
observation of herbarium specimens. The collections
consulted for our study are held at AAU, BISH, BM,
CAY, K, KYO, L, MICH, MO, NSW, P, TUR, U, UC,
US and Z.
MOLECULAR
DATA: SELECTION OF THE
DNA
REGIONS
We obtained silica-dried material for 37 specimens
and used herbarium material to broaden the molecular sampling by another 158 specimens. Because DNA
fragmentation is a problem with herbarium material,
we had to focus on relatively short sequences (Lehtonen & Christenhusz, 2010). This precluded using
the conservative mitochondrial genome (Seberg &
Petersen, 2006) and many of the plastid markers
commonly used in fern systematics (e.g. atpA, atpB,
rbcL). The nuclear genome presents particular problems because of paralogous sequences and common
polyploidy among ferns (Schuettpelz et al., 2008). For
amplification and sequencing we therefore selected
the four relatively short plastid regions with varying
rates of evolution, trnL-trnF, trnH-psbA, rpoC1 and
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
308
S. LEHTONEN ET AL.
rps4 + rps4-trnS; the latter was further divided into
two fragments for the analysis (see below), thus
resulting in five DNA fragments in our analyses.
Furthermore, we coded observed inversion events (see
below) as binary characters in a separate data matrix
(Appendices 3 and 4).
trnL-trnF intergenic spacer
This spacer region was among the first non-coding
sequences used in plant systematics (Taberlet et al.,
1991) and it has become one of the most widely used
at lower taxonomic levels in fern systematics (Small
et al., 2005). The spacer region amplifies almost universally in ferns with standard primers and it provides a high number of variable sites (Small et al.,
2005). However, the region is typically short (c. 400 bp
in our case) and reconstructing its evolution is complicated by numerous structural changes, including
short inversions (Quandt & Stech, 2004; Kim & Lee,
2005; Lehtonen, Myllys & Huttunen, 2009).
rpoC1 gene
This gene was among the markers proposed and
assessed for the bar coding of land plants (Chase
et al., 2007; Hollingsworth et al., 2009), although it
was not finally selected (CBOL Plant Working Group,
2009). It amplifies well in many plant groups, but the
rate of evolution is not high (Chase et al., 2007). We
sequenced a c. 730-bp long part of rpoC1.
trnH-psbA intergenic spacer
This region is now widely used in lower-level plant
systematics, because of its high level of variation
among closely related species and ease of amplification (Shaw et al., 2005). It had therefore been suggested as a potential DNA bar code for land plants
(Chase et al., 2007). However, the region is typically
short (c. 430 bp in our case) and usually does not
provide sufficient information for phylogenetic reconstruction unless coupled with other regions (Shaw
et al., 2005). Like the trnL-trnF spacer, the trnH-psbA
spacer often contains many structural rearrangements, which complicates its use in phylogenetic
inference (Bain & Jansen, 2006; Storchová & Olson,
2007; Borsch & Quandt, 2009; Lehtonen et al., 2009).
rps4 gene
The rps4 gene (c. 580 bp) was amplified in this study,
together with the rps4-trnS intergenic spacer (c.
250 bp). For the phylogenetic analyses, the rps4 gene
was separated from the spacer region and the gene
and the spacer region were submitted for the analyses
as separate fragments. This gene is often used in fern
systematics, but because of its low substitution rate it
is more useful at deeper phylogenetic levels (Small
et al., 2005).
rps4-trnS intergenic spacer
The rps4-trnS spacer is the shortest of the fragments
used in this study (c. 275 bp) and it has a relatively
low substitution rate in comparison with many other
non-coding plastid DNA regions (Shaw et al., 2005;
Small et al., 2005). Nevertheless, the spacer is widely
used in fern systematics (Small et al., 2005, and references therein).
MOLECULAR
DATA: LABORATORY PROCEDURES
Total genomic DNA was extracted by using DNeasy
Plant Mini Kit (Qiagen, Valencia, CA, USA) or
E.Z.N.A. SP Plant DNA Kit (Omega Bio-tek,
Doraville, GA, USA). For silica-dried material, the
manufacturer’s extraction protocols were followed,
but for herbarium specimens a modified protocol
(30 min incubation, 450 mL of cell lysis buffer, 50 mL of
elution buffer, 10 min elution) as described by Drábková, Kirschner & Vlcek (2002) was used. Primers
used for amplification and sequencing are listed in
Table 1.
DNA fragments were amplified using PureTaq RTG
PCR beads (Amersham Biosciences, Piscataway, NJ,
USA). Each reaction contained 5 mL of DNA template,
Table 1. Primers used for PCR and sequencing
Locus
5′–3′
Reference
trnL-trnF
e: GGTTCAAGTCCCTCTATCCC
f: ATTTGAACTGGTGACACGAG
Taberlet et al., 1991
Taberlet et al., 1991
trnH-psbA
trnH: CGCGCATGGTGGATTCACAATCC
psbA3′f: GTTATGCATGAACGTAATGCT C
Tate & Simpson, 2003
Sang, Crawford & Stuessy, 1997
rpoC1
LP1: TATGAAACCAGAATGGATGG
LP5: CAAGAAGCATATCTTGASTYGG
Chase et al., 2007
Chase et al., 2007
rps4-trnS
rps4.5′: ATGTCSCGTTAYCGAGGACCT
trnSGGA: TTACCGAGGGTTCGAATCCCT C
Small et al., 2005
Shaw et al., 2005
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
PHYLOGENETICS OF LINDSAEACEAE
1 mL of each primer and 18 mL of double distilled
water (ddH2O). The PCRs were carried out in a
GeneAmp PCR System 9700. The amplification profiles were: initial denaturation (95 °C, 2 min) followed
by 35 cycles of amplification, hybridization and extension (95 °C, 1 min; 57 °C, 1 min; 72 °C, 1 min), and
7 min of final extension at 72 °C for rps4-trnS, initial
denaturation (95 °C, 2 min) followed by 35 cycles of
amplification, hybridization and extension (95 °C,
1 min; 52 °C, 1 min; 72 °C, 1 min), and 7 min of final
extension at 72 °C for trnL-trnF, initial denaturation
(94 °C, 1 min) followed by 40 cycles of amplification
and extension (94 °C, 30 s; 48 °C, 40 s; 72 °C, 40 s),
and 5 min of final extension at 72 °C for trnH-psbA
and rpoC1.
PCR products were purified and sequenced in both
directions under BigDye™ terminator cycling conditions by Macrogen Inc. (Seoul, South Korea; http://
www.macrogen.com). Sequences were assembled and
incorrect bases corrected using 4Peaks (A. Griekspoor
& T. Groothuis, http://mekentosj.com). The corrected
sequences were initially aligned with ClustalX
version 1.83.1 (Thompson et al., 1997) by using
default alignment parameters. Putative inversions
were identified by eye from the aligned sequence
matrix. Before submitting the data to final POY
analyses (see below), all the gaps inserted by ClustalX
were removed. GenBank accession numbers and
voucher specimen information are given in Table 2.
Most of the sequences were newly generated, but
some were taken from Lehtonen & Tuomisto (2007)
and Lehtonen et al. (2009).
CONCEPT
OF HOMOLOGY, DATA OPTIMIZATION AND
THE ROLE OF TOTAL EVIDENCE
Characters are homologous when they share a common
ancestry and then they tell us about phylogenetic
history (Patterson, 1982). Therefore, homology statements and phylogenetic history are inseparable problems (Patterson, 1982; Löytynoja & Goldman, 2009).
Homology should be assumed unless there is evidence
against it, because otherwise building phylogenetic
hypotheses becomes impossible (Hennig, 1966) and the
evidence for refuting homology statements can only
come from the character congruence test in phylogenetic analysis (Farris, 1983). From this, it follows that
a phylogeneticist’s task is to maximize homology statements in the observed character data (e.g. De Laet,
2005; Phillips, 2006). Multiple sequence alignment is
traditionally used to establish primary homology
statements among sequence positions on the basis of
phenetic similarity, and subsequent phylogenetic
analysis is used to determine which of the primary
homologies are considered real (‘secondary’) homologies (de Pinna, 1991). Although improved computing
309
capacity has made this two-step approach unnecessary
(e.g. Lehtonen, 2008; Liu et al., 2008; Wheeler &
Giribet, 2009), many authors still favour it (e.g.
Simmons, 2004; Kjer, Gillespie & Ober, 2007; Ogden &
Rosenberg, 2007).
Direct optimization (DO) provides a means to determine homology correspondences and search for the
optimal tree simultaneously. The homology correspondences are then viewed as the results of an analysis
and the obtained topology maximizes the homology
correspondences in the available data (Wheeler,
1996). This requires that all the relevant data are
optimized together in a total-evidence character congruence test (Kluge, 1989; Phillips, 2006; Fitzhugh,
2006a). Consequently, if morphological characters are
included in the analysis, they will affect the determination of homology correspondences in the molecular
data (‘sequence alignment’), just as DNA characters
may direct the optimization of morphological
character-state transformations (Phillips, 2006;
Agolin & D’Haese, 2009).
We chose to use parsimony as the optimality criterion when selecting the preferred tree and homology
correspondences (Farris, 1983). When no common
model of evolution is assumed, maximum likelihood
gives the same results (Tuffley & Steel, 1997; Steel &
Penny, 2000), but requires parameterization of
branch lengths in addition to topology (Goloboff,
2003). Our data include a large number of heterogeneously evolving characters (structural changes, e.g.
minute inversions and repeats in non-coding
sequences, morphological characters) for which realistic evolutionary models are not available (Borsch &
Quandt, 2009). Lehtonen et al. (2009) demonstrated
that parsimony outperformed maximum likelihood
and Bayesian methods in inferring phylogenies from
sequences containing small-scale structural rearrangements. We also prefer parsimony over Bayesian
approaches because of the impossibility of flat priors
(Steel & Pickett, 2006), the need to specify probability
distributions for all parameters (Moyle et al., 2009)
and the peculiar behaviour of Bayesian inference in
the presence of missing data (Goloboff & Pol, 2005).
We performed simultaneous analysis of all available evidence (total evidence; Kluge, 1989) instead of
running partitioned analyses for different DNA fragments. Data partitioning can only be justified if the
partitions are independent of each other (Fitzhugh,
2006a, 2006b), which is not the case with DNA
sequences derived from the same plastid genome.
Combined data partitions have been found to have
higher nodal stability than separate partitions, indicating that the sequence alignment problem is less
serious in the combined analysis (Aagesen, 2005). We
did perform separate analyses for the different loci to
inspect them visually for incongruence that might
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
310
S. LEHTONEN ET AL.
Table 2. List of taxa used in this study with GenBank accession numbers and voucher information
Taxon
Voucher
trnL-trnF
trnH-psbA
rpoC1
rps4
rps4-trnS
Cystodium sorbifolium (Sm.)
J.Sm.
Lindsaea agatii (Brack.)
Lehtonen & Tuomisto
Lindsaea annamensis
K.U.Kramer
Lindsaea apoensis Copel. in
Perkins
Lindsaea arcuata Kunze
Lindsaea austrosinica Ching
Brass 23810 (BM)
GU478726
n.a.
n.a.
n.a.
n.a.
Braithwaite 4519 (U)
GU478854
GU478523
GU478605
n.a.
n.a.
Averyanov VH2540
(AAU)
Elmer 11565 (U)
GU478804
GU478501
GU478612
n.a.
n.a.
GU478865
GU478563
n.a.
n.a.
n.a.
Lindsaea azurea Christ
Lindsaea bifida (Kaulf.) Mett.
ex Kuhn
Lindsaea bifida (Kaulf.) Mett.
ex Kuhn
Lindsaea blanda Mett. ex
Kuhn
Lindsaea blotiana
K.U.Kramer 1
Lindsaea blotiana
K.U.Kramer 2
Lindsaea bolivarensis
V.Marcano
Lindsaea borneensis Hook.
Lindsaea botrychioides
A.St.-Hil.
Lindsaea bouillodii Christ
Lindsaea brachypoda (Baker)
Salomon
Lindsaea brevipes Copel.
Lindsaea cf. cambodgensis
Christ
Lindsaea carvifolia
K.U.Kramer
Lindsaea chienii Ching
Lindsaea chrysolepis
K.U.Kramer
Lindsaea coarctata
K.U.Kramer 1
Lindsaea coarctata
K.U.Kramer 2
Lindsaea crispa Baker
Lindsaea cubensis Underw. &
Maxon
Lindsaea cultrata (Willd.) Sw.
Lindsaea cyclophylla
K.U.Kramer
Lindsaea digitata Lehtonen &
Tuomisto
Lindsaea diplosora Alderw.
Lindsaea dissectiformis Ching
Lindsaea divaricata Klotzsch
Maas 5032 (U)
Averyanov VH4816
(AAU)
Cheesman 165 (U)
Hatschbach 18248 (L)
GU478788
GU478801
GU478506
GU478486
GU478615
n.a.
GU478657
n.a.
GU478359
n.a.
GU478852
FJ360991
GU478536
FJ360901
n.a.
FJ360946
n.a.
n.a.
n.a.
n.a.
Lehtonen 552 (TUR)
GU478799
GU478485
GU478608
n.a.
n.a.
Palmer 747 (U)
GU478806
GU478525
n.a.
n.a.
n.a.
Rakotondrainibe 6350
(P)
Rakotondrainibe 4327
(MO)
Tuomisto 14478 (TUR)
GU478813
GU478510
GU478633
GU478679
GU478381
GU478814
GU478511
n.a.
n.a.
n.a.
FJ360992
FJ360902
FJ360947
GU478652
GU478354
Wong 2 (AAU)
Windisch 4987 (AAU)
GU478866
FJ360994
GU478538
FJ360904
n.a.
FJ360949
n.a.
GU478714
n.a.
GU478416
Nielsen 592 (AAU)
Balgooy 1529 (L)
FJ360993
GU478848
FJ360903
GU478553
FJ360948
n.a.
GU478716
n.a.
GU478418
n.a.
Braithwaite 4029 (MO)
Iwatsuki 14505 (AAU)
GU478809
GU478840
GU478541
GU478502
GU478627
n.a.
n.a.
n.a.
n.a.
n.a.
Mjöberg 9 (BM)
GU478860
GU478562
n.a.
n.a.
n.a.
Kramer 7554 (U)
Croft 216 (L)
FJ360995
GU478850
FJ360905
GU478552
FJ360950
n.a.
n.a.
GU478709
n.a.
GU478411
Tuomisto 14500 (TUR)
FJ360996
FJ360906
FJ360951
GU478656
GU478358
Plowman 11667 (U)
GU478786
GU478507
n.a.
n.a.
n.a.
Parris 11469 (L)
Morton 10035 (BM)
GU478834
GU478795
GU478526
GU478494
n.a.
n.a.
n.a.
GU478687
n.a.
GU478389
Poulsen 128 (AAU)
Liesner 23788 (MO)
GU478859
GU478776
GU478554
GU478483
n.a.
n.a.
GU478668
n.a.
GU478370
n.a.
Tuomisto 14470 (TUR)
EU146057
EU146041
EU146051
GU478698
GU478400
Nielsen 815 (AAU)
Averyanov VH2557
(AAU)
Tuomisto 14553 (TUR)
GU478833
FJ360997
GU478535
FJ360907
GU478598
FJ360952
GU478722
n.a.
GU478424
n.a.
EU146052
EU146040
EU146042
GU478697
GU478399
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
PHYLOGENETICS OF LINDSAEACEAE
311
Table 2. Continued
Taxon
Voucher
trnL-trnF
trnH-psbA
rpoC1
rps4
rps4-trnS
Lindsaea divergens Wall. ex
Hook. & Grev.
Lindsaea doryphora
K.U.Kramer 1
Lindsaea doryphora
K.U.Kramer 2
Lindsaea dubia Spreng.
Abdullah 228 (U)
GU478765
GU478465
n.a.
n.a.
n.a.
Poulsen 341 (AAU)
GU478868
GU478539
GU478636
GU478683
GU478385
Magintan 560 (AAU)
GU478867
GU478540
n.a.
n.a.
n.a.
Christenhusz 2312
(TUR)
Larsen 42363 (AAU)
Kessler 13597 (GOET)
Tolentino HAL-049 (U)
Tuomisto 14925 (TUR)
GU478779
GU478493
GU478623
GU478701
GU478403
GU478853
n.a.
GU478857
FJ361005
GU478522
GU478521
GU478557
FJ360914
n.a.
GU478606
n.a.
FJ360960
n.a.
GU478678
n.a.
GU478702
n.a.
GU478380
n.a.
GU478404
van der Werff 3418 (U)
Streimann 8951 (L)
Hotta 12856 (U)
FJ361004
FJ360998
GU478820
FJ360913
FJ360908
GU478497
FJ360959
FJ360953
n.a.
GU478689
GU478719
n.a.
GU478391
GU478421
n.a.
Deroin 112 (P)
GU478818
n.a.
n.a.
n.a.
n.a.
Rakotondrainibe 4090
(MO)
Stone 2506 (US)
GU478810
GU478500
n.a.
n.a.
n.a.
GU478766
GU478467
GU478594
n.a.
n.a.
Tuomisto 14927 (TUR)
FJ360999
FJ360944
FJ360954
GU478700
GU478402
Wuzhishan fern survey
533 (MO)
GU478807
GU478555
GU478604
GU478671
GU478373
Brownlie 978 (TUR)
Tuomisto 12742 (TUR)
FJ361000
FJ361001
FJ360909
FJ360910
FJ360955
FJ360956
GU478673
GU478660
GU478375
GU478362
Moran 3637 (AAU)
GU478781
GU478487
n.a.
GU478707
GU478409
Tuomisto 13049 (TUR)
FJ374265
FJ374263
FJ374264
GU478717
GU478419
Charoenphol 5081
(AAU)
Christenhusz 2826
(TUR)
Rojas 2350 (BM)
GU478855
n.a.
GU478607
n.a.
n.a.
GU478772
GU478435
GU478592
GU478649
GU478351
n.a.
GU478436
n.a.
n.a.
n.a.
Blake 21210 (MO)
Nielsen 542 (AAU)
Poulsen 72 (AAU)
Clemens 30733 (BM)
Hennipman 3937 (U)
Poulsen 1714 (TUR)
Prance 15677 (U)
GU478856
GU478822
GU478821
GU478764
FJ361002
FJ361003
GU478792
GU478520
GU478532
GU478531
GU478466
FJ360911
FJ360912
GU478490
n.a.
n.a.
n.a.
n.a.
FJ360957
FJ360958
n.a.
GU478682
GU478669
GU478670
GU478711
n.a.
n.a.
n.a.
GU478384
GU478371
GU478372
GU478413
n.a.
n.a.
n.a.
Saiki 1093 (Z)
Braithwaite 4304 (U)
Tuomisto 14466 (TUR)
GU478803
GU478831
FJ361006
GU478499
n.a.
