The Lucilia group (Asteraceae,
Gnaphalieae): phylogenetic and taxonomic
considerations based on molecular and
morphological evidence
Susana E. Freire, M. Amelia Chemisquy,
Arne A. Anderberg, Stephan G. Beck,
Rosa I. Meneses, Benoît Loeuille &
Estrella Urtubey
Plant Systematics and Evolution
ISSN 0378-2697
Plant Syst Evol
DOI 10.1007/s00606-014-1147-0
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Author's personal copy
Plant Syst Evol
DOI 10.1007/s00606-014-1147-0
ORIGINAL ARTICLE
The Lucilia group (Asteraceae, Gnaphalieae): phylogenetic
and taxonomic considerations based on molecular
and morphological evidence
Susana E. Freire • M. Amelia Chemisquy •
Arne A. Anderberg • Stephan G. Beck •
Rosa I. Meneses • Benoı̂t Loeuille • Estrella Urtubey
Received: 19 March 2014 / Accepted: 28 July 2014
Ó Springer-Verlag Wien 2014
Abstract The Lucilia group sensu Anderberg and Freire
comprises nine South American genera: Belloa, Berroa,
Chevreulia, Cuatrecasasiella, Facelis, Gamochaetopsis,
Jalcophila, Lucilia and Luciliocline. The aims of this
contribution were, using DNA sequences from plastid
(rpl32-trnL, trnL-F) and nuclear (ITS and ETS) markers,
together with morphological characters, to test the monophyly of the Lucilia group and provide new insight into
generic circumscriptions. Our studies, including a broad
taxon sampling of Gnaphalieae species, suggest that the
Lucilia group is paraphyletic, since Antennaria, Chionolaena, Gamochaeta, Loricaria, Micropsis, Mniodes and
Electronic supplementary material The online version of this
article (doi:10.1007/s00606-014-1147-0) contains supplementary
material, which is available to authorized users.
S. E. Freire (&) E. Urtubey
Instituto de Botánica Darwinion-CONICET, Labardén 200,
CC 22, B1642 HYD San Isidro, Argentina
e-mail: sfreire@darwin.edu.ar
M. A. Chemisquy
Museo Argentino de Ciencias Naturales ‘‘Bernardino
Rivadavia’’-CONICET, Av. Angel Gallardo 470,
C1405DJR Ciudad Autónoma de Buenos Aires, Argentina
A. A. Anderberg
Swedish Musem of Natural History, P. O. Box 50007,
104 05 Stockholm, Sweden
S. G. Beck R. I. Meneses
Herbario Nacional de Bolivia, Museo Nacional de Historia
Natural, Universidad Mayor de San Andrés,
CC 10077 La Paz, Bolivia
B. Loeuille
Departamento de Botânica, Laboratório de Sistemática Vegetal,
Rua Do Matão, Travessa 14 no 321, Cidade Universatária,
São Paulo 05508-090, Brazil
Stuckertiella are all nested within the Lucilia group. Morphology and molecular analyses combined showed that the
traditional generic circumscription of most of the genera
(e.g., Berroa, Chevreulia, Chionolaena, Cuatrecasasiella,
Facelis, Jalcophila and Micropsis) correlates with the
inferred phylogenetic relationships. Conversely, Lucilia
and Luciliocline are non-monophyletic. Lucilia is nested in
a clade with Berroa, Facelis and Micropsis. Luciliocline is
strongly embedded within the clade Belloa pp ? Mniodes.
Our results are consistent with Dillon’s study that considered Belloa as a montotypic genus (B. chilensis). Luciliocline and the remaining species of Belloa are
accommodated in the genus Mniodes, and the necessary
combinations are proposed for the expanded Mniodes. All
the analyses showed that the monotypic genera Stuckertiella and Gamochaetopsis are in a well-supported clade
nested within Gamochaeta, which implies that taxonomic
changes are required also for these genera. Internal relationships in the group and the key morphological characters used in the taxonomy of the group, as well as
incongruences found between morphological and molecular analyses, are discussed.
Keywords
trnL-F
Belloa ETS ITS Mniodes rpl32-trnL
Introduction
The Lucilia group was first recognized by Merxmüller et al.