FJ360915
GU478596
GU478629
FJ360961
n.a.
GU478681
GU478651
n.a.
GU478383
GU478353
Lindsaea ensifolia Sw. 1
Lindsaea ensifolia Sw. 2
Lindsaea cf. fissa Copel.
Lindsaea falcata (Dryand.)
Rosenst.
Lindsaea feei C.Chr.
Lindsaea fraseri Hook.
Lindsaea gomphophylla
Baker
Lindsaea goudotiana (Kunze)
Mett. ex Kuhn
Lindsaea grandiareolata
(Bonap.) K.U.Kramer
Lindsaea gueriniana
(Gaudich.) Desv.
Lindsaea guianensis (Aubl.)
Dryand.
Lindsaea hainaniana
(K.U.Kramer) Lehtonen &
Tuomisto
Lindsaea harveyi Carrière
Lindsaea hemiglossa
K.U.Kramer 1
Lindsaea hemiglossa
K.U.Kramer 2
Lindsaea hemiptera
K.U.Kramer
Lindsaea heterophylla
Dryand.
Lindsaea imrayana (Hook.)
Perez 1
Lindsaea imrayana (Hook.)
Perez 2
Lindsaea incisa Prent.
Lindsaea integra Holttum 1
Lindsaea integra Holttum 2
Lindsaea jamesonioides Baker
Lindsaea javanensis Blume 1
Lindsaea javanensis Blume 2
Lindsaea javitensis Humb. &
Bonpl. ex Willd.
Lindsaea kawabatae Kurata
Lindsaea kingii Copel.
Lindsaea lancea (L.) Bedd.
var. lancea
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
312
S. LEHTONEN ET AL.
Table 2. Continued
Taxon
Voucher
trnL-trnF
trnH-psbA
rpoC1
rps4
rps4-trnS
Lindsaea lancea (L.) Bedd.
var. leprieurii (Hook.)
K.U.Kramer 1
Lindsaea lancea (L.) Bedd.
var. leprieurii (Hook.)
K.U.Kramer 2
Lindsaea lancea (L.) Bedd.
var. submontana Boudrie &
Cremers
Lindsaea lapeyrousei (Hook.)
Baker 1
Lindsaea lapeyrousei (Hook.)
Baker 2
Lindsaea leptophylla Baker
Maas 2296 (U)
GU478773
GU478481
n.a.
GU478706
GU478408
Christenhusz 2552
(TUR)
GU478780
GU478504
GU478617
GU478654
GU478356
Granville 14959 (CAY)
GU478774
GU478480
GU478614
n.a.
n.a.
Hadley 201 (BM)
n.a.
GU478556
GU478626
n.a.
n.a.
Brownlie 1575 (U)
FJ361007
FJ360916
FJ360962
GU478680
GU478382
GU478819
GU478509
n.a.
n.a.
n.a.
GU478784
FJ361008
FJ361009
GU478837
GU478808
GU478505
FJ360917
FJ360918
GU478527
GU478542
n.a.
FJ360963
FJ360964
n.a.
GU478628
GU478718
GU478721
GU478674
n.a.
n.a.
GU478420
GU478423
GU478376
n.a.
n.a.
GU478815
GU478512
GU478634
n.a.
n.a.
malayensis Holttum
Raharimalala 2017
(MO)
Bernard 4775 (P)
Braggins 589 (AAU)
Alston 16699 (U)
Elmer 16151 (U)
Charoenphol 4999
(AAU)
Rakotondrainibe 6349
(P)
Tagawa 4781 (U)
GU478836
GU478545
n.a.
n.a.
n.a.
malayensis Holttum
Schneider 222 (Z)
GU478858
GU478530
GU478602
GU478672
GU478374
media R.Br. 1
media R.Br. 2
Gittins s.n. (AAU)
van der Werff 11655
(MO)
Liesner 7062 (MO)
GU478842
GU478843
GU478515
GU478516
n.a.
GU478597
n.a.
n.a.
n.a.
n.a.
GU478783
GU478478
n.a.
n.a.
n.a.
Elmer 13488 (U)
GU478864
GU478558
n.a.
n.a.
n.a.
Kramer 8005 (U)
GU478863
GU478559
n.a.
n.a.
n.a.
Everist 8062 (AAU)
Lan 5065 (L)
FJ361010
GU478812
FJ360919
GU478513
FJ360965
n.a.
n.a.
n.a.
n.a.
n.a.
Guillaumet 4206 (P)
GU478811
n.a.
n.a.
n.a.
n.a.
Edwards 4414A (L)
FJ361011
FJ360920
FJ360966
n.a.
n.a.
Cicuzza 104 (GOET)
McKee 2617 (U)
Larsen 42928 (U)
GU478849
GU478829
FJ361012
GU478534
n.a.
FJ360921
GU478631
n.a.
FJ360967
GU478676
n.a.
GU478685
GU478378
n.a.
GU478387
Parris 11099 (AAU)
GU478824
GU478548
GU478632
n.a.
n.a.
Kramer 8004 (U)
GU478823
GU478547
GU478599
n.a.
n.a.
Averyanov VH4814
(AAU)
FJ361013
FJ360922
FJ360968
n.a.
n.a.
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
lherminieri Fée
linearis Sw.
lobata Poir. in Lam.
longifolia Copel.
lucida Blume
Lindsaea
Baker
Lindsaea
1
Lindsaea
2
Lindsaea
Lindsaea
madagascariensis
Lindsaea meifolia (Kunth)
Mett. ex Kuhn
Lindsaea merrillii Copel. ssp.
merrillii
Lindsaea merrillii Copel. ssp.
yaeyamensis (Tagawa)
K.U.Kramer
Lindsaea microphylla Sw.
Lindsaea millefolia
K.U.Kramer 1
Lindsaea millefolia
K.U.Kramer 2
Lindsaea monocarpa Rosenst.
in C.Chr.
Lindsaea multisora Alderw.
Lindsaea nervosa Mett.
Lindsaea oblanceolata
Alderw.
Lindsaea obtusa J.Sm. ex
Hook. 1
Lindsaea obtusa J.Sm. ex
Hook. 2
Lindsaea orbiculata (Lam.)
Mett. ex Kuhn
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
PHYLOGENETICS OF LINDSAEACEAE
313
Table 2. Continued
Taxon
Voucher
trnL-trnF
trnH-psbA
rpoC1
rps4
rps4-trnS
Lindsaea ovoidea Fée
Lindsaea oxyphylla Baker
Lindsaea pacifica
K.U.Kramer
Lindsaea pallida Klotzsch
Hatschbach 7083 (L)
Gautier 2662 (P)
Brownlie 979 (U)
FJ361014
GU478816
FJ361015
FJ360923
GU478508
FJ360924
FJ360969
n.a.
FJ360970
GU478713
n.a.
GU478663
GU478415
n.a.
GU478365
Christenhusz 2518
(TUR)
Poulsen 342 (AAU)
GU478778
GU478479
GU478624
GU478705
GU478407
GU478851
GU478533
n.a.
GU478675
GU478377
Larsen 42927 (AAU)
FJ361016
FJ360925
FJ360971
GU478684
GU478386
Boudrie 4254 (TUR)
GU478775
GU478492
GU478622
GU478695
GU478397
Nielsen 816 (AAU)
Kjellberg 3561 (BM)
Kramer 2891 (U)
Tuomisto 14940 (TUR)
Brownlie 996 (U)
FJ361021
GU478767
GU478782
FJ361017
FJ361018
FJ360930
GU478468
GU478477
FJ360926
FJ360927
FJ360976
n.a.
n.a.
FJ360972
FJ360973
GU478686
n.a.
n.a.
GU478659
GU478666
GU478388
n.a.
n.a.
GU478361
GU478368
Callmander 291 (P)
Price 2789 (Z)
GU478768
GU478838
GU478471
GU478544
GU478593
n.a.
GU478661
n.a.
GU478363
n.a.
Christenhusz 3384
(TUR)
Tuomisto 13045 (TUR)
Croat 90913 (MO)
Mackee 6609 (P)
Wood 10051 (BISH)
FJ361019
FJ360928
FJ360974
n.a.
n.a.
FJ361028
GU478771
GU478830
GU478825
FJ360937
GU478469
GU478519
GU478537
FJ360983
n.a.
n.a.
GU478601
GU478692
n.a.
n.a.
GU478662
GU478394
n.a.
n.a.
GU478364
Hou 245 (U)
GU478861
GU478560
n.a.
n.a.
n.a.
Alston 16692 (U)
GU478805
GU478528
n.a.
GU478723
GU478425
Brousilie 1049 (U)
GU478826
GU478551
n.a.
GU478665
GU478367
Christenhusz 3588
(TUR)
FJ361020
FJ360929
FJ360975
GU478653
GU478355
Jaag 1730 (Z)
Boudrie 4250 (TUR)
Tolentino HAL-026 (U)
Poole 2060 (Z)
GU478847
GU478777
GU478832
GU478794
GU478564
GU478482
GU478549
GU478476
n.a.
GU478618
GU478600
GU478621
n.a.
GU478704
GU478710
GU478691
n.a.
GU478406
GU478412
GU478393
Williams 14263 (US)
GU478793
GU478475
GU478620
n.a.
n.a.
FJ361023
GU478828
FJ361024
FJ360932
GU478518
FJ360933
FJ360978
n.a.
FJ360979
n.a.
n.a.
GU478688
n.a.
n.a.
GU478390
schizophylla (Baker)
Hoogland 10860 (L)
Munzinger 1254 (P)
Christenhusz 2618
(TUR)
Sledge 613 (Z)
GU478802
GU478498
n.a.
n.a.
n.a.
sessilis Copel.
sp. 1
sp. 2
Koster 13846 (U)
Cicuzza 891 (GOET)
Kluge 7230 (GOET)
GU478862
GU478846
FJ361022
GU478561
GU478546
FJ360931
n.a.
GU478635
FJ360977
n.a.
n.a.
GU478664
n.a.
n.a.
GU478366
Lindsaea parallelogramma
Alderw.
Lindsaea parasitica (Roxb. ex
Griffith) Hieron.
Lindsaea parkeri (Hook.)
Kuhn
Lindsaea pectinata Blume
Lindsaea pellaeiformis Christ
Lindsaea pendula Klotzsch
Lindsaea phassa K.U.Kramer
Lindsaea pickeringii (Brack.)
Mett. ex. Kuhn
Lindsaea plicata Baker
Lindsaea polyctena
K.U.Kramer
Lindsaea portoricensis Desv. 1
Lindsaea portoricensis Desv. 2
Lindsaea pratensis Maxon
Lindsaea prolongata E.Fourn.
Lindsaea propinqua Hook. in
Night.
Lindsaea pseudohemiptera
(Alderw.) Lehtonen &
Tuomisto
Lindsaea pulchella (J.Sm.)
Mett. ex Kuhn
Lindsaea pulchra (Brack.)
Carrière ex Seem.
Lindsaea quadrangularis
Raddi ssp. antillensis
K.U.Kramer
Lindsaea regularis Rosenst.
Lindsaea reniformis Dryand.
Lindsaea rigida J.Sm.
Lindsaea rigidiuscula Lindm.
1
Lindsaea rigidiuscula Lindm.
2
Lindsaea rosenstockii Brause
Lindsaea rufa K.U.Kramer
Lindsaea sagittata Dryand.
Lindsaea
Christ
Lindsaea
Lindsaea
Lindsaea
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
314
S. LEHTONEN ET AL.
Table 2. Continued
Taxon
Voucher
trnL-trnF
trnH-psbA
rpoC1
rps4
rps4-trnS
Lindsaea sp. 3
Lindsaea schomburgkii
Klotzsch
Lindsaea seemannii J.Sm. in
Seem.
Lindsaea semilunata (C.Chr.)
C.Chr.
Lindsaea sphenomeridopsis
K.U.Kramer
Lindsaea spruceana Mett. ex
Kuhn
Lindsaea stolonifera Mett. ex
Kuhn
Lindsaea stricta (Sw.)
Dryand. var.
jamesoniiformis
K.U.Kramer
Lindsaea stricta (Sw.)
Dryand. var. stricta
Lindsaea stricta (Sw.)
Dryand. var. parvula (Fée)
K.U.Kramer
Lindsaea subtilis K.U.Kramer
Laegaard 13835 (AAU)
Tuomisto 13044 (TUR)
FJ361025
FJ361026
FJ360934
FJ360935
FJ360980
FJ360981
n.a.
GU478694
n.a.
GU478396
Hammel 3369 (AAU)
GU478770
GU478470
n.a.
n.a.
n.a.
Renz 14307 (U)
GU478797
GU478489
GU478619
GU478693
GU478395
Renz 14184 (U)
FJ361027
FJ360936
FJ360982
GU478708
GU478410
Quipuscoa 878 (AAU)
GU478787
n.a.
n.a.
n.a.
n.a.
Braithwaite 4283 (U)
GU478827
GU478524
n.a.
n.a.
n.a.
Maas 6460 (U)
GU478790
GU478473
GU478611
GU478696
GU478398
Boudrie 4246 (TUR)
GU478791
GU478472
GU478610
GU478650
GU478352
Boudrie 4253 (TUR)
GU478789
GU478474
GU478625
GU478690
GU478392
van der Werff 12855
(MO)
Granville 15461 (CAY)
Tuomisto 14170 (TUR)
GU478817
GU478514
GU478595
n.a.
n.a.
GU478785
FJ361029
GU478495
FJ360938
GU478630
FJ360984
GU478703
GU478655
GU478405
GU478357
Hartley 12334 (AAU)
Maguine 53824 (U)
Kato 14212 (MO)
FJ361030
GU478798
GU478839
FJ360939
GU478491
GU478543
FJ360985
n.a.
GU478603
GU478677
GU478715
n.a.
GU478379
GU478417
n.a.
Tuomisto 13048 (TUR)
FJ361031
FJ360940
FJ360986
GU478699
GU478401
Cameron s.n. (AAU)
FJ361032
FJ360941
FJ360987
n.a.
n.a.
Tuomisto 13002 (TUR)
GU478796
GU478488
GU478616
GU478658
GU478360
Bostock 638 (Z)
Sledge 1377 (U)
GU478841
GU478835
GU478517
GU478550
n.a.
n.a.
n.a.
GU478720
n.a.
GU478422
Alston 16860 (U)
McKee 5304 (U)
Lehtonen 621 (TUR)
Crookes s.n. (U)
Smith 5918 (U)
FJ361034
GU478844
GU478800
GU478769
GU478845
FJ360943
GU478496
GU478484
GU478503
GU478529
FJ360989
n.a.
GU478609
n.a.
n.a.
GU478667
n.a.
GU478712
n.a.
n.a.
GU478369
n.a.
GU478414
n.a.
n.a.
Christenhusz 3508
(TUR)
Ballard 1390 (US)
GU478725
GU478429
GU478567
GU478640
n.a.
GU478757
GU478446
GU478570
n.a.
n.a.
Kramer 11073 (MO)
GU478758
GU478447
n.a.
n.a.
n.a.
Lindsaea surinamensis Posth.
Lindsaea taeniata
K.U.Kramer
Lindsaea tenuifolia Blume
Lindsaea tenuis Klotzch
Lindsaea tetragona
K.U.Kramer
Lindsaea tetraptera
K.U.Kramer
Lindsaea trichomanoides
Dryand.
Lindsaea ulei Hieron. ex
Christ
Lindsaea walkerae Hook.
Lindsaea venusta Kaulf. ex
Kuhn
Lindsaea werneri Rosenst.
Lindsaea vieillardii Mett.
Lindsaea virescens Sw.
Lindsaea viridis Col.
Lindsaea vitiensis
K.U.Kramer
Lonchitis hirsuta L.
Nesolindsaea caudata (Hook.)
Lehtonen & Christenh.
Nesolindsaea kirkii (Hook. ex
Baker) Lehtonen &
Christenh.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
PHYLOGENETICS OF LINDSAEACEAE
315
Table 2. Continued
Taxon
Voucher
trnL-trnF
trnH-psbA
rpoC1
rps4
rps4-trnS
Odontosoria aculeata (L.)
J.Sm.
Odontosoria afra
(K.U.Kramer) J.P.Roux
Odontosoria africana
F.Ballard
Odontosoria angustifolia
(Bernh.) C.Chr.
Odontosoria biflora (Kaulf.)
C.Chr.
Odontosoria chinensis (L.)
J.Sm.
Odontosoria deltoidea (Copel.)
Lehtonen & Tuomisto 1
Odontosoria deltoidea (Copel.)
Lehtonen & Tuomisto 2
Odontosoria flexuosa Maxon
Odontosoria fumarioides (Sw.)
J.Sm.
Odontosoria guatemalensis
Christ
Odontosoria jenmanii Maxon
Odontosoria melleri (Hook.)
C.Chr.
Odontosoria retusa (Cav.)
J.Sm.
Odontosoria scandens (Desv.)
C.Chr.
Odontosoria schlechtendalii
(C.Presl.) C.Chr.
Odontosoria wrightiana
Maxon
Osmolindsaea japonica
(Baker) Lehtonen &
Christenh.
Osmolindsaea sp.
Osmolindsaea odorata (Roxb.)
Lehtonen & Christenh. 1
Osmolindsaea odorata (Roxb.)
Lehtonen & Christenh. 2
Osmolindsaea odorata (Roxb.)
Lehtonen & Christenh. 3
Pteridium pinetorum
C.N.Page & R.R.Mill
Saccoloma elegans Kaulf.
Saccoloma inaequale (Kunze)
Mett.
Sphenomeris clavata (L.)
Maxon 1
Sphenomeris clavata (L.)
Maxon 2
Tapeinidium amboynense
(Hook.) C.Chr.
Christenhusz 4242
(TUR)
Hess-Wyss s.n. (Z)
GU478740
GU478463
GU478580
n.a.
n.a.
GU478738
GU478454
GU478578
n.a.
n.a.
Lewate 5959 (P)
GU478739
GU478455
n.a.
n.a.
n.a.
Sarasin 65 (Z)
GU478736
GU478451
n.a.
n.a.
n.a.
Raulerson 5549 (BISH)
GU478732
GU478453
GU478586
n.a.
n.a.
Mäkinen 98-239 (TUR)
GU478731
GU478452
n.a.
n.a.
n.a.
Mackee 19315 (P)
GU478733
n.a.
n.a.
n.a.
n.a.
Buchhofz 1051 (P)
GU478734
n.a.
n.a.
n.a.
n.a.
Ernst 1944 (BM)
Christenhusz 3050
(TUR)
Ventura 1090 (BM)
GU478742
GU478744
GU478464
GU478461
GU478583
GU478579
GU478648
n.a.
GU478350
n.a.
GU478746
GU478458
GU478584
n.a.
n.a.
Zahner 10 (Z)
Randriamanarivo 41
(MO)
Fallen 620 (MO)
GU478747
GU478737
GU478462
GU478456
n.a.
n.a.
n.a.
n.a.
n.a.
n.a.
GU478735
GU478450
n.a.
n.a.
n.a.
Christenhusz 3460
(TUR)
Nee 24879 (Z)
GU478743
GU478459
GU478581
n.a.
n.a.
GU478745
GU478457
GU478585
n.a.
n.a.
Morton 4343 (BM)
GU478741
GU478460
GU478582
n.a.
n.a.
Huang 329 (MO)
GU478761
GU478433
GU478590
GU478644
GU478346
Du Puy 2397 (MO)
Charoenphol 4708
(AAU)
Averyanov VH3287
(AAU)
Kramer 5993 (U)
GU478763
GU478759
GU478434
GU478430
n.a.
GU478588
n.a.
GU478647
n.a.
GU478349
GU478760
GU478431
GU478589
GU478646
GU478348
GU478762
GU478432
GU478591
GU478645
GU478347
Lehtonen 696 (TUR)
GU478724
GU478426
GU478566
GU478637
n.a.
Tuomisto 14948 (TUR)
Tuomisto 14409 (TUR)
GU478728
GU478727
GU478427
GU478428
GU478569
GU478568
GU478639
GU478638
n.a.
n.a.
Christenhusz 4218
(TUR)
Axelrod 5550 (MO)
GU478729
GU478448
GU478587
n.a.
n.a.
GU478730
GU478449
n.a.
n.a.
n.a.
Dayton 26238 (BISH)
GU478753
GU478441
GU478573
GU478642
GU478344
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
316
S. LEHTONEN ET AL.
Table 2. Continued
Taxon
Voucher
trnL-trnF
trnH-psbA
rpoC1
rps4
rps4-trnS
Tapeinidium calomelanos
K.U.Kramer
Tapeinidium denhamii
(Hook.) C.Chr.
Tapeinidium gracile Alderw.
Tapeinidium longipinnulum
(Ces.) C.Chr.
Tapeinidium luzonicum
(Hook.) K.U.Kramer
Tapeinidium melanesicum
K.U.Kramer
Tapeinidium moorei (Hook.)
Hieron.
Tapeinidium novoguineense
K.U.Kramer
Tapeinidium pinnatum (Cav.)
C.Chr.
Price 1305 (Z)
GU478755
GU478442
GU478575
n.a.
n.a.
Zogg 9266 (Z)
GU478748
GU478440
GU478571
n.a.
n.a.
Kluge 7058 (GOET)
Holttum s.n. (Z)
GU478750
GU478754
GU478437
GU478439
GU478577
GU478574
n.a.
GU478641
n.a.
GU478343
Kessler 13610 (GOET)
GU478751
GU478444
GU478576
GU478643
GU478345
Webster 14055 (BISH)
GU478749
GU478443
GU478572
n.a.
n.a.
Mackee 196 (AAU)
GU478756
GU478445
n.a.
n.a.
n.a.
Brass 23048 (BM)
GU478752
GU478438
n.a.
n.a.
n.a.
Kessler 13613 (GOET)
FJ360990
FJ360900
FJ360945
n.a.
n.a.
During the course of this study we also produced a trnL-trnF sequence (GenBank accession GU478565) of L. diplosora
(voucher Wong 2439, L), but this specimen was not included in the analyses, as we failed to produce other sequences from
it, and the trnL-trnF sequence was identical with the other L. diplosora sequence we used.
n.a., not available.
result from contamination or copy–paste errors
during data manipulation.
PHYLOGENETIC
ANALYSES
Our data set included three sequence anomalies
which are most parsimoniously explained as short
inversions. These were the 13-bp inversion in trnHpsbA spacer present in Sphenomeris clavata (L.)
Maxon and Lindsaea linearis Sw., the 7-bp inversion
frequently observed c. 200 bp upstream of the trnF
gene in various Lindsaea and Odontosoria spp. and
the 4-bp inversion located c. 350 bp upstream of the
trnF gene in Lindsaea tenuifolia Blume and L.
polyctena K.U.Kramer. The apparently inverted
sequence fragments were replaced with their complement sequences in the sequence data and an additional binary character was coded for each inversion
event to record the original orientation of the inverted
sequence. It would be preferable to optimize the
inversions directly under the framework of dynamic
homology (Catalano, Saidman & Vilardi, 2009), but
the current algorithms (Vinh, Varón & Wheeler, 2006;
Wheeler, 2007) do not recognize this kind of minute
inversions. The inversion events were mapped with
delayed transformation (DELTRAN) optimization on
the consensus trees to minimize the reversals and
interpret character-state changes as convergences
whenever possible (Swofford & Maddison, 1987; for
detailed discussion, see Agnarsson & Miller, 2008).
Character evolution was investigated with MacClade
(Maddison & Maddison, 2000).
We evaluated the robustness of the resulting phylogenetic hypotheses by calculating both nodal support
and nodal stability measures. Nodal support indicates
how well the data in question supports a given node,
whereas nodal stability specifies how sensitive the
node is to variation in analytical assumptions (Giribet,
2003). We obtained nodal support values by jackknifing the implied POY alignments (Farris et al., 1996;
Giribet, 2005). Bremer support values (Bremer, 1988)
were not used, because they would have been biased by
the fact that we do not have 100% character sampling
(DeBry, 2001). As the optimal topology is, by definition,
the hypothesis that conforms with the data best
(Fitzhugh, 2006b), we do not see any logical reason
to collapse ‘poorly supported’ nodes to polytomies.
Instead, the jackknife values are shown on the topologies to draw attention to areas where the results are
most dependent on specific assumptions and can most
easily be challenged.
We evaluated the stability of our hypothesis by
applying sensitivity analysis (Wheeler, 1995), i.e. by
varying the assumptions made about transformation
costs. The phylogenetic trees we present are based on
equal transformation costs for all character-state
changes, which maximizes the explanatory power of
the hypothesis (Frost et al., 2001; Giribet, Edgecombe
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
PHYLOGENETICS OF LINDSAEACEAE
Phylogenetic analyses were run in a parallel environment of 2 ¥ 2.26 GHz Quad-Core Intel Xeon
Macintosh, using either POY (for molecular data,
combined analysis of molecular and morphological
data and sensitivity analyses; Varón, Vinh & Wheeler,
2010) or TNT (for morphological data analysis and
jackknife calculations; Goloboff, Farris & Nixon,
2008). POY searches were conducted by a combination of 500 random addition starting trees with
subtree pruning and reconnection (SPR) and tree
bisection–reconnection (TBR) branch swapping, and
evaluating all the suboptimal trees within 5% of the
best cost, followed by 20 rounds of ratcheting (Nixon,
1999), 200 rounds of tree fusing (Goloboff, 1999) and
final swapping with SPR and TBR. Sensitivity analyses were principally similar, but only 20 random
addition starting trees were built, no suboptimal
topologies were evaluated during TBR swapping and
only 10 rounds of ratcheting were performed. Furthermore, in sensitivity analyses, the time allocated
for each swapping round was limited to 3600 s for
SPR, TBR and tree fusing and 20 000 s for ratcheting.
The results of the sensitivity analyses were investigated with the aid of Cladescan (Sanders, 2010). In
the morphological data analysis, we applied a search
with 500 random addition starting trees swapped
with ratcheting and holding 10 trees per replicate.
Morphological characters were equally weighted and
treated as non-additive (unordered) throughout all
the analyses. For jackknife calculations, 100 pseudoreplicates with a deletion probability of e–1 were
performed and, for each pseudoreplicate, 100 random
addition starting trees were built and swapped with
ratcheting. The command lines applied are given in
Appendix 5. The numbers of potentially parsimony
informative characters were calculated in PAUP*
4.0b10 (Swofford, 2002) using the implied alignments
and treating a gap as a fifth character state.
4
RESULTS
1
2
SAMPLING
0.5
transversion:transition
& Wheeler, 2001; Terry & Whiting, 2005a, 2005b;
Espinasa, Flick & Giribet, 2007; Whiting et al., 2008).
However, equal costs may lead to illogical, non-metric
results and actually cannot be applied when ‘true’
indel lengths are variable (Giribet & Wheeler, 2007),
and some studies have preferred non-equal costs (e.g.
Laamanen et al., 2005; Sørensen, Sterrer & Giribet,
2006; Boyer & Giribet, 2007; Giribet & Wheeler, 2007;
Kutty et al., 2007; Lindgren & Daly, 2007). To test the
robustness of the equal-cost hypothesis, we also
applied another 15 transformation cost regimes.
Theoretically, the available parameter space is infinite, but in practice this space can be narrowed down
to a reasonable set of parameters. The lower limit for
a transversion–transition cost ratio must be 0.5 (otherwise transformation A → C → G would be cheaper
than A → G) and the gap cost must be at least one
half of the cost of transformations (Wheeler, 1995). If
the gap cost reaches a high enough level, the resulting tree starts to reflect the history of gaps more than
of substitutions, until substitution information
becomes completely overruled by the gaps (Spagna &
Álvarez-Padilla, 2008). Simulations and empirical
data suggested that the upper limit for a gap cost
should not be more than four times the highest nucleotide transformation cost (Spagna & Álvarez-Padilla,
2008). Based on these constraints, we varied the
transversion–transition and indel–transversion cost
ratio in four increments (0.5, 1, 2, 4) in order to
equally sample across the reasonable parameter
space and hence analysed 16 different transformation
cost regimes (Fig. 2). The separately coded inversion
events and, in the total-evidence analysis, the morphological characters, were given the same weight as
indels (Wheeler & Hayashi, 1998; Giribet et al., 2002;
Schulmeister, Wheeler & Carpenter, 2002; Grazia,
Schuh & Wheeler, 2008).
317
0.5
1
2
4
substitution:indel
Figure 2. Transformation
measure nodal stability.
cost
regimes
applied
to
SUCCESS
Although some morphological characters could not be
recorded for all taxa, in practice our taxon sampling
was limited by the availability of specimens suitable
for DNA extraction. Our final sampling covered 195
terminals representing 175 taxa (as accepted here) or
approximately 69% of the taxa (73% of the species)
generally accepted in Lindsaeaceae. All genera of the
family were included in our analyses, except the
monotypic Xyropteris, which did not yield DNA
sequences of adequate quality. Of the other genera,
the most complete sampling was achieved for Lindsaea (71% of accepted taxa) and the least complete for
Tapeinidium (50% of accepted taxa). Some taxa were
represented by more than a single specimen.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
318
S. LEHTONEN ET AL.
Amplification and sequencing success varied widely
among the sampled loci, such that trnL-trnF
sequences were obtained for 98% of the sampled taxa
but rps4-trnS sequences for only 43% (Table 3). The
proportion of missing data at the data set level (195
taxa ¥ 7 sequences) was approximately 33% and, at
the character level (195 taxa ¥ 3636 aligned characters), c. 25%.
Sequence lengths were 567–580 bp for rps4, 231–
295 bp for the rps4-trnS spacer, 378–534 bp for the
trnL-trnF spacer and 426–495 bp for the trnH-psbA
spacer. The sequenced rpoC1 region was the same
length in all species (732 bp), but the length of the
POY implied alignment was 734 bp. The number of
potentially parsimony informative characters in the
implied alignments varied from 186 in rpoC1 to 589
in the trnL-trnF spacer.
PHYLOGENETIC
HYPOTHESES
Molecular data
When analysed under equal transformation costs, the
molecular data resulted in a single most parsimonious tree of 5483 steps (Figs 3–7). This tree resolved
Lonchitis, Saccoloma and Cystodium as the first
branching lineages of the ingroup, with Cystodium
being sister to all traditional lindsaeoid genera.
Within the lindsaeoids, Sphenomeris clavata
formed the first diverging lineage. All other species
previously placed in Sphenomeris were mixed with
Odontosoria in the next diverging lineage. The next
clade brought together species that have previously
not been associated with each other. Tapeinidium is a
well-established genus, but it was found to be a sister
to a group of species previously placed in Lindsaea;
here, these are treated as two new genera, Nesolindsaea and Osmolindsaea.
All other Lindsaea spp. formed a single clade.
Core Lindsaea is discussed here by using informal
clades numbered from I to XIII. The first diverging
lineage within core Lindsaea (clade I) is composed of
two morphologically unusual species from Central
America and northern South America. The six
species of clade II are morphologically diverse, have
great variation in the studied sequences and are
distributed from Madagascar through Melanesia to
New Zealand.
Clade III consists of a single species from Australia,
L. incisa Prent., which is rather distinct from other
species based on the studied sequences. Clade IV
consists of species distributed from Australia through
Melanesia to South-East Asia. The species in clade V
are true epiphytes, an unusual habit within Lindsaea.
Clade VI consists of a large number of species from
the Melanesian and Pacific islands.
The phylogenetic relationships among clades VII–
XIII were resolved only partly, such that clades VII
(VIII–IX), X and (XI–XIII) formed a polytomy. Clade
VII consists of only two Australasian species. Clades
VIII and IX were resolved as sisters. Clade VIII
consists of mostly Asian species, but includes L. grandiareolata (Bonap.) K.U.Kramer from Madagascar and
L. vieillardii Mett. from New Caledonia. Lindsaea
vieillardii was placed as the first branching species in
clade VIII with rather low stability and no jackknife
support. Clade IX includes many species endemic to
Madagascar, but also species with wider distribution
in the Palaeotropics. Clade X consists of species
endemic to New Caledonia or New Zealand.
Clades XI–XIII are strictly Neotropical, and indeed
all Neotropical Lindsaea spp. were placed in these
clades, except the two species that form clade I.
However, we failed to sample L. macrophylla Kaulf., a
Neotropical species that morphologically closely
resembles some species in clade IX. All species in clade
XI are endemic to the Atlantic coastal rain forests
of south-eastern Brazil. Clade XII consists of L.
imrayana (Hook.) Perez [Ormoloma imrayanum
Hook.) Maxon], which differs from the other species by
its distinct morphology and marked differences in the
studied sequences. Although the position of this
lineage was unstable in the sensitivity analysis, it was
always placed well within core Lindsaea. Most Neotropical species were placed in clade XIII. Although large,
this clade cannot be usefully subdivided because the
sequences we used were almost invariable among the
species. Consequently, most of the nodes within clade
XIII are highly unstable and lack jackknife support.
Table 3. The number of taxa sampled for each of the included data sets
Sequence range (bp)
Implied alignment (bp)
PI characters*
No. of terminal taxa
% missing taxa
Morphology
Inversion
rps4
rps4-trnS
trnL-trnF
trnH-psbA
rpoC1
55
55
55
195
0
3
3
3
192
2
567–580
605
208
87
55
231–295
411
225
83
57
378–534
1056
589
192
2
426–495
772
411
186
5
732
734
186
117
40
*Potentially parsimony-informative characters.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
PHYLOGENETICS OF LINDSAEACEAE
319
Sphenomeris
Odontosoria
Nesolindsaea
Osmolindsaea
Tapeinidium
Lindsaea
10 changes
Figure 3. Phylogram showing the topology and branch lengths of the single most parsimonious tree obtained in a POY
analysis of molecular data with equal transformation costs.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
320
S. LEHTONEN ET AL.
Figure 4. Phylogenetic relationships among Lindsaeaceae based on POY analysis of molecular data with equal transformation costs. DELTRAN optimization of the inversion events is shown on the branches. Filled diamonds: 13-bp
inversions in the trnH-psbA spacer from A-rich type to T-rich type. Filled circles: 4-bp inversions in the trnL-trnF spacer
from GT-type to CA-type. Squares: 7-bp inversions in the trnL-trnF spacer, open squares indicate inversion from CT-type
to GA-type and filled squares the reverse. Jackknife support values are shown above the branches, with values below 50
omitted. The results of sensitivity analysis are shown below the branches. Transformation cost regimes (see Fig. 2) under
which a node is resolved as monophyletic is indicated by a black box and unresolved or unsupported relationships are
indicated by white box. In the cases where we propose a change in nomenclature, the old taxon names (Kramer, 1957a,
1967a, b, 1970, 1971a, 1972a, b) are shown in parentheses. Continues in Figure 5.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
PHYLOGENETICS OF LINDSAEACEAE
Figure 5. Continued from Figure 4, continues in Figure 6.
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S. LEHTONEN ET AL.
Figure 6. Continued from Figure 5, continues in Figure 7.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
PHYLOGENETICS OF LINDSAEACEAE
Figure 7. Continued from Figure 6.
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323
324
S. LEHTONEN ET AL.
On average, the nodes in the molecular tree
received 56% jackknife support and were resolved as
monophyletic groups with nine transformation cost
regimes out of the 16 used in the sensitivity analysis.
The inversion events were found to be highly
homoplastic. According to DELTRAN optimization, it
must be assumed that the 4-bp inversion in the trnLtrnF spacer has occurred twice and that the 7-bp
inversion has changed twice from the original orientation, and 20 times back to it.
Morphological data
When analysed under equal transformation costs, the
morphological data resulted in three equally parsimonious trees of 466 steps. The strict consensus tree had
116 resolved nodes (Figs 8–11), 23 of which were
shared with the molecular tree. The morphological
data agreed with the molecular data in placing the
traditional lindsaeoid genera in a monophyletic clade
that excludes Lonchitis and Cystodium (77% jackknife
support) and in recognizing a monophyletic Lindsaea
(clades I–XIII of the molecular tree; without jackknife
support) and a Neotropical clade within Odontosoria
(with 96% jackknife support). Morphological characters were highly homoplastic (consistency index = 0.16,
retention index = 0.76), resulting in relatively poor
resolution and low average jackknife support (13%).
Combined data
The simultaneous analysis of molecular and morphological data under equal transformation costs
resulted in a single most parsimonious tree with 6117
steps (Figs 12–15). The strict consensus tree had, in
total, 184 resolved nodes, and 126 of these were
shared with the molecular tree.
In broad terms, the topologies obtained with the
molecular and combined data sets were similar and
the differences were in some species-level groupings
within the 13 major clades. For example, the two
analyses resolved some sister species relationships in
the Odontosoria–Sphenomeris clade differently.
Within core Lindsaea, the main clades I–XIII were
identical in the two analyses, with the single exception of L. vieillardii which was resolved as sister to
the reminder of clade VIII in the molecular analysis,
but as sister to clade IX in the combined analysis. The
molecular analysis was unable to resolve the divergence order among clades VII, VIII (IX–X) and (XI–
XIII). In the combined analysis, this polytomy was
resolved, although with no jackknife support and low
stability (5/16).