(1977) as a subgroup of the tribe Inuleae, subtribe Gnaphaliinae. It was defined by its dorsally pubescent style
branches and consisted of 12 genera, Belloa, Berroa,
Chevreulia, Facelis, Leucopholis, Lucilia, probably
Gnaphaliothamnus and Raouliopsis, and the dioecious or
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S. E. Freire et al.
subdioecious genera Chionolaena, Luciliopsis, Mniodes
and Oligandra (Table 1). A few years later, Robinson
(1985) considered Luciliopsis to be a synonym of Facelis,
placing two of its three species in the new genus Cuatrecasasiella. Anderberg and Freire (1990a) later showed that
the type of the genus Luciliopsis belongs in Chaetanthera
of the Mutisieae. Two genera were added to this group,
Jalcophila (Dillon and Sagastegui-Alva 1986) and Novenia
(Freire 1986a). Oligandra was stated later by Freire (1989)
to be a synonym of Lucilia, whereas Leucopholis was a
synonym of Chionolaena (Anderberg 1991; Freire 1993).
Based on a morphological cladistic analysis, Anderberg
(1991) established five subtribes for the tribe Gnaphalieae:
Angianthinae Benth., Relhaniinae Less., Cassiniinae Anderb., Gnaphaliinae, and Loricariinae Anderb. That study
indicated that the Lucilia group, as earlier understood, was
a highly polyphyletic assemblage and also excluded Novenia from the Gnaphalieae. The remaining genera were
placed in three clades, one composed of Gnaphaliothamnus
and Chionolaena (subtribe Cassiniinae), the second
including Loricaria, Mniodes and Raouliopsis (subtribe
Loricariinae) and the third one, Lucilia group s. str. (subtribe Gnaphaliinae), was composed of Belloa, Berroa,
Chevreulia, Cuatrecasasiella, Facelis, Lucilia and Jalcophila. Subsequently, Anderberg and Freire (1991) added
two further taxa to the Lucilia group s. str., viz. Gamochaetopsis and Luciliocline. Both were segregated from
Lucilia which was shown to be non-monophyletic. Anderberg and Freire (1991) recognized a Lucilia group s. str.,
comprising nine genera (Table 1) with the following traits:
very slender pappus bristles basally connate, dorsally
pubescent style branches, purple tipped florets and polychromous phyllaries. Later, Dillon (2003), based on a
previous cladistic analysis of morphological characters
(Dillon 2000) revealed the need for a new circumscription
for the group, suggesting a close potential relationship
between Chionolaena, Gamochaeta, Micropsis, Stuckertiella and the other members of the Lucilia group (Table 1).
Most of the genera included in the Lucilia group have
been monographed since they were described, i.e., Berroa,
Facelis, Micropsis and Stuckertiella (Beauverd 1913a, b, c,
d); Loricaria and Mniodes (Cuatrecasas 1954a, b); Belloa
(Cabrera 1958); Lucilia (Freire 1986b); Jalcophila (Dillon
and Sagástegui-Alva 1986); Chionolaena (Freire 1993;
Nesom 2001; Loeuille et al. 2011); Luciliocline (Anderberg
and Freire 1991); Gamochaeta (Nesom 1990a; Freire and
Iharlegui 1997), but most of their species have been placed
in two or more different genera (Table 1). The delimitation
of the genus Lucilia is probably the most controversial, and
the limits between Lucilia, Belloa and Luciliocline have
been discussed in recent years. As an example, Rémy
(1847) created Belloa on the basis of Lucilia chilensis.
Cabrera (1958) expanded the monotypic genus Belloa to 11
123
species. Dillon and Sagástegui-Alva (1985) described three
new species of Belloa and transferred another four to this
genus (one from Mniodes and three from Lucilia), raising
the number of Belloa species to 18 (Dillon and SagásteguiAlva 1991) or 16 (Dillon and Sagástegui-Alva 1992).
Freire (1986b, 1987) merged Belloa with Lucilia. Anderberg and Freire (1991) maintained Belloa as an independent genus for the species with prostrate stems and
proposed the genus Luciliocline for the species with erect
or ascending stems. Finally, Dillon (2003) recognized
Belloa as a monotypic genus and transferred the remaining
species of Belloa to Luciliocline. The evident instability in
the classification of the Lucilia group reflects the general
scarcity of morphological characters traditionally considered relevant for the classification of the group and their
high level of homoplasy. This affects mainly not only the
generic boundaries, but also the circumscription of the
Lucilia group, and this urged for an investigation based on
molecular data to shed light on the classification.
In this context, a phylogenetic analysis including
molecular and morphological information could be useful
to elucidate the taxonomic arrangement of the taxa mentioned above. Both chloroplast and nuclear DNA markers
have been used previously to address the phylogenetic
relationships in the tribe Gnaphalieae, mainly focused on
African and Australian taxa (Bergh and Linder 2009; Bayer
et al. 2000, 2002; Galbany-Casals et al. 2010; Smissen
et al. 2011), but molecular information on South American
groups remains unknown or poorly studied (Ward et al.
2009).
The aims of this work were, using two plastid (rpl32trnL and trnL-F) and two nuclear DNA regions (ITS and
ETS), to test the various hypotheses of relationships within
the Lucilia group, using a broad sampling of the
Gnaphalieae.
Materials and methods
Taxon sampling
A special effort was made to cover the morphological and
geographical variation of Lucilia group and allied genera in
South America. The sampling for plastid and nuclear
sequencing includes material from Argentina, Bolivia,
Brazil, Chile, Colombia and Ecuador. The analyses comprised a total of 56 species, 21 belonging to the Lucilia
group sensu Anderberg and Freire (1991), representing
51 % of the group. At least one species each of the 9
genera included in this group were used in the analyses
(Appendix 1 in ESM). In order to assess the placement of
the Lucilia group members within the tribe, 35 species
belonging to closely related genera were used as outgroups
Genera
Nr of species and distribution
Species
Merxmüller et al.
(1977), 12 genera
Belloa
11, S. America
None mentioned
Lucilia group
Berroa
1, S. America
None mentioned
Chevreulia
6, S. America
None mentioned
Chionolaena
c. 8, Mexico, Colombia, Brazil
None mentioned
Facelis
4, S. America
None mentioned
Gnaphaliothamnus
Leucopholis
1, Mexico, Guatemala
4, Brazil
None mentioned
None mentioned
Lucilia
c. 20, S. America
None mentioned
Luciliopsis
4, S. America
None mentioned
Mniodes
5, Andean Peru
None mentioned
Oligandra
3, S. America
None mentioned
Raouliopsis
2, Andean Colombia
None mentioned
Anderberg (1991), 7
genera
Belloa
12, S. America
B. burkartii (=Lucilia burkartii), B. catamarcensis (=Lucilia catamarcensis), B. chilensis (=Lucilia
nivea), B. longifolia (=Lucilia longifolia), B. lopezmirandae (=B. turneri, Lucilia lopezmirandae),
B. pickeringii (=Lucilia pickeringii), B. piptolepis (=Lucilia piptolepis), B. plicatifolia (=Lucilia
plicatifolia), B. radians (=Lucilia radians), B. santanica (=Lucilia santanica, Belloa spathulifolia),
B. schultzii (=B. cerrateae, Lucilia schultzii, Mniodes cerrateae), Belloa subspicata (=Lucilia
subspicata)
South American
Lucilia group
Berroa
1, S. America
B. gnaphalioides
Chevreulia
5, S. America
C. acuminata, C. diemii, C. lycopodioides, C. pusilla, C. sarmentosa
Cuatrecasasiella
(=Luciliopsis pp.)
2, S. America
C. isernii (=Luciliopsis isernii), C. argentina (=Luciliopsis argentina)
Anderberg and
Freire (1991), 9
genera
Facelis
3, S. America
F. lasiocarpa, F. plumosa, F. retusa
Lucilia (including
Oligandra)
11, S. America
L. acutifolia, L. alpina, L. eriophora, L. ferruginea, L. kunthiana, L. lehmannii, L. linearifolia, L.
lycopodioides (=Oligandra lycopodioides), L. nitens, L. recurva, L. tomentosa
Jalcophila
3, S. America
J. boliviensis, J. ecuadoriensis, J. peruviana
Belloa
9, Andean Venezuela to Chile
B. chilensis (=Lucilia araucana, L. nivea, Freire 1986b)., B. kunthiana (=Lucilia conoidea, Freire
1986b), B. lehmannii, B. longifolia, B. pickeringii, B. piptolepis, B. plicatifolia, B. radians, B.