The sister species relationships resolved within
clades II, V and VI differed markedly between the
molecular and combined tree. The nodes of the combined tree were better supported and more stable
than those of the molecular tree in the case of clade
II. In contrast, the addition of morphological data
reduced the overall support and stability of the nodes
in clade V and the nodes in clade VI were generally
unstable in both trees. The single-species clade III
(Lindsaea incisa) was in the combined analysis
resolved as sister to clades IV–XIII, whereas in the
molecular tree it had a more derived position as sister
to clades IV–VI. Although clade XIII contains the
same taxa in the molecular and combined tree, its
internal topology was resolved quite differently by the
two analyses. Both analyses recognized the same
monophyletic group, with L. reniformis Dryand. as
sister to the remaining species, but otherwise both
topologies were highly unstable and poorly supported.
The combined tree explained the inversions more
parsimoniously than the molecular tree. The distribution of the 4-bp inversions in the trnL-trnF spacer can
be explained in the combined tree by a single change.
This inversion was only observed in L. tenuifolia and L.
polyctena of clade VI, which were placed as sisters in
the combined tree. The 7-bp inversion can be explained
by assuming two changes from the original orientation
and 19 changes back to it. Despite the high levels of
homoplasy and low average jackknife support in the
morphological analysis, the combined analysis
resulted in a much higher average jackknife support
(65%) than the molecular analysis. Average nodal
stability (8/16) was slightly lower, however.
DISCUSSION
RELIABILITY
OF THE PHYLOGENETIC RESULTS
In general, our taxon sampling (c. 73% of the species)
can be considered sufficient for reliable phylogeny
estimation (e.g. Zwickl & Hillis, 2002). Nevertheless,
in some groups (e.g. Tapeinidium) our sampling
remained rather poor and our inability to sequence all
loci from all taxa may compromise the reliability of
some groupings. The DNA sequences of some closely
related taxa were so similar that the corresponding
phylogenetic hypotheses are tentative at best.
However, the comparison of molecular and morphological evidence in the light of nodal support and
stability measures strengthens the discussion on evolutionary relationships.
Although Lonchitis and Cystodium have traditionally not been considered lindsaeoid genera, nowadays they are usually included in Lindsaeaceae
(Schuettpelz, Korall & Pryer, 2006; Smith et al.,
2006; Schuettpelz & Pryer, 2007). Our analyses
placed Cystodium close to the lindsaeoids, but Lonchitis branched off from the lindsaeoid lineage even
before Saccoloma did. The phylogenetic position of
Lonchitis was well supported and stable in our
analyses, but that of Cystodium was unstable, and
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
PHYLOGENETICS OF LINDSAEACEAE
325
Figure 8. Strict consensus of the three equally parsimonious trees obtained in the analysis of the morphological data. The thick
branches represent nodes that were also supported by the molecular data (Figs 4–7). Jackknife support values are shown above
the branches, with values below 50 omitted. Old taxon names are shown in parentheses. Continues in Figure 9.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
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S. LEHTONEN ET AL.
Figure 9. Continued from Figure 8, continues in Figure 10.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
PHYLOGENETICS OF LINDSAEACEAE
Figure 10. Continued from Figure 9, continues in Figure 11.
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327
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S. LEHTONEN ET AL.
Figure 11. Continued from Figure 10.
several transformation cost regimes in the molecular
and combined analyses resolved it as sister to Saccoloma. Unfortunately, the only DNA sequence that
we managed to obtain from Cystodium was the
trnL-trnF intergenic spacer. This, together with the
fact that our sampling included only two species of
Saccoloma and one dennstaedtioid, renders our
results on the phylogenetic position of Cystodium
and Lonchitis only tentative.
Our analyses strongly support their monophyly of
the traditional lindsaeoid genera. The lindsaeoid
clade obtained 77% jackknife support in the morphological analysis and 100% jackknife support in the
DNA and total-evidence analyses. In the DNA and
total-evidence analyses, the clade was also present
under all transformation cost regimes.
High branch support or stability values as such,
however, cannot guarantee that the correct phylogeny has been inferred. Our molecular sampling was
based on plastid sequences and the obtained tree
can be considered a good estimate of plastid evolution, but plastid phylogenies may in some cases
drastically differ from those inferred from nuclear
markers (e.g. Jakob & Blattner, 2006). Incongruence
can result from hybridization as well as from incomplete lineage sorting of ancient polymorphisms
(Funk & Omland, 2003). A wide sampling of independent loci and multiple individuals per species is
required to detect such patterns (Maddison &
Knowles, 2006). It is generally assumed that incomplete lineage sorting complicates the inference of
recently diverged lineages only, but ancient plastid
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PHYLOGENETICS OF LINDSAEACEAE
329
Figure 12. Phylogenetic relationships among Lindsaeaceae based on combined POY analysis of morphological and
molecular data under equal transformation costs. DELTRAN optimization of the inversion events is shown on the
branches. Filled diamonds: 13-bp inversions in the trnH-psbA spacer from A-rich type to T-rich type. Filled circles: 4-bp
inversions in the trnL-trnF spacer from GT-type to CA-type. Squares: 7-bp inversions in the trnL-trnF spacer, open
squares indicate inversion from CT-type to GA-type and filled squares the reverse. Jackknife support values are shown
above the branches, with values below 50 omitted. The results of sensitivity analysis are shown below the branches.
Transformation cost regimes (see Fig. 2) under which a node is resolved as monophyletic is indicated by a black box,
unresolved or unsupported relationships are indicated by a white box. Old taxon names are shown in parentheses.
Continues in Figure 13.
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330
S. LEHTONEN ET AL.
Figure 13. Continued from Figure 12, continues in Figure 14.
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PHYLOGENETICS OF LINDSAEACEAE
Figure 14. Continued from Figure 13, continues in Figure 15.
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331
332
S. LEHTONEN ET AL.
Figure 15. Continued from Figure 14.
haplotypes may persist for millions of years, potentially also affecting deeper phylogenetic levels
(Jakob & Blattner, 2006). In the present phylogenetic analysis of Lindsaeaceae, these problems may
be responsible for the observed polyphyly of species
and lack of support and stability, especially within
the possibly rapidly radiated South American clade
XIII. Our revised taxonomy, however, is supported
by both molecular evidence and morphological
studies of herbarium specimens.
REVISED GENERIC CLASSIFICATION OF
LINDSAEACEAE
The phylogenetic evidence presented above indicates
that the prevailing generic limits among the traditional lindsaeoid genera are artificial. Three of the
genera as currently circumscribed are either para- or
polyphyletic: Sphenomeris, Odontosoria and Lindsaea
itself. Tapeinidium and Ormoloma are monophyletic,
but Ormoloma is so deeply embedded within Lind-
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PHYLOGENETICS OF LINDSAEACEAE
333
Table 4. Morphological characters supporting the six lindsaeoid genera in the total evidence analysis
Sphenomeris
Odontosoria
Osmolindsaea
Nesolindsaea
Tapeinidium
Lindsaea
8. INDUMENT,
NUMBER OF
CELL SERIES
AT THE BASE:
2–3
20. ARCHITECTURE:
flexuose
50. NUMBER
OF
SPORANGIA/
SORUS: few*
15. LENGTH:
short
25. VEIN
ORDERS:
three
23. TEXTURE:
coriaceous*
33. SHAPE:
equal sided
36. SEGMENTS:
connected
by wing*
15. LENGTH:
short*
16. RACHIS
ABAXIALLY:
keeled*
21. NATURE OF
SULCUS:
broad*
25. VEIN
ORDERS: two*
Numbers refer to character numbers in Appendix 1. Characters supporting a genus but variable within it are marked
with *.
saea that maintaining it as a separate genus is not
justified. Several species traditionally placed in Lindsaea are closely related to Tapeinidium. One of these
is sister to the Tapeinidium clade and also fits morphologically in this rather uniform genus. The other
species are morphologically so unlike Tapeinidium
that they are more practically separated into two new
genera, which are also highly differentiated based on
the studied DNA sequences. Here we describe the
new genera Osmolindsaea and Nesolindsaea and
provide revised circumscriptions for the old ones.
SPHENOMERIS MAXON,
NOM. CONS.
Synonym: Stenoloma Fée, nom. rej.
Typus generis: Sphenomeris clavata (L.) Maxon
Taxonomic history: The typification of Sphenomeris
has caused some confusion. Originally Fée (1852)
described two genera, Odontosoria with one species
(O. uncinella (Kunze) Fée) and Stenoloma with ten
species. Farwell (1931) designated Stenoloma clavata
(L.) Fée as the type of the genus. Probably not aware
of this earlier typification, Pichi-Sermolli (1953) typified Stenoloma with S. dumosa Fée (= Odontosoria
aculeata (L.) J.Sm.). The generic name Sphenomeris
of Maxon (1913) was later conserved against the older
Stenoloma (Lanjouw et al., 1956). Following Morton’s
(1959) proposal, the Committee for Pteridophyta
(1959) changed the typification from S. dumosa to S.
clavata, in order to keep Sphenomeris in the list of
conserved names and to follow the original generic
description more closely. Kramer (1971a) criticized
the re-typification and argued that S. clavata does not
fit in the original generic description. However, the
generic typification by Farwell (1931) makes the later
typification and re-typification superfluous.
Morphological characters used to circumscribe
Sphenomeris and Odontosoria were found to be unsatisfactory by Kramer (1972a) and Sphenomeris has
sometimes been treated as a synonym of Odontosoria
(Tryon & Tryon, 1982; Kramer & Green, 1990).
However, both generic names are still in use (e.g.
Smith et al., 2006; Schuettpelz & Pryer, 2008). Barcelona (2000) suggested that three new genera should
be recognized in the Sphenomeris–Odontosoria group,
but did not formally describe them. In our analyses,
most species of the Sphenomeris–Odontosoria group
formed a monophyletic clade, but the type species of
Sphenomeris (S. clavata) was placed in a clade of its
own as sister to all other lindsaeoids. Therefore, we
recognize Sphenomeris in a narrow sense and transfer most species to a broadly defined Odontosoria.
According to this circumscription, Sphenomeris is
endemic to the Neotropics. Sphenomeris clavata is
distributed from southern Florida to the Bahamas and
the Greater Antilles (Kramer, 1957a). Two similar
species (S. spathulata (Maxon) K.U.Kramer and S.
killipii (Maxon) K.U.Kramer) have been described
from Colombia (Maxon, 1947; Kramer, 1957a), but
both are apparently only known from the type material. We tentatively accept these species as members of
Sphenomeris, but their status needs to be verified.
In the total evidence tree, Sphenomeris has two
morphological apomorphies: less than three scale cells
in the rhizome scales and flexuose rachises (Table 4).
These characters are not unique to Sphenomeris, so it
is nested within Odontosoria in our morphological
tree. However, Sphenomeris is quite distinct based on
the studied DNA sequences and terminates a long
lineage. The separation of Sphenomeris and other
lindsaeoid genera is well supported, although not
fully stable. We failed to amplify the most conservative locus (rps4) for Sphenomeris, so we cannot rule
out the possibility of long-branch attraction towards
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334
S. LEHTONEN ET AL.
the long root node. Sphenomeris clavata is reported to
have a chromosome number N = 38 (Walker, 1966).
This differs from other chromosome counts in Lindsaeaceae and provides additional support for the evolutionary distinctness of Sphenomeris.
ODONTOSORIA FÉE
Synonym: Lindsayopsis Kuhn
Typus generis: Odontosoria uncinella
Fée = O. scandens (Desv.) C.Chr.
(Kunze)
Taxonomic history: The name Odontosoria was first
used for a section of Davallia by Presl (1836). Fée
(1852) used Odontosoria at the generic rank, basing it
on the single species O. uncinella, which was not
published until 1850, and was therefore not known to
Presl. Kuhn (1882) wrongly credited the genus Odontosoria to Presl and described a new genus Lindsayopsis for O. scandens, hence providing a synonym for
Odontosoria. Diels (1899) also accredited Odontosoria
to Presl, but recognized two sections in the genus,
‘Eu-Odontosoria’ for rather small plants with erect
habit and determinate growth and ‘Stenoloma’ for
scandent plants with indefinite growth. This synonymized the two genera (Odontosoria and Stenoloma)
proposed by Fée (1852). Maxon (1913) decided that
both sections need to be recognized at the generic
level, but stated that the name Odontosoria is to be
applied to the scandent group based on the type
species and description by Fée. He clearly stated that
O. chinensis (L.) J.Sm. and S. clavata have no place in
the genera Lindsaea, Schizoloma or Odontosoria, and
he therefore proposed the genus Sphenomeris, with S.
clavata as the type. Tryon & Tryon (1982) and
Kramer & Green (1990) considered Sphenomeris as
congeneric with Odontosoria. The thesis of Barcelona
(2000) provided a good overview of the genus Odontosoria, but proposed a generic classification that is
not well founded or effectively published (article 30.5
of the ICBN; McNeill et al., 2006).
Most of the species that we include in Odontosoria
have already been placed in this genus by some earlier
author. Here we propose just one new combination.
ODONTOSORIA DELTOIDEA (C.CHR.) LEHTONEN &
TUOMISTO, COMB. NOV.
Basionym: Lindsaea deltoidea C.Chr., Index Filic.
393, 1906; based on Lindsaea elongata Labillardière,
Sert. Austro-Caled. 6, t. 9, 1824, non Cavanilles, 1802.
Type: New Caledonia, Labillardière s.n. (holotype P,
P00633680!, isotype P, P00633679!).
Notes: Odontosoria as circumscribed here is a pantropical genus. All Neotropical Odontosoria included
in our analyses were resolved into a single wellsupported and highly stable clade. The first division
within this clade separates the spineless O. schlechtendalii (C.Presl) C.Chr. and O. guatemalensis Christ
from the rest of the Neotropical species, which are all
spiny. This sister clade relationship is supported by
all analyses, including the one based on morphology
only. Tryon & Tryon (1982) considered O. wrightiana
Maxon as a narrow-segmented form of O. aculeata
(L.) J.Sm., but our analyses do not support this view.
We were unable to obtain molecular data from three
Neotropical species, which all share morphological
synapomorphies with the Neotropical clade and are
assumed to belong to it (O. colombiana Maxon, O.
gymnogrammoides Christ and the recently described
O. reyesii Caluff).
The Neotropical clade is sister to a clade that
includes O. chinensis, which is distributed throughout
the Palaeotropics (except continental Africa) and is a
well-known example of a species complex with
various levels of polyploidy and hybridization and
probably several cryptic species (Lin, Kato & Iwatsuki, 1994, 1996). The two African species (O. afra
(K.U.Kramer) J.P.Roux and O. africana F.Ballard) are
morphologically highly similar, but differ in the angle
between primary and secondary divisions, which is
straight in O. africana and acute in O. afra (Kramer,
1971b). The two had identical DNA sequences,
however, and they may be conspecific.
The third main clade within Odontosoria includes
species from Madagascar (O. melleri (Hook. ex Baker)
C.Chr.), Malesia (O. retusa (Cav.) J.Sm.) and New
Caledonia [O. angustifolia (Bernh.) and O. deltoidea].
The New Caledonian species are resolved as sisters
with high support and stability. The DNA sequencing
failed for another New Caledonian endemic, Sphenomeris alutacea (Mett.) Copel., but based on morphological characters it most likely belongs to this
clade as well. The combined analysis resolved O.
retusa and O. melleri as sisters with high support and
stability, unlike the molecular analysis in which they
formed successive lineages in a poorly supported and
unstable grouping.
Odontosoria is rather difficult to define morphologically. In the total evidence analysis, the genus
was supported by the number of sporangia per sorus
being small, but this character is not shared by all
species (Table 4). Cytological data have played an
important role in the taxonomy of the O. chinensis
complex (Lin, Kato & Iwatsuki, 1990; Lin et al.,
1994, 1996). Odontosoria biflora has N = 48,
whereas in O. chinensis both diploid (N = 48) and
tetraploid (N = 96) populations are known (Lin et al.,
1990, 1994). Small deviations from these basic
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PHYLOGENETICS OF LINDSAEACEAE
335
Figure 16. Cross sections of lindsaeoid rhizomes: A, solenostele with an internal sclerified pith (Osmolindsaea odorata,
Ohba 3374, U); B, solenostele (Nesolindsaea caudata, Comanor 1077, MO); C, ‘Lindsaea-type’ protostele (Lindsaea
ovoidea, Lehtonen 558, TUR).
numbers also occur and sometimes segregate
species have been recognized as a result (Lin
et al., 1994, 1996). Both Neotropical species with
available chromosome counts (O. fumarioides (Sw.)
J.Sm. and O. jenmanii Maxon) are clearly tetraploid
(N ª 96; Walker, 1966), but N ª 88 has been reported
for O. deltoidea and O. retusa of the third Odontosoria clade (Brownlie, 1965; Walker in Kramer,
1971a).
OSMOLINDSAEA (K.U.KRAMER) LEHTONEN &
CHRISTENH., GEN. & STAT. NOV.
Basionym: Lindsaea Dryand. ex Sm. section
Osmolindsaea K.U.Kramer, Blumea 15: 560 (1967).
Typus generis: Osmolindsaea odorata (Roxburg) Lehtonen & Christenh.
Distinction: The spores of Osmolindsaea are monolete
and the rhizomes have a solenostele with an internal
sclerified pith (Fig. 16A). In the total evidence analysis, the genus is supported by having short petioles
(Table 4).
Taxonomic history: Kramer (1967b, 1971a) treated
Osmolindsaea as a section of Lindsaea. However, the
clade including Osmolindsaea is sister to Tapeinidium and synonymizing Tapeinidium with Lindsaea
would result in a genus that is morphologically difficult to define. Therefore, we describe Osmolindsaea
here as a new genus of Lindsaeaceae. The name
refers to the scent of the fresh leaves, ‘osme’ meaning
fragrance in Greek.
The following new combinations are proposed here:
Osmolindsaea odorata (Roxb.) Lehtonen & Christenh., comb. nov.
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336
S. LEHTONEN ET AL.
Basionym: Lindsaea odorata Roxb., Calcutta Journal
of Natural History 4: 511 (1846).
Type: A plant from the Garrow Hills, India; no specimen extant. Lectotype (designated by Kramer,
1967b): in W. Roxburgh, Icones Roxburghianae (K!).
Osmolindsaea japonica (Baker) Lehtonen & Christenh., comb. nov.
Basionym: Lindsaea cultrata (Willd.) Sw. var.
japonica Baker, Synopsis Filicum 1st ed. 105 (1868).
Synonym: Lindsaea japonica (Baker) Diels, Die
Natürlichen Pflanzenfamilien, I, 4: 221 (1899).
Lectotype (designated here): Japan, Nagasaki,
growing on large boulder in streams, Oldham 477
(upper plant), ex Herb. Hookerianum (K!, duplicates
K!, GH).
Note: Osmolindsaea japonica has usually been considered as a variety of L. odorata (Kramer, 1972b),
but it is clearly distinct both in morphological characters and based on the studied DNA sequences.
Osmolindsaea japonica has continuous sori, entire
pinnules, a large terminal segment and sparsely distributed, minute rhizome scales. In contrast, O.
odorata has interrupted sori, incised pinnules, gradually reduced upper pinnules and densely packed long
rhizome scales.
Distribution: Osmolindsaea is distributed from East
Africa and Madagascar through India and the Malay
Peninsula, north to Japan and Korea and east to the
Solomon Islands.
Notes: Lindsaea odorata Roxb. var. darjeelingensis
T.Sen & U.Sen is similar to O. odorata, but may prove
to be a different taxon. The Madagascan specimen
included in our study clearly represents an undescribed species, which differs from the other
Osmolindsaea spp. in having broad rhizome scales.
This species will be described in a more detailed
taxonomic revision of Osmolindsaea (S. Lehtonen, H.
Tuomisto, G. Rouhan, M. J. M. Christenhusz, unpubl.
data). Osmolindsaea spp. have a solenostele with an
internal sclerified pith, in contrast to Lindsaea spp.,
which have a protostele. Osmolindsaea japonica is
reported to have N ª 75 (Lin et al., 1990) and O.
odorata N = 150 (as L. cultrata, Manton & Sledge,
1954; Mehra & Khanna, 1959).
NESOLINDSAEA LEHTONEN & CHRISTENH.,
GEN. NOV.
Diagnosis: Genus novum Lindsaeae simile, a qua rhizomate solenostelam ferente differt; sporae triletae.
Synonym: Lindsaea Dryand. ex Sm. section Aulacorhachis K.U.Kramer
Typus generis: Nesolindsaea caudata (Hook.) Lehtonen & Christenh.
Distinction: Members of Nesolindsaea superficially
resemble typical Lindsaea. However, all Lindsaea
spp. have protosteles, whereas Nesolindsaea spp.
have solenosteles, which is a character they share
with Osmolindsaea (Fig. 16B). The spores of
Nesolindsaea are trilete, in contrast to the monolete
spores in Osmolindsaea, Xyropteris and Tapeinidium.
In the total evidence analysis, the genus is supported
by three orders of lamina veins (Table 4). The only
reported chromosome count is N = 82 for N. caudata
(Manton & Sledge, 1954).
Taxonomic history: All previous taxonomic works
have placed the two species of Nesolindsaea in the
genus Lindsaea. Kramer (1972a) discussed the affinity between these two species, but he placed them in
different sections on the basis of several distinguishing characters (interrupted vs. continuous sori, pubescent vs. glabrous axes and different insertion of
rhizome scales). Kramer (1972b) placed Lindsaea
caudata Hook. in the monotypic section Aulacorhachis. Kramer (1972a) placed Lindsaea kirkii Hook. in
section Temnolindsaea, but this section is based on L.
klotzschiana Moritz (= L. feei C.Chr.), which is a true
Lindsaea. The section name Aulacorhachis is not
used here at the generic level, because it refers to the
furrowed midrib of N. caudata, which is absent in N.
kirkii. Because both species are island endemics, we
chose the Greek name component ‘neso-’, meaning
island.
The following new combinations are proposed here:
Nesolindsaea caudata (Hook.) Lehtonen & Christenh., comb. nov.
Basionym: Lindsaea caudata Hook., Species Filicum,
ed. 1: 215 (1846).
Type: Ceylon, Adam’s Peak, Walker s.n. (holotype K!).
Nesolindsaea kirkii (Hook.) Lehtonen & Christenh., comb. nov.
Basionym: Lindsaea kirkii Hook., Synopsis Filicum,
ed. 1: 108 (1868).
Lectotype (designated here): Seychelles, 1862, Kirk
s.n. (K!, duplicate GH).
Distribution and biogeography: Nesolindsaea has a
highly restricted distribution, with N. caudata being
endemic to Sri Lanka and N. kirkii to the granitic
islands in the Seychelles. The long branches indicate
a great age for the separation of the two species. The
Seychelles are continental in origin and separated
from mainland India and Sri Lanka during the early
Tertiary (Chaubey et al., 1998). ‘Lemurian stepping
stones’ during the Eocene–Oligocene may explain the
biogeographical relationships between India, Sri
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PHYLOGENETICS OF LINDSAEACEAE
337
Lanka and Madagascar via the Seychelles (Schatz,
1996). Biogeographical links between India, Sri
Lanka and the Seychelles have been shown before in
various groups, including frogs (Biju & Bossuyt,
2003), Dillenia L. (Hoogland, 1952) and Nepenthes L.
(Meimberg et al., 2001), and we hereby provide a
novel example from the ferns. The illustration of
Nesolindsaea kirkii (as Lindsaya kirkii) from Baker
(1871–1875; Plate 28) is reproduced here as Fig. 17.
Taxonomic history: This monotypic genus has been
found in Borneo and Sumatra and is known from only
a few collections. The affinities of X. stortii have been
difficult to establish. It was first described as Schizoloma (Alderwerelt van Rosenburgh, 1914), which is
now a synonym of Lindsaea, but has also been
included in Tapeinidium (Copeland, 1929) and was
placed in its own genus by Kramer (1957b) on the
basis of a unique combination of characters.
TAPEINIDIUM (C.PRESL) C.CHR.
Notes: Unfortunately we failed in our attempts to
sequence this highly interesting species. Xyropteris
is simply pinnate and differs from Tapeinidium in
having continuous sori and large auricles at the
bases of pinnae. Kramer (1971a) considered the two
genera to be closely related. No chromosome counts
are available.
Basionym: Microlepia subgenus Tapeinidium C.Presl.
Synonym: Protolindsaya Copel.
Typus generis: Tapeinidium pinnatum (Cav.) C.Chr.
Taxonomic history: Tapeinidium was originally
described as an infrageneric taxon within Microlepia
(Presl, 1851), but was already treated as a genus by
Fée (1852), albeit with the incorrect name Wibelia.
Kramer (1967c) provided a taxonomic revision of the
genus.
Notes: Tapeinidium is a genus of approximately 18
species distributed from southern India to Samoa.
Our phylogenetic evidence strongly supports the
inclusion of Tapeinidium in Lindsaeaceae. This contrasts with the early molecular hypothesis of Wolf
(1995), which placed it in the dryopteroid clade. Our
circumscription of Tapeinidium includes the New
Caledonian endemic T. moorei. This species was considered to belong to Tapeinidium by Hieronymus
(1920), but Kramer (1967a) placed it in Lindsaea.
Stelar anatomy is variable in Tapeinidium: the large
species have a true solenostele (Kramer, 1971a), but
the smaller ones, for example T. moorei, have a protostele with an internal sclerotic strand near the leaf
bases (Kramer, 1967a). Tapeinidium species are characterized by uninerval (rarely binerval) sori and laterally quite adnate rigid indusia. In our total evidence
analysis, the genus was supported by equally sided
ultimate segments, connection of the segments and
coriaceous lamina (Table 4). Not all species, however,
have all these characters. More comprehensive sampling of Tapeinidium is desirable in the future, as we
were able to obtain molecular data from only ten
species. Cytology of the genus is not well known, but
N ª 150 has been reported for T. pinnatum (Lin et al.,
1990).
XYROPTERIS K.U.KRAMER
Typus
generis:
K.U.Kramer
Xyropteris
stortii
(Alderw.)
LINDSAEA DRYAND.
Synonyms: Guerinia J.Sm., Humblotiella Tardieu,
Isoloma J.Sm, Lindsaenium Fée, Odontoloma J.Sm.,
Ormoloma Maxon, Sambirania Tardieu, Schizolegnia
Alston, Schizoloma Gaudich., Synaphlebium J.Sm.
Typus generis: Lindsaea trapeziformis Dryand. =
Lindsaea lancea (L.) Bedd.
Taxonomic history: The genus Lindsaea was described
by Dryander (1797), who included 10 species in the
genus. More species were added by several workers
(e.g. Klotzsch, 1844; Fée, 1852). The genus name was
often incorrectly spelled Lindsaya until Copeland
(1947) restored the original spelling. Kramer (1957a,
1967b, 1971a, 1972a) was the first to provide a proper
revision of the genus and he broadened the circumscription of Lindsaea considerably. For example, he
(Kramer, 1967b, 1972a) placed Schizoloma, Isoloma,
Humblotiella and Sambirania as sections under
Lindsaea. Kramer (1957a, 1967b, 1971a, 1972a) proposed the subdivision of Lindsaea into two subgenera
and 23 sections and this has been followed by all later
workers (e.g. Walker, 1973; Tryon & Tryon, 1982).
The present paper is the first attempt to investigate
phylogenetic relationships among Lindsaea spp. in
detail. In the process, it has become obvious that the
varieties of some previously recognized species do not
form a monophyletic group. The following new combinations are therefore proposed:
Lindsaea pseudohemiptera (Alderw.) Lehtonen &
Tuomisto, comb. nov.
Basionym: Lindsaea repens var. pseudohemiptera
Alderw. Bulletin du Jardin Botanique de Buitenzorg,
III, 2: 157 (1920).
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338
S. LEHTONEN ET AL.
Figure 17. Nesolindsaea kirkii, reproduced from Baker (1871–1875).
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PHYLOGENETICS OF LINDSAEACEAE
Type: Sumatra, Mt. Merapi, Bünnemeijer 5419 (lectotype BO, isolectotypes L!, SING, U!, US!).
Lindsaea hainaniana (K.U.Kramer) Lehtonen &
Tuomisto, comb. nov.
Basionym: Lindsaea lobata Poiret var. hainaniana
K.U.Kramer, Gardens’ Bulletin, Singapore 26: 37
(1972).
Type: Hainan, Liang 63789 (holotype US!, isotype K!).
Lindsaea agatii (Brack.) Lehtonen & Tuomisto,
comb. nov.
Basionym: Schizoloma agatii Brack. in United States
Exploring Expedition. Botany. Cryptogamia. Filices
16: 216 (1854). Type: Fiji, U.S. Expl. Exped. s.n.
(holotype US!, isotypes K!, P, P00633682!).
Synonym: Lindsaea ensifolia Sw. ssp. agatii (Brack.)
K.U.Kramer
Kramer (1967b) described a new species, L.
sarawakensis K.U.Kramer and considered the earlier
names L. diplosora Alderw. and L. diplosora Alderw.
var. acrosora C.Chr. as synonyms of L. rigida J.Sm.
(Kramer, 1971a). In our opinion L. rigida and L.
diplosora are distinct taxa, but L. sarawakensis is
conspecific with L. diplosora. Furthermore, we do not
give L. diplosora var. acrosora a distinct taxonomic
status. Consequently, we accept Lindsaea diplosora
Alderw. (holotype: Matthew 523 BO, photograph in
AAU!) as a species with the heterotypic synonyms
Lindsaea sarawakensis K.U.Kramer (holotype:
Mjöberg 9, P!) and Lindsaea diplosora Alderw. var.
acrosora C.Chr. (lectotype (designated here): Mjöberg
94, S!, duplicate BM!).
Lindsaea lapeyrousei (Hook.) Baker was originally
described based on two samples: one from Vanikoro in
the Solomon Islands (Moore s.n., K) and one from Fiji
(Milne s.n., K). Kramer labelled the Moore specimen as
‘holotype’ and the Milne specimen as ‘paratype’, but
they are both syntypes. The latter was then placed into
Kramer’s L. lapeyrousei ssp. fijiensis K.U.Kramer
(type: Fiji, Degener & Ordonez 13734a, holotype L,
isotypes MICH, BISH, GH, K). The lectotype of L.
lapeyrousei (designated here) is ‘Vaniholla’, C. Moore
s.n. (K!), and we place all samples from the Solomon
islands and Fiji under this (including L. lapeyrousei
ssp. fijiensis and L. kajewskii Copel.). The name
honours French explorer Jean-François de La Pérouse,
who was shipwrecked in Vanikoro in 1788, and is
correctly cited as L. lapeyrousei, instead of L. lapeyrousii (article 60.7 of the ICBN; McNeill et al., 2006).
Notes: Lindsaea is a pantropical genus of approximately 150 species, some of which extend to the
subtropics in Japan, Australia and New Zealand. The
monophyly of Lindsaea (as circumscribed here) was
supported in all our analyses. Kramer (1957a) defined
Lindsaea as having laterally free indusia, but this
character is variable. Several Lindsaea spp. have
339
laterally adnate indusia and laterally free indusia are
not restricted to Lindsaea either. In the total evidence
analysis, Lindsaea was supported by short petioles,
abaxially keeled rachises, broad rachis sulcation and
twice-ordered laminar venation (Table 4). However,
none of these characters is present in all Lindsaea
spp. and some are not even the prevailing characters
in the genus. Neither of the subgenera defined by
Kramer (1967b) is monophyletic in our analyses.
Species placed in subgenus Odontoloma were resolved
in clades V, VI and IX, thus also rendering subgenus
Lindsaea paraphyletic. Consequently, we do not recognize the subgeneric classification. Most of the proposed sections within Lindsaea are not monophyletic
and those which are monophyletic are embedded
within other sections. Therefore, we do not recognize
the sections either. Instead of presenting a new
formal subgeneric classification here, we will discuss
the phylogenetic lineages within Lindsaea by using
informal clades numbered from I to XIII.
SUBDIVISION OF LINDSAEA
CLADE I
This clade consists of the Central American L. seemannii J.Sm. and L. pratensis Maxon and is well
supported and highly stable in the molecular, morphological and combined analyses. Both species
belong to Kramer’s (1957a) section Tropidolindsaea,
but we failed to sample another two species of the
section. The Caribbean L. protensa C.Chr. is probably
a member of clade I, but L. adiantoides J.Sm. from
the Philippines is more likely to belong to our clade II.
Kramer (1957a, 1971a) correctly suggested that these
species are isolated within the genus. Members of
clade I resemble the species in clade II in having a
keeled rachis and clustered fronds. Spores are monolete in clade I, whereas most species of clade II have
trilete spores. There are no chromosome counts available for clade I.
CLADE II
This well-supported clade includes all species of Kramer’s (1967b) section Isoloma (sometimes treated as a
distinct genus), but also L. viridis Col. (of the monotypic section Chlorolindsaea; Kramer & Tindale, 1976)
and L. plicata Baker (the only member of section
Sambirania that we were able to sample; Kramer,
1972a). The clade is found in Madagascar and New
Zealand and from Malesia to western Polynesia.
Common morphological characters in this clade are
keeled rachises, clustered fronds and dark axes. Most
of the species have non-dimidiate and basally auriculate pinnules, but L. viridis and L. plicata have deeply
dissected pinnules. Spores are trilete, except in L.
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340
S. LEHTONEN ET AL.
viridis, in which they are monolete. The studied
sequences are highly divergent within the clade, suggesting a great age for the divergences. Lindsaea
gueriniana (Gaudich.) Desv. and L. pellaeiformis
Christ were not resolved as sister species despite their
morphological similarity. We were unable to sequence
two species of section Isoloma that most likely belong
to this clade: L. ovata J.Sm. and L. philippinensis
K.U.Kramer. The latter, however, seems morphologically indistinguishable from L. jamesonioides Baker
and probably should be considered synonymous with
that species. The only available chromosome count for
clade II is N = 88 for L. viridis (Brownlie, 1961).
Kramer (1970) divided L. lapeyrousei into two subspecies, with the specimens from Fiji placed in ssp.
fijiensis. The subspecies are recognized by slight differences in pinnule segmentation and in the distance
between the indusium and the pinnule margin.
However, the morphological variation is overlapping
and we found no differences in the DNA sequences of
the specimens sampled. Hence the recognition of two
subspecies seems unnecessary.
The available chromosome counts for clade IV are
N = 47 for both L. brachypoda (Baker) Salomon (as L.
concinna, Kramer, 1957a) and L. lucida (Mitui, 1976).
CLADE V
CLADE III
This clade only includes L. incisa Prent., an endemic
species from eastern Australia. Kramer & Tindale
(1976) suggested that L. microphylla Sw., L. linearis
Sw. and L. dimorpha F.M.Bailey (not included in our
study) could be the closest relatives of L. incisa.
Indeed, L. linearis and L. microphylla are resolved as
a clade, but without close affinity with L. incisa. In
the molecular tree, L. incisa is resolved as sister to
the clade [IV (V VI)], but the combined analysis
placed it as sister to clades IV–XIII. The position in
the molecular tree is quite unstable and lacks
support, but the more isolated phylogenetic position
in the combined analysis is rather stable and well
supported. Lindsaea incisa has trilete spores. No
chromosome counts are available.
CLADE IV
This clade and the phylogenetic relationships within
it are well supported and mostly stable in the molecular and the combined analyses. With the exclusion of
L. kingii Copel., this clade was also resolved in the
morphological analysis.
Kramer (1971a) treated L. brevipes Copel. as a
subspecies of L. lucida Blume and Kramer (1970)
suggested that both, especially ssp. brevipes, are
closely related with L. lapeyrousei (Hook.) Baker. This
hypothesis is supported by our analyses, as L. brevipes was resolved as sister to L. lapeyrousei, and these
two together as sister to L. lucida. As the two proposed subspecies of L. lucida did not form a monophyletic group in any of our analyses, we recognize
them as separate species. Lindsaea brevipes usually
has short petioles and more deeply incised and
smaller pinnules than L. lucida, but the exact boundary between the two is fuzzy. According to the literature, L. brevipes occurs only in eastern Malesia but L.
lucida is distributed from Malesia to the Himalayas;
L. lapeyrousei is confined to the Bismarck Archipelago, the Santa Cruz (Solomon) Islands and Fiji.
The species in clade V are epiphytes and thus form an
unusual group within the predominantly terrestrial
Lindsaea. The monophyly of the group is well supported and highly stable in the molecular analysis,
although less so in the combined analysis.
Lindsaea repens (Bory) Thwaites sensu Kramer
(1971a) was not supported as a monophyletic entity in
our analyses. Out of the 11 varieties (Kramer, 1967b,
1970, 1971a), we were able to sequence three: var.
pectinata (Blume) Mett. ex Kuhn, var. sessilis (Copel.)
K.U.Kramer and var. pseudohemiptera Alderw. We
accept these varieties as distinct species and we
assume that many of the unsampled varieties should
also have a status at the species level. In the combined analysis, L. pectinata Blume was resolved as
the sister of L. oblanceolata Alderw. with high
support and low stability, but in the molecular analysis they were poorly supported and of unstable
successive lineages. Nevertheless, these two species
are morphologically highly similar with somewhat
rounded and only shallowly incised pinnules and typically plurinerval sori. Lindsaea pectinata and L.
oblanceolata have widely overlapping distribution in
Malesia and Thailand. They can be distinguished by
L. pectinata having much shorter sori and pinnules
with numerous shallow incisions, in contrast to L.
oblanceolata, which has only a few shallow incisions
and irregularly interrupted sori. Lindsaea sessilis
Copel. was resolved as sister to Lindsaea sp. 1, both
in the molecular and the combined analyses.