schultzii
Author's personal copy
References
Systematics of the Lucilia group
Table 1 Comparison of the genera composition of Lucilia group and its genera (in bold face taxa with different placement) through the treatments
123
123
Table 1 continued
Genera
Nr of species and distribution
Species
South American
Lucilia group
Berroa
1, Brazil, Uruguay, Argentina
B. gnaphalioides
Chevreulia
5, Brazil, Bolivia, Paraguay, Uruguay,
Chile, Argentina and Falkland Islands
C. acuminata, C. diemii, C. lycopodioides, C. pusilla, C. sarmentosa
Cuatrecasasiella
2, Andean Ecuador to Argentina
C. isernii, C. argentina
Facelis
3, Brazil, Peru, Bolivia, Paraguay, Chile,
Uruguay, Argentina
F. lasiocarpa, F. plumosa, F. retusa
Gamochaetopsis
1, Andean Chile, Argentina
G. alpina (=Lucilia alpina)
Jalcophila
3, Andean Ecuador, Peru, Bolivia
J. boliviensis, J. ecuadoriensis, J. peruviana
Lucilia
8, Brazil, Paraguay, Uruguay, Argentina,
Andean Bolivia, Argentina, Chile
L. acutifolia, L. eriophora, L. ferruginea, L. linearifolia, L. lycopodioides, L. nitens, L. recurva, L.
tomentosa
Luciliocline
5, Andean Peru, Bolivia, Argentina
L. burkartii, L. catamarcensis, L. lopezmirandae (=L. turneri), L. santanica (=L. spathulifolia), L.
subspicata
Dillon (2003), 13
genera
Belloa
1, Austral Chile and Argentina
B. chilensis
Lucilia group
Berroa
1, S. America
B. gnaphalioides
Chevreulia
6, Austral S. America
None mentioned
Chionolaena
(including
Leucopholis)
Not stated
None mentioned
Cuatrecasasiella
2, Northern and Southern Andes
None mentioned
Facelis
Not stated
None mentioned
Gamochaeta
c. 80, New World
G. boliviensis (=Jalcophila boliviensis), None mentioned
Gamochaetopsis
1, Andean Chile and Argentina
G. alpina (=Lucilia alpina)
Jalcophila
3, Northern Andes
J. colombiana, J. ecuadoriensis, J. peruviana
Lucilia
12, Brazil, Paraguay, Uruguay,
Argentina, Andean Venezuela to Chile
L. acutifolia, L. araucana, L. conoidea, L. eriophora, L. ferruginea, L. kunthiana, L. linearifolia, L.
lycopodioides, L. nitens, L. nivea, L. recurva, L. tomentosa
Luciliocline
13 Andean Venezuela to Chile and
Argentina
L. burkartii, L. catamarcensis, L. longifolia, L. lopezmirandae, L. pickeringii, L. piptolepis, L.
plicatifolia, L. radians, L. santanica, L. schultzii, L. spathulifolia, L. subspicata, L. turneri
Micropsis
Not stated, S. America
None mentioned
Stuckertiella
Not stated, S. America
None mentioned
Author's personal copy
References
S. E. Freire et al.
Author's personal copy
Systematics of the Lucilia group
(Appendix 1 in ESM). Trees were rooted with Relhania as
outgroup.
Using DNA obtained from plants collected in wild
populations and dried in silica gel, or from herbarium
material, a total of 117 sequences (representing 36 species)
were generated for this study, while 64 sequences (for 20
species from the outgroups) were obtained from GenBank
(see Appendix 1 in ESM). A complete list of the specimens
used in this study, the locality where each specimen was
collected, the herbarium voucher information and GenBank
accession numbers are shown in the Appendix 1 in ESM.
increase the yield of PCR reactions. The annealing temperatures ranged between 48 and 52 °C for the chloroplast
markers and 56–60 °C for the nuclear markers. PCR products were electrophoresed on a 1 % TBE agarose gel
stained with SYBR safe DNA gel stain (Invitrogen, Brazil).
Macrogen Inc. (Korea) performed the cleaning of the PCR
products using the Montage PCR purification kit from
Millipore following the manufacturer’s protocol.