Lindsaea sp. 1 may represent an undescribed
species, as we were unable to mach it with any
species description. It has pinnules quite similar to
those of L. sessilis, but differs from that species in
having long petioles and bipinnate fronds. The specimen Cicuzza 891 (Z!) was originally identified as L.
microstegia Copel., but it clearly differs from that
species in pinnule shape. Lindsaea sessilis differs
from the other species by having relatively narrow
incisions in pinnules and reniform indusia. Lindsaea
pseudohemiptera has irregularly incised pinnules,
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PHYLOGENETICS OF LINDSAEACEAE
with the incisions being quite deep, especially
towards the pinnule apices. In this character, it
resembles its closest relative, L. carvifolia
K.U.Kramer, which also has deeply incised pinnules.
Apparently juvenile plants of this clade often have
deeply incised pinnules and the repeated evolution of
deeply incised adult forms can be explained as convergent retention of juvenile traits (paedomorphosis).
Another species with deeply incised pinnules is L.
fissa Copel. The specimen we sampled for molecular
analysis was, however, sterile and had juvenile fronds
only. Its species identification is thus uncertain, but
the specimen is morphologically identical to juvenile
leaves of typical L. fissa. In the molecular analysis, L.
cf. fissa was resolved as sister to L. merrillii Copel.
ssp. yaeyamensis (Tagawa) K.U.Kramer, but the combined analysis resolved L. merrillii ssp. yaeyamensis
as sister to L. merrillii ssp. merrillii. Because of these
conflicting results and uncertain identification of the
specimen representing L. fissa, we accept Kramer’s
(1972b) subspecific ranks for L. merrillii for the time
being.
The chromosome numbers N ª 44 (L. sessilis;
Walker in Kramer, 1971a) and N ª 47 (L. doryphora
and L. pectinata; Kramer, 1957a) have been reported
for members of clade V.
CLADE VI
This clade is composed of both terrestrial and epiphytic groups and was resolved as well supported,
but rather unstable sister to the purely epiphytic
clade V. Also the phylogenetic relationships within
the clade are mostly unstable and some groupings
were differently resolved in the molecular and the
combined analyses. The first diverging lineage
within this clade is, however, well supported and
highly stable. This lineage contains L. diplosora
Alderw. (= L. sarawakensis) from Borneo, L. sp. 2
from Sulawesi, L. rigida J.Sm. from Malesia and L.
monocarpa Rosenst. from New Guinea. All these
species have apically located sori. Lindsaea rigida
and L. monocarpa have coriaceous pinnules, but can
be separated because L. monocarpa has almost
entire pinnules, hidden veins and a single apical
sorus, whereas L. rigida has dentate–crenate pinnules, elevated veins and 1–4 sori per pinnule.
Lindsaea diplosora and L. sp. 2 have herbaceous
pinnules. Pinnules are less incised, more dense and
inserted to the rachis at a more acute angle in L.
diplosora than in L. sp. 2. Although the node separating L. diplosora and L. sp. 2 is well supported
and highly stable, it may represent an incongruence
between gene and species trees. Hence, further sampling is desirable before formal taxonomic actions
are taken. In addition to the voucher specimens
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mentioned in Table 2, L. diplosora is represented by
Chew 1811 (K!) and Parris 11612 (L!), L. rigida by
Anderson 2815 (MO!), Fallen 439 (MO!), Parris 6026
(K!) and Richards 1703 (K!) and L. sp. 2 by Kluge
7248 (GOET!).
The next diverging lineage is composed of three
species: L. propinqua Hook. and L. pacifica
K.U.Kramer from the Pacific islands and L. azurea
Christ from Malesia. Of these species, L. propinqua is
morphologically highly variable across its wide range
and may actually include several species.
The next diverging lineage corresponds with the
section Penna-arborea, one of the few sections supported as a monophyletic entity. All the species of this
clade typically grow as epiphytes. We found L.
pulchra (Brack.) Carruthers ex Seem. sensu Kramer
(1970) to be polyphyletic. Kramer (1970) himself
noted that specimens from the Bismarck Archipelago
and Solomon Islands have unusually large pinnules
and we recognize them as L. stolonifera Mett. ex
Kuhn. In the molecular analysis, this species was
resolved as sister to L. pulchella (J.Sm.) Mett. ex
Kuhn, but in the combined analysis as sister to L.
chrysolepis K.U.Kramer. Lindsaea blanda Mett. ex
Kuhn was treated as a variety of L. pulchella by
Kramer (1971a), but is recognized here as a separate
species.
The remaining species are terrestrial and form a
clade with L. parallelogramma Alderw. as the first
branching species. Lindsaea tenuifolia Blume, L.
polyctena K.U.Kramer, L. multisora Alderw., L. tetragona K.U.Kramer and L. longifolia Copel. form a
clade with slightly different internal relationships
between the molecular and the combined trees. In the
combined analysis, L. tenuifolia and L. polyctena are
resolved as sisters, with high support and stability, in
contrast to their highly unstable position as successive lineages in the molecular analysis. A sister group
relationship is supported by the fact that these two
species share a unique 4-bp inversion in the trnL-trnF
intergenic spacer region. We found L. lobata Poiret
sensu Kramer (1972b) to be polyphyletic and correspondingly recognize his var. hainaniana at the
species level as L. hainaniana. Lindsaea cultrata
(Willd.) Sw. and L. integra Holtt. are often confused,
but L. cultrata is generally larger, often bipinnate,
has some incisions in the upper margin of the pinnules and has pinnules more than twice as long as
broad. Lindsaea integra, however, is generally
smaller, simply pinnate and has almost entire pinnules that are relatively broader than in L. cultrata
and, at most, twice as long as broad. Lindsaea cultrata has also often been confused with Osmolindsaea
odorata (Kramer, 1967b). This explains the observations of a solenostelic rhizome in L. cultrata (GwynneVaughan, 1903; Barcelona, 2000), which actually has
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S. LEHTONEN ET AL.
a protostele in contrast to a solenostele in Osmolindsaea. According to the available cytological studies, L.
parallelogramma and L. integra (‘L. nitida’) have
N = 47 (Kramer, 1957a), L. blanda has N = 44–45
(Walker in Kramer, 1971a) and L. obtusa J.Sm. ex
Hook. has N ª 50 or 100 (Holttum, 1954).
CLADE VII
Lindsaea microphylla and L. linearis formed a wellsupported clade that was also stable in the molecular
analysis. This clade probably also includes L. dimorpha, although we were unable to obtain any
sequences from this species. All the species occur in
Australia, but L. linearis extends to New Caledonia,
Norfolk Island and New Zealand (Kramer & Tindale,
1976) and L. dimorpha extends to New Caledonia
(Kramer, 1967a). Both L. linearis and L. dimorpha
are dimorphic with dissimilar sterile and fertile
fronds, which is unusual in Lindsaea. Lindsaea
microphylla is not as clearly dimorphic, but its sterile
fronds typically have larger segments than those in
fertile fronds and sterile fronds usually persist in
fertile plants (Kramer & Tindale, 1976). This clade
appears to be distinct also cytologically, as the available chromosome count N = 34 for L. linearis (Brownlie, 1958) is unique in the genus.
CLADE VIII
Clades VIII and IX together roughly correspond to
section Schizoloma. Lindsaea vieillardii Mett., a New
Caledonian endemic, was resolved as the first diverging lineage of clade VIII in the molecular analysis,
but as the first diverging lineage of clade IX in the
combined analysis. In both analyses the position of
this species was unstable and lacked jackknife
support. The rest of clade VIII is more stable and
more strongly supported. Lindsaea schizophylla
(Baker) Christ is endemic to Sri Lanka. We sequenced
two specimens originally identified as this species and
they were resolved as sisters. However, only one of
them has the deeply dissected pinnules and rather
short rhizomes typical of L. schizophylla. The other
specimen (Laegaard 13835 AAU!) has long rhizomes
and only slightly incised, flabellate pinnules and
apparently represents an unknown species (L. sp. 3).
Lindsaea bouillodii Christ was resolved as sister to L.
cf. cambodgensis Christ. However, the latter specimen
has much larger pinnules than typical L. cambodgensis and may actually represent another species.
Molecular data alone were insufficient to resolve
the relationships of six apparently closely related
species: L. grandiareolata (Bonap.) K.U.Kramer from
Madagascar, L. dissectiformis Ching from Vietnam
and Hainan, L. chienii Ching from Japan to Thailand,
L. annamensis K.U.Kramer from Vietnam, L. kawabatae Kurata from Japan and L. austrosinica Ching
from South China and Indo-China. Lindsaea grandiareolata is morphologically the most distinct. It has
lanceolate pinnules and anastomosing veins, unlike
any other species in the group. The other species are
more homogeneous and their status as separate
species has been questioned. The main distinctive
characters are in the dissection of the lamina. Kramer
(1972b) suggested that L. dissectiformis and L. kawabatae may be conspecific, and Dong & Zhang (2006)
considered L. annamensis as a synonym of L. chienii
but accepted L. dissectiformis as a distinct species. In
our opinion, L. annamensis and L. chienii are distinct
and for the moment we accept all the species accepted
by Kramer (1972b). Dong & Zhang (2006) used the
name L. eberhardtii (Christ) K.U.Kramer, but, as
explained by Kramer (1972b), the basionym Stenoloma eberhardtii is a nomen nudum and the correct
name for this species is L. dissectiformis.
The available chromosome counts are N ª 47 for
both L. chienii (Kurita & Nishida, 1963) and L. vieillardii (Brownlie, 1965), although the latter species
may belong to clade IX.
CLADE IX
This clade received poor support and was unstable
and the position of L. vieillardii as the first diverging
lineage in the combined analysis is questionable. The
clade as a whole is distributed widely around the
Indian Ocean and the Pacific. The Madagascan
species were grouped together in the combined analysis, but L. oxyphylla Baker was excluded from this
group in the molecular analysis. The species of clade
IX usually have equilateral pinnae or undivided
pinna apices.
Lindsaea ensifolia Sw. and L. heterophylla Dryand.
have presented taxonomic problems because of their
great morphological variation (Dixit & Ghosh, 1980,
1983). High chromosome numbers have been reported
for L. ensifolia (N = 88; Manton & Sledge, 1954),
indicating that polyploidy may have been involved in
the evolution of this complex. Hybrid origin of L.
heterophylla has also been suggested; the species is
reported to often have irregularly shaped and abortive spores (Kramer, 1971a). The specimen included
in our analyses had both GA- and CT-type (Lehtonen
et al., 2009) loop regions of the trnL-trnF stem-loop
structure, which must mean that either the specimen
has two types of plastid genomes, or the inversion has
occurred in a somatic cell. In comparison, the CT-type
inversion was found in L. ensifolia and the GA-type in
L. agatii. This species complex also includes several
taxa that we were not able to include in our analyses:
L. ensifolia ssp. coriacea (Alderw.) K.U.Kramer, L.
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PHYLOGENETICS OF LINDSAEACEAE
rutlandica R.D.Dixit & B.Ghosh and L. beddomei
R.D.Dixit & B.Ghosh. The latter two taxa were not
accepted by Fraser-Jenkins (2008), who considered L.
beddomei conspecific with L. heterophylla and L. rutlandica conspecific with L. walkerae Hook. We have
not been able to study the type specimens of these
taxa. Lindsaea fraseri Hook. and L. media R.Br. are
also problematic species that require further study.
Kramer & Tindale (1976) found only abortive spores
in L. fraseri and speculated that this species may be
a hybrid between L. media and L. agatii. We found no
direct evidence of hybrid origin, but almost identical
sequences of L. media and L. fraseri suggest a close
affinity between these two species.
The Madagascan species formed a monophyletic
clade both in the molecular and combined analyses,
with the latter receiving higher jackknife support and
stability. In both analyses, L. madagascariensis
Baker and L. leptophylla Baker were resolved as
sister species, as were L. goudotiana (Kunze) Mett. ex
Kuhn and L. subtilis K.U.Kramer. Although L. blotiana K.U.Kramer and L. millefolia K.U.Kramer are
morphologically distinct, with the pinnules of L. blotiana being clearly less divided, the two had no variation in the studied sequences. The finely dissected
pinnules of L. millefolia give the species an appearance similar to the unrelated L. dissectiformis of clade
VIII, L. bifida of clade XI and L. sphenomeridopsis of
clade XIII.
CLADE X
This clade was rather unstable and not well supported in our molecular analysis, but in the combined
analysis both support and stability measures were
higher. The close relationship among these species
had already been suggested by Kramer (1967a) and
Kramer & Tindale (1976). Clade X is biogeographically well defined, with three species endemic to New
Caledonia (L. rufa K.U.Kramer, L. nervosa Mett. and
L. prolongata E.Fourn.) and one distributed in New
Zealand, Australia and Tasmania (L. trichomanoides
Dryand.). We found no differences in the studied
sequences between L. rufa and L. trichomanoides,
which suggests a recent divergence of these species
(for a recent discussion of New Caledonian biogeography, see Grandcolas et al., 2008; Heads, 2008).
Lindsaea rufa and L. trichomanoides are morphologically very similar, but the former is more robust.
The molecular analysis was unable to resolve the
branching order of clades VII (VIII IX), X and [XI (XII
XIII)]. In the combined analysis, clade X was resolved
as the sister to the South American clade [XI (XII
XIII)], although with low stability and no support.
Available chromosome numbers in this clade are
N = 42 for L. trichomanoides (as L. cuneata, Brownlie,
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1957) and N ª 40 for L. prolongata (Brownlie, 1965).
Similar chromosome numbers have only been
reported from Neotropical Lindsaea, supporting the
sister relationship as recognized in the combined
analysis.
CLADE XI
This well-supported but relatively unstable clade is
composed of species endemic to the Atlantic coastal
rain forests of Brazil (Mata Atlântica). The studied
sequences of Lindsaea bifida (Kaulf.) Mett. ex Kuhn
were barely different from those of L. virescens Sw.
and a second well-supported and stable sister species
pair was L. ovoidea Fée with L. botrychioides A.St.Hil. Both Lindsaea virescens and L. bifida have finely
dissected laminas, whereas L. ovoidea and L. botrychioides have more or less flabellate pinnules. Lindsaea bifida is morphologically almost inseparable
from L. sphenomeridopsis K.U.Kramer from the
Guyana shield and Kramer (1957a) considered the
two closely allied. However, our analyses resolved L.
sphenomeridopsis to clade XIII. No chromosome
counts are available for clade XI.
CLADE XII
Ormoloma has been considered a separate genus but
a close relative of Lindsaea (Kramer, 1957a). All of
our analyses resolve Ormoloma to be deeply nested
within Lindsaea, although its position within the
genus is unstable. Ormoloma is divergent both morphologically and based on the sequence data, and low
stability suggests possible issues caused by these long
branches. However, cytological studies of Lindsaeaceae have reported N = 42 only from Ormoloma
(Wagner, 1980) and some members of clades X and
XIII. The phylogenetic position of the Caribbean
Ormoloma within the Neotropical Lindsaea clade is
also biogeographically reasonable. However, additional sampling of more conservative loci is needed to
confirm the placement of Ormoloma. Two species
have been recognized, but their status as distinct
species was already rejected by Tryon & Tryon (1982).
We were unable to find any constant morphological or
molecular differences between the two proposed
species and consequently accept only Lindsaea
imrayana (Hook.) Perez.
CLADE XIII
This large clade is well supported but rather unstable
and includes only Neotropical species. Although some
groups within the clade are morphologically clearly
distinct, we found practically no variation among the
species at the sequence level. Hence, the topology
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S. LEHTONEN ET AL.
within the clade is poorly supported and highly
unstable and only a few observations are worth
making.
Both the molecular and combined analyses resolved
Lindsaea feei C.Chr. from northern South America as
sister to the rest of clade XIII (this species was called
L. klotzschiana Moritz by Kramer, 1957a; for a discussion on the nomenclature, see Morton, 1967).
Lindsaea pendula Klotzsch and L. meifolia (Kunth)
Mett. are morphologically unique within the genus in
having pendulous segments and they are resolved as
sister species in all analyses, with full stability. One
larger monophyletic group, which includes species
from L. cyclophylla K.U.Kramer to L. arcuata Kunze,
is recognized in both the molecular and the combined
analysis with high support and, in the case of the
molecular analysis, with high stability as well.
However, this clade includes L. cyclophylla but
excludes the two other species of Kramer’s (1957a)
section Haplolindsaea, namely L. sagittata (Aublet)
Dryand. and L. reniformis Dryand. All three species
are morphologically similar with a simple lamina.
The polyphyletic origin of Haplolindsaea is unexpected, although the different spore architecture of L.
cyclophylla (monolete spores in contrast with trilete
spores in L. sagittata and L. reniformis) may be a
morphological indication of this.
Our sampling included all three varieties of L.
stricta accepted by Kramer (1957a) and we failed to
resolve them as a monophyletic group. Several other
species were also not supported as monophyletic entities; these include L. portoricensis Desv., L. rigidiuscula Lindm. and L. lancea (L.) Bedd. In the case of L.
lancea, the non-monophyletic origin was expected on
the basis of the great morphological differences
between the varieties. We follow our earlier justification (Tuomisto, 1998) and treat L. falcata Dryand. as
a full species instead of a variety under L. lancea,
contrary to Rosenstock (1906) and Kramer (1957a).
Species of clade XIII have apparently diverged
recently. As we only used plastid sequences, hybridization and incomplete lineage sorting because of
retained ancient polymorphisms may have confused
the phylogenetic inference (Maddison & Knowles,
2006). The presence of polyploidy within the clade
also suggests that hybridization may have taken
place. Available chromosome counts are N = 42 for L.
divaricata Klotzsch and L. falcata (Tryon, Bautista &
da Silva Araújo, 1975), N = 84 for L. schomburgkii
Klotzsch (Tryon et al., 1975), N = 88 for L. portoricensis (Walker, 1966) and either N ª 84 or N ª 88 for L.
arcuata (Mickel et al., 1966; Smith & Mickel, 1977)
and L. quadrangularis Raddi (Tryon et al., 1975).
More detailed studies using multiple rapidly evolving
nuclear markers are needed to solve the taxonomic
problems within the clade.
EVOLUTIONARY RELATIONSHIPS WITHIN
THE LINDSAEOIDS
Based on our phylogenetic analyses, the first lineage
to diverge from the lindsaeoid stock is Sphenomeris
clavata. Its branch is long and located near the root,
thus raising concerns of long-branch attraction (Bergsten, 2005). The node combines 100% jackknife
support with low stability, which can be an indication
of long-branch problems (Giribet, 2003). Further sampling of more conservative genes is needed to verify
the phylogenetic position of Sphenomeris.
The next diverging lineage is Odontosoria, which is
here circumscribed such that it also includes all the
sampled species of Sphenomeris, except S. clavata.
The clade is pantropical, but the Neotropical species
form a monophyletic and strongly supported group
nested within it (96% jackknife support in morphological analysis, 100% support and high stability in
molecular and combined analyses). All the Neotropical species are climbers and they share several morphological synapomorphies (scrambling fronds with
indeterminate growth, flexuose rachises, opposite and
reflexed pinnae and large spores; Table 4).
An early study based on rbcL sequences (Wolf, 1995)
suggested that Tapeinidium should be excluded from
Lindsaeaceae, but this result must have been based on
erroneous identification or sample contamination; the
position of Saccoloma in that study was also problematic. In our study, Tapeinidium forms a clade with
several curious species that have traditionally been
placed in Lindsaea, but which we place in the new
genera Osmolindsaea and Nesolindsaea. This clade is
Palaeotropical, with a centre of diversity in Melanesia.
It is separated from Lindsaea by a long, well-supported
and highly stable branch. The sister relationship
between Lindsaea and (Tapeinidium (Nesolindsaea
Osmolindsaea)) clade obtains high jackknife support
(99%), but only 3/16 stability in the combined analysis.
The sister relationship (Odontosoria Lindsaea) actually obtains higher stability (5/16), but did not emerge
in the equal-cost regime favoured by us.
The monophyly of a strictly defined Lindsaea is well
established with 100% jackknife support in the
molecular and combined analyses. The morphological
analysis resolved the clade as well, but without jackknife support. The clade is stable in the combined
analysis (13/16), but less so in the molecular analysis
(8/16). The monophyletic Lindsaea also includes
Ormoloma, an enigmatic Neotropical group previously recognized as a separate genus.
EVOLUTION OF MORPHOLOGICAL AND
ANATOMICAL CHARACTERS
The ‘Lindsaea-type’ protostele (Fig. 16C) is present in
all Lindsaea and Sphenomeris, and in some Tapein-
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
PHYLOGENETICS OF LINDSAEACEAE
idium and Odontosoria, but is unknown among adult
members of other ferns (Kramer, 1957a). Nesolindsaea and most Odontosoria have solenosteles. The
stelar anatomy of Osmolindsaea and most Tapeinidium may be considered intermediate, as internal
sclerified pith is typically present at least near the
frond bases. Kramer & Green (1990) considered solenostele as the primitive state in lindsaeoids, from
which protostele was derived by simplification. The
protostele is clearly a derived state within Polypodiales (Wolf, 1995), but as it is present in both Lindsaea
and Sphenomeris, character optimization of stelar
anatomy remains ambiguous for the common ancestor
of lindsaeoids.
Some Lindsaea spp. (e.g. L. bifida, L. sphenomeridopsis, L. millefolia, L. dissectiformis) have highly
dissected leaves similar to those of species in several
other lindsaeoid genera. Kramer (1957a) therefore
considered high degree of leaf dissection to be a
primitive character. However, our analyses suggest
that the common ancestor of modern Lindsaea had
erose–crenate pinnule margins and that both the
entire and the highly dissected pinnule forms have
evolved independently several times. Early Lindsaea
probably had once pinnate leaves, from which bipinnate leaves have evolved several times with many
reversals back to the once pinnate form. Large terminal pinnule appears to have evolved multiple times
from the more primitive state of reduced distal pinnules. Most species of Lindsaeaceae have free veins,
but anastomosing veins prevail in clade VI and may
be a synapomorphy of this lineage, although with
some reversals to free venation. Anastomosing veins
also occur in several species of clades VIII and IX and
several independent origins of vein fusion must be
assumed.
The coenosorus appears to be derived from the
uni-binerval sorus, in accordance with Kramer’s
(1957a) hypothesis. However, continuous sori have
evolved separately in Nesolindsaea, Osmolindsaea,
Lindsaea and, possibly, Xyropteris (the phylogenetic
position of which remains unknown). The coenosorus
is present among the earliest lineages of Lindsaea,
although it is most common in the derived clade
XIII. A narrow indusium is a derived character, as
already assumed by Kramer (1957a), with multiple
independent origins. Just like the evolution of
laminar architecture, the evolution of sorus
structure is also confounded by convergence and
reversals.
Monolete spores have been derived from trilete
ancestors more than once within Lindsaeaeae.
However, it is not clear whether the common ancestor
of modern Lindsaea had monolete or trilete spores.
Tapeinidium and Osmolindsaea have monolete
spores, but Nesolindsaea, Sphenomeris and most
345
Odontosoria have trilete spores. One transformation
from trilete to monolete type must be assumed in
Odontosoria. All species of Lindsaea clade I have
monolete spores, as does L. viridis of clade II. Trilete
spores are optimized for the common ancestor of
Lindsaea clades II–XIII. Therefore, monolete and
trilete spores can be equally parsimoniously assumed
to represent the ancestral state for Lindsaea. In the
combined analysis, L. viridis was resolved as the first
branching species of clade II, but in the molecular
analysis it was more derived. If the former is correct,
the monolete spores of clade I and L. viridis can be
considered homologous (although it would still be
equally parsimonious to assume independent evolution from a trilete ancestor). Apart from these clades,
monolete spores in Lindsaea are restricted to a few
species of clade XIII. These species do not form a
monophyletic group in our analyses, thus suggesting
at least two independent origins of monolete spores
within clade XIII.
Species of Lindsaeaceae are typically terrestrial,
but epiphytism occurs in two groups within Lindsaea.
Clade V is predominantly epiphytic and several epiphytic species form a monophyletic group within clade
VI. These two occurrences are most parsimoniously
explained as independent origins of epiphytism, but
the origin in closely related groups may indicate that
some preadaptations to epiphytic habit were already
present in their common ancestor. We failed to sample
L. odontolabia (Baker) K.U.Kramer, an epiphytic
species endemic to Madagascar, which may be a
member of clade IX. In any case, epiphytism is a
derived character in the family, as suggested by previous authors (Copeland, 1947; Kramer, 1971a),
although the fossilized roots of a lindsaeoid fern
dating to the Early Cretaceous were growing epiphytically on a tree fern trunk (Schneider & Kenrick,
2001). Pryer et al. (2004) used this fossil to constrain
the minimum age of Lindsaeaceae in their estimation
of leptosporangiate divergence times. On the one
hand, if the fossil taxon is a member of an extant
epiphytic Lindsaea clade, rather than some now
extinct epiphytic lineage, this may have led to serious
underestimation of the family age. On the other hand,
several terrestrial Lindsaea spp. can occasionally
grow as epiphytes on the lower parts of tree fern
trunks. Another possible calibration point for the
molecular clock is provided by fossil Lindsaea spores
from Upper Miocene deposits in New Zealand
(Mildenhall, 1980). There are only three extant Lindsaea spp. in New Zealand (L. viridis, L. trichomanoides, L. linearis; Kramer & Tindale, 1976) and each
of them belongs to a different clade. If the fossil
spores could be associated with a modern species, a
more exact dating of the Lindsaea clades might be
possible.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
346
S. LEHTONEN ET AL.
ACKNOWLEDGEMENTS
We thank Michael Kessler and Michel Boudrie for the
plant material they kindly provided for our project,
Veikko Rinne for taking the cross-section images of
rhizomes and anonymous reviewers for their constructive comments on the earlier version of the
manuscript. We are grateful to the curators of AAU,
BISH, BM, CAY, KYO, L, MO, P, TUR, U, US and Z
for allowing their specimens to be destructively
sampled for the molecular study and to the curators
of K, MICH, NSW and UC for providing digital
images or material on loan. The Willi Hennig Society
is acknowledged for making TNT publicly available.
This study was funded by a grant from the Academy
of Finland to H.T. and by grants from the Kone
Foundation and the Oskar Öflund Foundation to S.L.
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APPENDIX 1
Morphological characters.
ROOTS
0. ANATOMY: (0) Dennstaedtia-type; (1) Lonchitistype; (2) Osmunda-type; (3) Lindsaea-type. Character state descriptions follow Schneider (1996).
RHIZOMES
1. HABIT: (0) short; (1) long. This character is modified from character 1 of Barcelona (2000).
2. RHIZOME SYMMETRY: (0) radial; (1) dorsiventral. This character corresponds to character 26 of
Pryer et al. (1995).
3. MATURE RHIZOME STELE TYPE: (0) protostele;
(1) solenostele; (2) dictyostele. This character corresponds to character 27 of Pryer et al. (1995).
4. XYLEM WIDTH: (0) < 1/3 of rhizome diameter; (1)
! 1/2 of rhizome diameter.
5. LEAVES ISSUING AT: (0) right angle; (1) acute
angle.
6. DIAMETER: (0) < 5 mm; (1) > 1 cm. This character
is modified from character 4 of Barcelona (2000).
INDUMENT
7. INDUMENT, ATTACHMENT: (0) normal; (1)
inserted on mounds.
8. INDUMENT, NUMBER OF CELL SERIES AT
THE BASE: (0) one; (1) 2 or 3; (2) 4–10; (3) > 10.
This character is modified from character 18 of
Barcelona (2000).
9. INDUMENT, LENGTH: (0) < 2.5 mm; (1)
> 2.5 mm.
11. ARCHITECTURE: (0) determinate; (1) indeterminate. This character corresponds to character
20 of Barcelona (2000).
STIPES
12. SHAPE IN CROSS SECTION: (0) subterete; (1)
triangular; (2) quadrangular. This character corresponds to character 23 of Barcelona (2000).
13. NUMBER OF VASCULAR BUNDLES: (0) two–
many; (1) single. This character is modified from
character 28 of Barcelona (2000).
14. WINGS: (0) absent; (1) present.
15. LENGTH: (0) short, < 1/4 of the lamina; (1) long,
! 1/2 of the lamina. This character is modified
from character 29 of Barcelona (2000).
RACHISES
10. HABIT: (0) erect; (1) scrambling. This character
corresponds to character 19 of Barcelona (2000).
AND MINOR AXES
16. RACHIS ABAXIALLY: (0) terete; (1) bi-angular;
(2) keeled.
17. SURFACE: (0) unarmed; (1) spinules/spiny. This
character corresponds to character 45 of Barcelona (2000).
18. SPINE LENGTH: (0) < 1.5 mm; (1) 2–3 mm. This
character was coded as inapplicable for the taxa
without spines.
19. INDUMENT: (0) macroscopically hairy; (1) macroscopically glabrous.
20. ARCHITECTURE: (0) straight; (1) flexuose (zigzagging). This character corresponds to character
48 of Barcelona (2000).
21. NATURE OF SULCUS: (0) narrow; (1) broad; (2)
absent.
LAMINAE
22. DIMORPHISM: (0) monomorphic; (1) dimorphic.
This character is modified from character 32 of
Barcelona (2000).
23. TEXTURE: (0) herbaceous; (1) coriaceous. This
character is modified from character 36 of Barcelona (2000).
24. DROMY AT THE BASE OF BLADE (LOWERMOST PINNAE): (0) catadromous; (1) anadromous. This character corresponds to character 14
of Pryer et al. (1995).
25. VEIN ORDERS: (0) one; (1) two; (2) three; (3) four
or more. This character corresponds to character
5 of Pryer et al. (1995).
PINNAE
FRONDS
351
AND PINNULES
26. PINNAE ATTATCHMENT IN ADULTS: (0) opposite; (1) alternate. This character is modified from
character 51 of Barcelona (2000).
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
352
S. LEHTONEN ET AL.
27. DISPOSITION: (0) ascending; (1) reflexed. This
character is modified from character 50 of Barcelona (2000).
28. TERMINAL PINNA ARCHITECTURE: (0)
conform; (1) confluent. This character corresponds to character 55 of Barcelona (2000).
29. PINNULE INSERTION: (0) at ridges; (1) below
ridges.
30. LOWER PINNULES: (0) not much reduced; (1)
strongly reduced; (2) aphlebioid.
31. PINNULES PENDULOUS: (0) no; (1) yes.
32. PINNAE SURFACE: (0) macroscopically hairy;
(1) macroscopically glabrous.
ULTIMATE
SEGMENTS
33. SHAPE: (0) equal sided; (1) cuneate-rhombic; (2)
dimidiate. This character is modified from character 75 of Barcelona (2000).
34. SEGMENT BASE: (0) non-auriculate (1) auriculate.
35. SEGMENT MARGIN: (0) entire; (1) erose–
crenate; (2) incised. This character is modified
from character 78 of Barcelona (2000).
36. SEGMENTS: (0) stalked; (1) sessile; (2) connected
by wing.
VENATION
37. VEINS: (0) running out to the margin; (1) stop
short of the margin.
38. VEIN FUSION: (0) non-anastomosing; (1) anastomosing. This character is modified from character 7 of Pryer et al. (1995). Here, even nonconsistent formation of areoles is coded as
anastomosing, as this happens only in certain
species, while most of the species constantly have
free veins.
INDUSIA
39. ORIGIN OF INDUSIA OR INDUSIAL COMPONENTS: (0) leaf margin; (1) abaxial leaf surface.
This character corresponds to character 53 of
Pryer et al. (1995).
40. FALSE INDUSIUM: (0) present; (1) absent. This
character corresponds to character 57 of Stevenson & Loconte (1996).
41. INDUSIAL OPENING: (0) introrse; (1) extrorse;
(2) suprasoral. This character corresponds to
character 55 of Pryer et al. (1995).
42. EXTENT OF LATERAL ADNATION: (0) free (1)
adnate. This character is modified from character
84 of Barcelona (2000).
43. SORI LOCATION: (0) inner to outer part of the
segment margin; (1) only in the outer part of the
upper segment margin.
44. INDUSIUM: (0) reaching margin; (1) intramarginal; (2) longer than and protruding beyon
lamina. This character is inapplicable for taxa
with leaf marginal origin of indusium.
45. INDUSIUM SHAPE: (0) obovate to ovate; (1)
elliptic; (2) horseshoe-shaped; (3) flabellate. This
character is modified from character 85 of Barcelona (2000).
46. INDUSIUM REFLEXED: (0) no; (1) yes.
47. INDUSIUM MARGIN: (0) erose; (1) entire. This
character is modified from character 92 of Barcelona (2000).
48. INDUSIUM WIDTH: (0) less than 0.3 mm; (1)
0.3–0.6 mm; (2) 0.7–1 mm. This character is
modified from character 94 of Barcelona (2000).
SPORANGIA
49. SIZE: (0) < 160 mm; (1) 200–250 mm; (2) > 250 mm.
50. NUMBER OF SPORANGIA/SORUS: (0) few
(< 12); (1) many (usually > 20). This character
corresponds to character 51 of Pryer et al. (1995).
51. ANNULUS CELLS: (0) 9–12; (1) 15–23.
SPORES
52. TYPE: (0) monolete; (1) trilete. This character
corresponds to character 107 of Barcelona (2000).
53. SIZE: (0) 18–35 mm; (1) 35–43 mm; (2) 50–60 mm.
This character is modified from character 109 of
Barcelona, (2000).
54. PERISPORE
(EPISPORE)
SURFACE:
(0)
(nearly) smooth or plain; (1) obviously patterned
or sculptured. This character corresponds to character 64 of Pryer et al. (1995).
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
PHYLOGENETICS OF LINDSAEACEAE
353
APPENDIX 2
Morphological data matrix. Polymorphic entries: a = [01], b = [12], c = [13]. Inapplicable data = ‘–’. Missing
data = ‘?’.
111111111122222222223333333333444444444455555
0123456789012345678901234567890123456789012345678901345
Nesolindsaea caudata
Nesolindsaea kirkii
Cystodium sorbifolium
Lindsaea agatii
Lindsaea annamensis
Lindsaea apoensis
Lindsaea arcuata
Lindsaea austrosinica
Lindsaea azurea
Lindsaea bifida 1
Lindsaea bifida 2
Lindsaea blanda
Lindsaea blotiana 2
Lindsaea blotiana 2
Lindsaea bolivarensis
Lindsaea borneensis
Lindsaea botrychioides
Lindsaea bouillodii
Lindsaea brachypoda
Lindsaea brevipes
Lindsaea cf. cambodgensis
Lindsaea carvifolia
Lindsaea chienii
Lindsaea chrysolepis
Lindsaea coarctata 1
Lindsaea coarctata 2
Lindsaea crispa
Lindsaea cubensis
Lindsaea cultrata
Lindsaea cyclophylla
Lindsaea digitata
Lindsaea diplosora
Lindsaea dissectiformis
Lindsaea divaricata
Lindsaea divergens
Lindsaea doryphora 1
Lindsaea doryphora 2
Lindsaea dubia
Lindsaea ensifolia 1
Lindsaea ensifolia 2
Lindsaea falcata
Lindsaea feei
Lindsaea cf. fissa
Lindsaea fraseri
Lindsaea gomphophylla
Lindsaea goudotiana
Lindsaea grandiareolata
Lindsaea gueriniana
Lindsaea guianensis
301100011100010100-001001210100002000101111003010111110
301100001100010100-100001210100002010101110021011111110
?00201100100000100-00000031010001001200a021020002211111
301000001000210110-101001210000000000111110003011010100
301000001000210110-100001210100001020101110001001010100
311011003100010010-102001110110002020101110001111010100
301000001000210110-100001210000002000101110003110010100
301000001000211110-101001210000001010101110013001010100
301000001000010110-101001210100002010111111013110010100
301000001000210110-101001210100001020101110001110010100
301000001000210110-101001210100001020101110001110010100
311000001000010010-100001110100002010101110011111010100
311000002000011110-1010012100000010101011100020010?0100
311000002000010110-101001210100001010101110011101010?00
301000001000211110-101001210000002000101110013110010100
311011001100010100-100001210100002000101110003110010100
301000001000210a10-100001110000001010101110003101010100
301000001000010110-101001210100001010101110001001010100
301000002000210010-100101b10100002000101110001011010100
301000001000210010-101001110101002010101110001011010100
301000001000010110-100001210100001010101110011001010100
311011003100010010-102001110111002020101110001110010100
301000002000010110-101001210100001010101110011001010100
311000003100010010-101001110100002010111111001011010100
301000001000010110-101001210000002000101110013110010100
301000001000010110-101001210000002000101110013110010100
301000001000010110-100001210100002010111110003011010100
301000001000210110-100101210000001000101110013001010000
301000001000111110-101001210000002000111110001110010100
3010000010000111-0-1010011-00---0--0-101110013111010000
301000001000011110-101001210000002000101110013110010100
311000003100010100-101001210100002010101111101011010100
301000001000010110-100001210100001020101110011001010100
301000001000011110-101001210000002000101110013110010100
301000002000010020-101001110001000101101110003010010100
301001003000010a00-100001210000002000101110013110010100
301001003000010a00-100001210000002000101110013110010100
301000001000211110-101001110000002010101110003110010100
301000001000210110-100001210000000000111110003011010100
301000001000210110-100001210000000000111110003011010100
301000001000211110-101001110000002000101110013110010100
301000001000010110-100001210100002010101110011101010100
311011003100010010-102001110101002020101110001011100100
301000001000010110-100001210000000010111110003011?1????