Sequencing reactions were also performed by Macrogen
Inc.
Sequence analyses
Morphological characters
For the morphological matrix, 21 ingroup taxa and 12
outgroup taxa (Achyrocline ramosissima, A. tomentosa,
Antennaria dioica, Chionolaena arbuscula, C. campestris,
Gamochaeta serpyllifolia, Loricaria colombiana, Micropsis dasycarpa, Mniodes andina, Pseudognaphalium badium, P. lacteum, Stuckertiella capitata), were analyzed
using 35 morphological characters taken from a previous
work (Anderberg and Freire 1991) and adding the following character, i.e., leaves not densely imbrıcate (0)/
densely imbricate (1) (Appendix 2 in ESM). Characters
were taken from direct examination of herbarium specimens (Appendix 1 in ESM), and information was completed from literature (Anderberg and Freire 1991).
Molecular methods
Total genomic DNA from silica-dried material was
extracted using a modified CTAB protocol from Doyle and
Dickson (1987), while exactions from herbarium material
were performed using the DNeasy Plant Mini Kit (QIAGEN Inc., Hilden, Germany). Genomic DNA was used as a
template to amplify four regions: the chloroplast fragment
containing the trnL (UAA) intron and the intergenic spacer
between the trnL (UAA) 30 exon and the trnF (GAA) gene
(trnL-F region) using primers C and F from Taberlet et al.
(1991); the rpl32-trnL intergenic spacer (chloroplast) using
primers rpl32F and trnL(UAG) from Shaw et al. (2007);
the nuclear region ETS using the reverse primer 18S-ETS
(Baldwin and Markos 1998) and one of the following
forward primers: AST1, ETS1 or ETS2 (Bayer et al. 2002);
and the nuclear marker ITS using the primers ITS4 and
ITS5 from White et al. (1990).
Polymerase chain reactions (PCR) were carried out on
25 ll volumes, each reaction containing between 50 and
100 ng of DNA, 1.5 U of Taq polymerase (Invitrogen Life
Technologies, São Paulo, Brazil), 19 PCR buffer, 5 mM
MgCl2, 0.2 mM of each primer and 0.025 mM dNTP each.
In species for which these protocols were unsuccessful,
0.4 % bovine serum albumin was included as additive to
Sequence data were edited and contigs assembled using the
program Chromas Pro ver. 1.34 (Technelysium Pty, Ltd,
Tewantin, Australia), and the matrix was edited using the
software BioEdit (Hall 1999). Sequences were aligned
using the program MAFFT (http://mafft.cbrc.jp/alignment/
server/; Katoh et al. 2002), using the default parameters
and an automatic alignment strategy, with subsequent
visual inspection and manual revision. Data matrices are
deposited on TreeBase (accession number 16182).
Phylogenetic analyses
Three maximum parsimony analyses were conducted, the
first including only the nuclear markers, the second
including the complete molecular data set and the third
combining the molecular information with the morphological data in a combined analysis (Nixon and Carpenter
1996). Searches were carried out using the software TNT
(Goloboff et al. 2008), with the characters equally weighted and considering gaps as missing data. The heuristic
searches were performed as follows: 1,000 series of random addition sequences (RAS), swapping the trees with
tree bisection-reconnection (TBR), plus an additional
rearrangement of all the most parsimonious trees found.
Branch support was evaluated using Jackknifing (JK; Farris
et al. 1996), which was calculated by performing 5,000
pseudoreplicates, each consisting of 10 RAS.
Bayesian inference of phylogeny with posterior probabilities (PP) was conducted with MrBayes ver. 3.2.2
(Huelsenbeck and Ronquist 2001; Ronquist and Huelsenbeck 2003) for the three combined analyses mentioned
above. The models of molecular evolution were selected
using the Akaike Information Criterion (AIC) as implemented in jModelTest ver. 2.1.4 (Table 2; Guindon and
Gascuel 2003; Darriba et al. 2012). The chosen models
were GTR ? G for rpl32-trnL, trnL-F, ETS and
GTR ? I ? G for ITS. The standard discrete model was
used for the morphological data (Lewis 2001). Searches
used default settings for all parameters. Four simultaneous
independent runs initiated from random start trees were run
123
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0.36
Each region its
model ? standard discrete
model
0.69
Each region
its model
0.69
Each region
its model
–
GTR ? G
0.47
1,857
1,672
0.67
912
0.52
–
–
10
24
8
–
651
2,953
2,917
1,143
302
944
60
617
for 10 million generations, sampling from the posterior
distribution of trees every 1,000 generations (for a total of
10,000 samples). Several strategies were employed to
confirm that chains had achieved stationarity and the
appropriate burn-in for each analysis was determined: (1)
we plotted overall—lnL, (2) we examined the standard
deviation of split frequencies, (3) we examined the
potential scale reduction factor (PSRF) and (4) we
checked graphically the convergence of the MCMC by
monitoring the cumulative posterior split probabilities and
among-run variability of split frequencies using the online
tool AWTY (Wilgenbusch et al. 2004). A total of 25 % of
the samples were discarded as burn-in.
Bayesian posterior probabilities (PP) values were
described as high (0.95–1.00), moderate (0.90–0.94) and
low (0.50–0.89), while parsimony jackknife (JK) values
were described as high, (90–100 %), moderate (70–89 %)
and low (B69 %). Jackknife values of less than 50 %,
though extremely low, were also considered since in some
cases they can be showing just lack of information instead
of inconsistencies in the phylogenetic signal (Goloboff
et al. 2003). Nodes with Bayesian posterior probabilities
of less than 0.5 were considered as unsupported and the
values are not reported.
Indices and number of steps were calculated excluding uninformative characters
–
GTR ? G
–
GTR ? G
–
GTR ? I ? G
Model of molecular
evolution
Retention index
–
–
–
–
–
–
Consistency index
Number of steps
–
–
Number of most
parsimonious tres
–
830
87
636
507
Parsimony
informative
characters
153
149
Results
Aligned length (bp)
–
56
56
–
55
–
465 (G. uliginosum) to
485 (R. pungens)
43
39
436 (Leontopodium) to
692 (R. pungens)
54
Sequence length
(bp)
45
123
Number of taxa
605 (S. muelleri) to 626
(P. serpyllifolia)
814 (L. nitens and L. acutifolia) to
852 (Pseudognaphalium)
Molecular
data set
rpl32-trnL
ETS
ITS
Table 2 Main characteristics and results for the different regions and datasets analyzed
trnL-F
ITS ? ETS
Simultaneous analysis
S. E. Freire et al.
In total we included in the analyses 54 ETS sequences, of
which 35 are new; 45 ITS sequences, of which 28 are new;
39 rpl32-trnL, intergenic spacer sequences, of which 28
are new; and 43 trnL intron intergeneric spacer sequences,
from which 26 are new (Appendix 1 in ESM). The main
characteristics of the datasets, along with the corresponding tree statistics are summarized in Table 2.
Both Parsimony and Bayesian inference analyses
showed highly congruent topologies for molecular data or
combination of molecular data and morphological characters. All the analyses showed short branches for the
Lucilia group, mainly in the nodes (Figs. 1, 2, 3).
The analysis of the plastid markers resulted in a highly
polytomized tree, with almost no support and no resolution below the node that groups the FLAG clade (tree not
shown), so they are not described here.
Nuclear markers (ITS?ETS)
The nuclear markers combined showed that the Lucilia
group as previously circumscribed is not monophyletic,
due to the inclusion of Antennaria, Gamochaeta, Stuckertiella, Micropsis, Loricaria, Chionolaena and Mniodes
(Fig. 1) in a high supported clade for the Bayesian analysis (0.99 PP, 3 % JK). Most of the basal nodes (from the
Author's personal copy
Systematics of the Lucilia group
Fig. 1 Consensus phylogram
obtained from the Bayesian
analysis of ITS ? ETS
sequences (nuclear markers).