301000001000011100-101001110100001010101110003001010100
311000001000010010-101001210100001020101110022011010100
301000001000011110-101001210000000000111110003011011100
301000002000010120-101011110100000100101110003011111100
301000001000010100-100001210100002000101110013110010100
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
354
S. LEHTONEN ET AL.
APPENDIX 2 Continued
111111111122222222223333333333444444444455555
0123456789012345678901234567890123456789012345678901345
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
hainaniana
harveyi
hemiglossa 1
hemiglossa 2
hemiptera
heterophylla
imrayana 1
imrayana 2
incisa
integra 1
integra 2
jamesonioides
javanensis 1
javanensis 2
cf. javitensis
kawabatae
kingii
lancea var. lancea
lancea var. leprieurii 1
lancea var. leprieurii 2
lancea var. submontana
lapeyrousei 1
lapeyrousei 2
leptophylla
lherminieri
linearis
lobata
longifolia
lucida
madagascariensis
malayensis 1
malayensis 2
media 1
media 2
meifolia
merrillii ssp. merrillii
merrillii ssp. yaeyamensis
microphylla
millefolia 1
millefolia 2
monocarpa
multisora
nervosa
oblanceolata
obtusa 1
obtusa 2
orbiculata
ovoidea
oxyphylla
pacifica
pallida
parallelogramma
301000001000010110-100001210100002010111110001111010100
301000001000010110-100001210000002010111110011011010100
301000001000010110-101001210000002000101110013110010100
301000001000010110-101001210000002000101110013110010100
301000001000011100-101001210100002000101110003010010100
301000001000010110-100001210000000010111110003011010100
311000003100010110-1000012-0000000010101110011111010100
311000003100010110-1000012-0000000010101110011111010100
301000002010210010-101001110100001000101110001002111100
301000001000210010-101001b10000002000111110003111010100
301000001000210010-101001b10000002000111110003111010100
301000001100110020-101011110000000101101110003012111100
301000001000010110-100001210000001010101110003011010100
301000001000010110-100001210000001010101110003011010100
301000001000010110-101011210100002000101110003000110100
301000001000010110-101001210100001010101110011001010100
301000002100210110-100001210101002010101110001001010100
301000001000210110-101001210000002000101110013110010100
301000001000011110-101001110000002000101110013110010100
301000001000011110-101001110000002000101110013110010100
301000001000211110-101001110000002000101110003110010100
301000001000210010-101001110101002020101111001001010100
301000001000210010-101001110101002020101111001001010100
311000001000011000-101001210000001010101110021011010100
301000001000210110-101001210000002000101110013110010100
301000001000010a00-101101110000001000101110003002011110
301000001000010110-100001210100002010111110001111010100
301000001000010110-101001210100002010111110001011010100
301000001000210010-100001110100002010101110001011010100
311000002000010110-101001210100001010101110011101010?00
301000001000010110-100001210100002010111110011110010100
301000001000010110-101001210100002010111110001010010100
301000001000010110-100001210000000000111110003011?1????
301000001000010110-1000012101000010101a1110001001010100
301000001000010100-101011210100101000101110000011011110
311011003100010010-101001110101002010101110011010000100
311011003100010010-101001110101002010101110001010000100
301000002100010000-101001210100001010101110001001011100
301000002000011110-101001210100001020101110011110010100
301000002000011110-101001210100001020101110011110010100
311000001100010110-101011210100002010111111121001010100
301000001000210110-1010012101000020101011100011100?0100
301000002000010110-100001210000001010101110001100010100
311011003100010010-102001110a11002000101110003111010100
301000001000010110-101001210100002010111110001111010100
301000001000010110-101001210100002010111110001111010100
301000001000010a10-100001210100001010101110003001010100
301000001000010110-100001210100001010101110001101010100
301000001000010100-101001110100000010101110023000010???
301000001000010110-1010012101000020101111100010110?0100
301000001000010110-100001210000002000101110001001010010
301000001000211110-101001210100002010111110001010010100
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
PHYLOGENETICS OF LINDSAEACEAE
355
APPENDIX 2 Continued
111111111122222222223333333333444444444455555
0123456789012345678901234567890123456789012345678901345
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
parasitica
parkeri
pectinata
pellaeiformis
pendula
phassa
pickeringii
plicata
polyctena
portoricensis 1
portoricensis 2
pratensis
prolongata
propinqua
pseudohemiptera
pulchella
pulchra
quadrangularis ssp. antillensis
regularis
reniformis
rigida
rigidiuscula 1
rigidiuscula 2
rosenstockii
rufa
sagittata
schizophylla
schomburgkii
seemannii
semilunata
sessilis
sp. 1
sp. 2
sp. 3
sphenomeridopsis
spruceana
stolonifera
stricta var. jamesoniiformis
stricta var. parvula
stricta var. stricta
subtilis
surinamensis
taeniata
tenuifolia
tenuis
tetragona
tetraptera
trichomanoides
ulei
venusta
vieillardii
virescens
311011003100010a00-101001210000002000101110003111010100
301000001000011110-101001210000002000101110003111010100
311011003100010010-102001110111002010101110011010010100
301000002100010a20-101011110100000100101110003011111100
301000001000010100-101011210100101000101110001001110110
301000001000210110-101001210000002000101110013110010100
311010003000010010-1010011101010020101a1110011111010100
30100000?000010020-101001110100000010101110001012111120
301000001000210110-101001210100002020101110011110010100
301000001000010a10-101011210100002000101110013101010100
301000001000010a10-101011210100002000101110013101010100
301000003100010020-101011110101002000101111003001111020
301000001000010110-100001210000001010101110001010010100
311000001100010110-100001210100002010111110001011010100
311011003100010010-102001110111002010101110011110010100
311000001000010010-1010011101000020101a1110011011010100
311000001000210010-101001110100002010111110001111010100
301000001000210110-100001210000002000101110003110010100
311011003100010a10-101001b10100002010101110001111010100
3010000010000111-0-1010011-00---0--0-101110013111010100
311000001100010110-1010112101000020101a1111101001110100
301000001000211110-101011210000002000101110003110110100
301000001000211110-101011210000002000101110003110110100
311010003100010110-100001210100002020101110011110010100
301000001000010110-100001210000001010101110001101010100
3010000010000111-0-1010011-00---0--0-101110013111010100
311000001000010110-101001210100001010101110001001010100
301000001000211110-101011110000002000101110003110010100
301000003100010020-101001110101002010101111003011111020
301000001000211110-101001110000002000101110003110010100
311011003100010010-102001110111002010101110011110010100
311010003100010110-1010012101000020101011100111100?0100
311000001100010110-1010112101000020101a1111101001110100
311000001000010100-100001210100001010101110001001010100
301000001000011110-101001210100001020101110011001010100
301000001000010100-101001210100002000101110003110010100
311000001000210010-101001110100002010111110001111010100
301000001000010a00-101011210100002000101110003101110110
301000001000010a00-101011210100002000101110003101110110
301000001000010100-101011210100002000101110003101110110
311000002000010010-100001110100001010101110022011010100
301000001000111110-101001110000002000101110013010010100
301000001000210110-100001210000002000101110013010010100
301000001000110120-101001210100002020101110011110010100
301000001010010010-101001210100002010101110011101010100
301000001000210110-101001210100002020101110001110010100
301000001000011110-101001210000002000101110003010010100
301000003000010110-100001210100001010101110001001010100
301000001000011100-101001110000002000101110013110010100
301000001000210110-101001210100002010111110001011010100
301000002000210110-101001210000000010111110003011010100
301000001000210110-101001210100001010101110001100010100
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
356
S. LEHTONEN ET AL.
APPENDIX 2 Continued
111111111122222222223333333333444444444455555
0123456789012345678901234567890123456789012345678901345
Lindsaea viridis
Lindsaea vitiensis
Lindsaea walkerae
Lindsaea werneri
Lonchitis hirsuta
Odontosoria aculeata
Odontosoria afra
Odontosoria africana
Odontosoria angustifolia
Odontosoria biflora
Odontosoria chinensis
Odontosoria deltoidea 1
Odontosoria deltoidea 2
Odontosoria flexuosa
Odontosoria fumarioides
Odontosoria guatemalensis
Odontosoria jenmanii
Odontosoria melleri
Odontosoria retusa
Odontosoria scandens
Odontosoria schlechtendalii
Odontosoria wrightiana
Osmolindsaea japonica
Osmolindsaea odorata 1
Osmolindsaea odorata 2
Osmolindsaea odorata 3
Osmolindsaea sp.
Pteridium pinetorum
Saccoloma elegans
Saccoloma inaequale
Sphenomeris clavata 1
Sphenomeris clavata 2
Tapeinidium amboynense
Tapeinidium calomelanos
Tapeinidium denhamii
Tapeinidium gracile
Tapeinidium longipinnulum
Tapeinidium luzonicum
Tapeinidium melanesicum
Tapeinidium moorei
Tapeinidium novoguineense
Tapeinidium pinnatum
301000001100010020-100001110100001020101110001002111020
311000001000210010-101001110100002010101110011111010100
301000001000010100-101011210000000000101110003011111100
311000001000210110-101001110100002010111110011111010100
101100100000000100-00100031010001000210010-0-----211121
3111000011110100011111011301102001010101111020011101120
301000002100010000-1010013101000010201011110210012011b0
301000002110010000-110011311100001020101111020001101110
301?00103000010100-100011310100001020101111001001101110
301000001100010100-101011310100001020101111000012101010
301000002100010100-10101131010000102010111100a001201010
311100102100010100-100011310100001010101111021001111110
311100102100010100-100011310100001010101111021001111110
3111000011110100010111001301102001010101111000001201120
3111000011110100011111011301102001020101111000012201120
311100001111010000-111001301102001020101111020012201120
3111000031110100011111011301102001010101111021012101120
301100101100010100-110011310100001010101110021011201110
301100103100010100-10001131010000101010111000c001201110
3111000011110100010111011301102001010101111001012101120
31110000?111010000-111001301102001020101111021012101120
3111000011110100011110011301102001010101111020011101120
301100001000010000-100001110000002000101111003012111010
301100001000010000-100001110100002010101111001001111010
301100001000010000-100001110100002010101111001001111010
301100001000010000-100001110101002010101111001002111010
301100001000010000-100001110101002010101111001001111010
011100100000000100-00000031000001000200000-0-----111101
200201103100010100-1000012-0000000000001110001101211101
200201103100010100-100001310100000012001111000002201101
301000002100010100-110001310100001020101111021002111120
301000002100010100-110001310100001020101111021002111120
301100001100010110-101011310100000012101111010011101000
301000001000010100-101011310100000012101111001011111000
301000001000110110-101001310100000012101110020001101000
301100001100110110-1010112101000000101011110100011?1000
301100003100210110-101011210000000010101111001001111000
301100001100110110-1010113101000000121011110100111?1010
301100001000010100-101011210000000010101111011001111000
301000011000010100-100011310100000012101111001001111020
311100003100010100-101011310100000012101111011011101000
301100001100110110-1010112101000000101011110100011?1000
APPENDIX 3
DNA-structure characters.
0. 4-bp INVERSION IN trnL-trnF: (0) GT-type; (1) CA-type.
1. 7-bp INVERSION IN trnL-trnF: (0) CT-type; (1) GA-type.
2. 13-bp INVERSION IN trnH-psbA: (0) T-type; (1) A-type.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
PHYLOGENETICS OF LINDSAEACEAE
357
APPENDIX 4
DNA-structure data matrix. Polymorphic entries: a = [01]. Missing data = ‘?’.
Nesolindsaea caudata
Nesolindsaea kirkii
Cystodium sorbifolium
Lindsaea agatii
Lindsaea annamensis
Lindsaea apoensis
Lindsaea arcuata
Lindsaea austrosinica
Lindsaea azurea
Lindsaea bifida 1
Lindsaea bifida 2
Lindsaea blanda
Lindsaea blotiana 1
Lindsaea blotiana 2
Lindsaea bolivarensis
Lindsaea borneensis
Lindsaea botrychioides
Lindsaea bouillodii
Lindsaea brachypoda
Lindsaea brevipes
Lindsaea cf. cambodgensis
Lindsaea carvifolia
Lindsaea chienii
Lindsaea chrysolepis
Lindsaea coarctata 1
Lindsaea coarctata 2
Lindsaea crispa
Lindsaea cubensis
Lindsaea cultrata
Lindsaea cyclophylla
Lindsaea digitata
Lindsaea diplosora
Lindsaea dissectiformis
Lindsaea divaricata
Lindsaea divergens
Lindsaea doryphora 1
Lindsaea doryphora 2
Lindsaea dubia
Lindsaea ensifolia 1
Lindsaea ensifolia 2
Lindsaea falcata
Lindsaea feei
Lindsaea cf. fissa
Lindsaea fraseri
Lindsaea gomphophylla
Lindsaea goudotiana
Lindsaea grandiareolata
Lindsaea gueriniana
Lindsaea guianensis
Lindsaea hainaniana
Lindsaea harveyi
Lindsaea hemiglossa 1
Lindsaea hemiglossa 2
Lindsaea hemiptera
000
000
00?
010
000
010
010
000
010
000
000
010
000
000
010
010
010
000
000
010
010
010
000
010
010
010
010
000
000
010
010
010
000
000
010
010
010
010
000
???
010
010
010
010
010
00?
000
000
010
010
010
010
010
000
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
heterophylla
imrayana 1
imrayana 2
incisa
integra 1
integra 2
jamesonioides
javanensis 1
javanensis 2
cf. javitensis
kawabatea
kingii
lancea var. lancea
lancea var. leprieurii 1
lancea var. leprieurii 2
lancea var. submontana
lapeyrousei 1
lapeyrousei 2
leptophylla
lherminieri
linearis
lobata
longifolia
lucida
madagascariensis
malayensis 1
malayensis 2
media 1
media 2
meifolia
merrillii ssp. merrillii
merrillii ssp. yaeyamensis
microphylla
millefolium 1
millefolium 2
monocarpa
multisora
nervosa
oblanceolata
obtusa 1
obtusa 2
orbiculata
ovoidea
oxyphylla
pacifica
pallida
parallelogramma
parasitica
parkeri
pectinata
pellaeiformis
pendula
phassa
pickeringii
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
0a?
010
???
010
000
000
010
010
010
000
000
01?
010
010
010
010
010
???
010
010
001
010
010
010
010
010
010
010
010
010
010
010
010
000
00?
010
010
00?
010
010
010
000
010
010
010
010
000
010
010
010
010
010
000
010
358
S. LEHTONEN ET AL.
APPENDIX 4 Continued
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
Lindsaea
plicata
polyctena
portoricensis 1
portoricensis 2
pratensis
prolongata
propinqua
pseudohemiptera
pulchella
pulchra
quadrangularis ssp. antillensis
regularis
reniformis
rigida
rigidiuscula 1
rigidiuscula 2
rosenstockii
rufa
sagittata
schizophylla
schomburgkii
seemannii
semilunata
sessilis
sp. 1
sp. 2
sp. 3
sphenomeridopsis
spruceana
stolonifera
stricta var. jamesoniiformis
stricta var. parvula
stricta var. stricta
subtilis
surinamensis
taeniata
tenuifolia
tenuis
tetragona
tetraptera
trichomanoides
ulei
venusta
vieillardii
000
110
000
010
010
000
010
010
010
010
010
010
010
0?0
010
010
010
000
010
010
010
010
010
010
010
010
010
010
01?
010
010
000
010
000
010
010
110
010
010
000
000
010
010
010
Lindsaea virescens
Lindsaea viridis
Lindsaea vitiensis
Lindsaea walkerae
Lindsaea werneri
Lonchitis hirsuta
Odontosoria aculeata
Odontosoria afra
Odontosoria africana
Odontosoria angustifolia
Odontosoria biflora
Odontosoria chinensis
Odontosoria deltoidea 1
Odontosoria deltoidea 2
Odontosoria flexuosa
Odontosoria fumarioides
Odontosoria guatemalensis
Odontosoria jenmanii
Odontosoria melleri
Odontosoria retusa
Odontosoria scandens
Odontosoria schlechtendalii
Odontosoria wrightiana
Osmolindsaea japonica
Osmolindsaea odorata 1
Osmolindsaea odorata 2
Osmolindsaea odorata 3
Osmolindsaea sp.
Pteridium pinetorum
Saccoloma elegans
Saccoloma inaequale
Sphenomeris clavata 1
Sphenomeris clavata 2
Tapeinidium amboynense
Tapeinidium calomelanos
Tapeinidium denhamii
Tapeinidium gracile
Tapeinidium longipinnulum
Tapeinidium luzonicum
Tapeinidium melanesicum
Tapeinidium moorei
Tapeinidium novoguineense
Tapeinidium pinnatum
000
01?
010
000
010
00010
010
010
010
010
010
01?
01?
010
000
000
000
010
0?0
000
000
010
00?
00?
000
000
000
000
0000001
001
000
000
000
000
000
000
000
000
000
000
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359
PHYLOGENETICS OF LINDSAEACEAE
APPENDIX 5
Command lines applied.
Morphological data analysis using TNT:
log filename;
mxram 256;
p datafile;
taxname=;
out Pteridium_pinetorum;
hold 100000;
mult=ratchet replic 500 hold 10;
length;
tsave *filename;
save;
tsave /;
nelsen;
tsave *filename;
save;
tsave /;
quit;
Jackknife analyses using TNT:
log filename;
mxram 256;
p datafile;
taxname=;
out Pteridium_pinetorum;
hold 100000;
resample jak replications 100 [mult=ratchet
replic 100 hold 1];
quit;
Molecular and combined analyses using POY:
read(“datafiles”)
report(“filename”,timer:“search start”)
transform(tcm:“111.txt”)
set(seed:1,log:“filename”,root:“Pteridium_
pinetorum”)
build(500)
359
swap(threshold:5.0)
select()
perturb(transform(static_approx),iterations:20,
ratchet:(0.25,3))
select()
fuse(iterations:200,swap())
select()
report(“filename”,treestats)
report(“filename”,trees)
report(“filename”,consensus)
report(“filename”,graphconsensus)
report(“filename”,diagnosis)
report(“filename”,ia)
report(“filename”,cross_references:all)
report(“filename”,timer:“search_end”)
set(nolog)
exit()
Sensitivity analyses using POY:
read(“datafiles”)
set(seed:1,log:“filename”,root:“Pteridium_
pinetorum”)
store(“original_data”)
transform(tcm:“filename”)
transform((names:(“filename”),weightfactor:N))
build(20)
swap(timeout:3600)
select()
perturb(transform(static_approx),iterations:10,
ratchet:(0.25,3), swap(timeout:20000))
select()
fuse(iterations:200,swap())
select()
report(“filename”,trees:(total),“filename”,consensus,“filename”,graphconsensus)
use(“original_data”) . . .
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 305–359