Bayesian posterior probabilities
(PP) and Jackknife values from
the parsimony analyses are
shown associated with the
branches. An asterisk indicates
a branch missing from the
parsimony analysis. Dotted
branches were shortened to
have a clearer topology
Relhania pungens
Pseudognaphalium lacteum
Pseudognaphalium badium
1.00/99
1.00/100
Achyrocline tomentosa
Achyrocline ramosissima
Helichrysum stoechas
0.71
/60
1.00/76
Anaphalis nepalensis
Anaphalis margaritacea
Vellereophyton dealbatum
0.99
1.00/98
Cassinia longifolia
/24
Acanthocladium dockeri
0.90
/29
Edmondia sesamoides
0.68
/* 0.75
Stuartina muelleri
/*
Ewartia catipes
0.88/*
Plecostachys serpyllifolia
Gnaphalium uliginosum
1.00/100
Leontopodium alpinum
Leontopodium microphyllum
Logfia gallica
0.54
Filago eriocephala
/*
1.00/100
Filago lutescens
0.80
1.00/99 Filago fuscescens
0.87/14
/55
Filago pyramidata
1.00/99
Antennaria dioica
FLAG
Antennaria chilensis
clade
0.52/*
Chevreulia acuminata
1.00/99
Cuatrecasasiella argentina
0.89
/*
Jalcophila boliviensis
0.76/41
Jalcophila ecuadoriensis
0.55/10
0.99
Loricaria colombiana
/81
1.00/81
Belloa longifolia
Belloa plicatifolia
0.99
Belloa piptolepis
/53
Belloa schultzii
0.78/*
0.99
0.81 Luciliocline subspicata
/3
Luciliocline santanica
/ * 0.83
/*
Luciliocline lopezmirandae
Lucilia group
Belloa kunthiana
0.99
/58
sensu lato
Mniodes andina
Gamochaetopsis alpina
1.00/99
Gamochaeta serpyllifolia
1.00/89
Stuckertiella capitata
0.78
/55 1.00/99
Gamochaeta longipedicellata
Gamochaeta americana
1.00
/70
Belloa chilensis
Chionolaena arbuscula
1.00/96
0.75/68
Chionolaena campestris
0.81/41
Lucilia linearifolia
Berroa gnaphalioides
0.98
/44
Facelis retusa
0.99/67
Facelis plumosa
0.84/26
Micropsis dasycarpa
0.86/36
Lucilia lycopodioides
0.78/36
Lucilia acutifolia
0.05
Lucilia nitens
outgroups) were lost in the parsimony analysis, having a
tree with more polytomies as a result of that analysis
(Fig. 1). However, inside the Lucilia group s.l. both analyses showed almost the same topology (with the exception
of the placement of the Antennaria clade, and the inner
structure of the Belloa ? Luciliochline ? Mniodes
clade) (Fig. 1). Since the clades of the Lucilia group s.l. are
also present in the other analyses, they will be discussed in
detail below, in the combined analysis.
Complete molecular data set (trnL-F ? rpl32trnL ? ITS ? ETS)
The analysis of the four molecular markers (Fig. 2)
recovered the same topology provided by the nuclear
1.00/100
analysis, with two exceptions: Micropsis is grouped
together with two species of Facelis (vs. with three
species of Lucilia in the nuclear analysis; Fig.1) and
Luciliocline subspicata is placed in a basal polytomy of
the Belloa pp ? the remaining two species of Luciliocline?Mniodes clade (Fig. 2) (vs. grouped with the
remaining two species of Luciliocline in nuclear DNA
analysis; Fig. 1). The major difference between the
parsimony and the Bayesian analyses is that the first
fails to recover the Lucilia group s.l. as monophyletic
(Fig. 2), but instead places the major clades that conform it as a polytomy (not shown). Since the polytomy
does not contradict the topology obtained in the
Bayesian analysis, we consider the results of this analysis as valid.
123
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S. E. Freire et al.
Relhania pungens
Oedera squarrosa
Vellereophyton dealbatum
Cassinia longifolia
Acanthocladium dockeri
Edmondia sesamoides
Stuartina muelleri
Ewartia catipes
1.00/100 Pseudognaphalium lacteum
Pseudognaphalium badium
1.00/100
Achyrocline ramosissima
1.00/99
Achyrocline
tomentosa
0.71/57
Helichrysum stoechas
0.51/47
Anaphalis margaritacea
1.00/87
Anaphalis nepalensis
Plecostachys serpyllifolia
Gnaphalium uliginosum
Leontopodium microphyllum
1.00/100
Leontopodium alpinum
Logfia gallica
Filago
eriocephala
1.00/100
Filago lutescens
0.96/69
1.00 Filago fuscescens
/99 Filago pyramidata
Antennaria chilensis
1.00/100
Antennaria dioica
Chevreulia acuminata
1.00
/99
Cuatrecasasiella argentina
0.60
Jalcophila boliviensis
/57
Jalcophila ecuadoriensis
Loricaria colombiana
1.00
Belloa plicatifolia
/83
0.63/*
0.99 Belloa kunthiana
1.00
/75 Mniodes andina
/87
Luciliocline santanica
0.79
/*
Luciliocline lopezmirandae
0.99
Belloa longifolia
/78 0.89
/*
Belloa piptolepis
Belloa schultzii
Luciliocline subspicata
Belloa chilensis
0.99/82
1.00/99
Chionolaena arbuscula
Chionolaena campestris
0.81
/38
Lucilia linearifolia
0.89
Berroa gnaphalioides
/46
Micropsis dasycarpa
1.00
Facelis retusa
/74 1.00/99
Facelis plumosa
1.00 0.90
/73
/86
Lucilia acutifolia
1.00
Lucilia lycopodioides
/82 0.99
/75
Lucilia nitens
Gamochaeta longipedicellata
1.00/99
Gamochaeta americana
0.91
/71
Stuckertiella capitata
0.99
/75 1.00 Gamochaetopsis alpina
/99
Gamochaeta serpyllifolia
1.00/99
0.99/61
0.66
/*0.51
/*
1.00/97
Crown
radiation
clade
0.51/59
0.95/*
0.68/*
0.86
/*
0.99
/70
FLAG
clade
0.91/*
0.99/*
Lucilia group
sensu lato
0.59/*
0.03
Fig. 2 Consensus phylogram obtained from the Bayesian analysis of
the complete molecular dataset (ITS ? ETS ? rpl32-trnL intergenic
spacer ? trnL intron ? trnL-F intergenic spacer sequences). Bayesian posterior probabilities (PP) and Jackknife values from the
parsimony analyses are shown associated with the branches. An
asterisk indicates maximum support for both analyses (i.e.,[0.99 and
98 %). Dotted branches were shortened to have a clearer topology
Combined analysis (molecular data ? morphological
characters)
Stuartina, and Ewartia (clade 1, 0.84 PP); a second one
(clade 2, 1.00 PP, 100 % JK), was constituted by the genera
Pseudognaphalium (P. badium. P. lacteum), Helichrysum
(H. stoechas), Anaphalis (A. nepalensis, A. margaritacea),
and Achyrocline (A. tomentosa, A. ramosissima); the third
one (clade 3, 0.91 PP) was constituted by Plecostachys serpyllifolia and Gnaphalium uliginosum, and the forth clade
(clade 4, 0.96 PP, 70/JK) comprised the rest of the genera
included in the analyses.
One major clade can be identified within clade 4, which
is missing in the parsimony analysis (Fig. 3): clade C (1.00
PP) subdivided into clade C.1 (1.00 PP, 100 % JK)
including Antennaria chilensis and A. dioica; clade C.2
Considering both the Parsimony and the Bayesian combined analyses, the Bayesian inference gave the highest
resolution. Therefore, we adopt the hypothesis obtained
from Bayesian analysis for description and discussion of
the results. This topology is shown with the addition of PP/
JK values (Fig. 3).
From the topology inferred by Bayesian analysis, and
following the Relhania and Oedera clades, four clades
were recovered. One, clade was constituted by six genera,
Vellereophyton, Cassinia, Acanthocladium, Edmondia,
123
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Systematics of the Lucilia group
Relhania pungens
Oedera squarrosa
Clade 2
1.00/99
Clade 1
Vellereophyton dealbatum
Cassinia longifolia
Acanthocladium dockeri
0.98
/62
Edmondia sesamoides
0.66
Stuartina muelleri
/*0.51
/*
Ewartia catipes
Pseudognaphalium lacteum
1.00/100
1.00/97
Pseudognaphalium badium
1.00/100
Helichrysum stoechas
Crown
Anaphalis nepalensis
0.76 1.00/86
radiation
/58
Anaphalis margaritacea
clade
Achyrocline tomentosa
1.00/100
Achyrocline ramosissima
0.91/*
Plecostachys serpyllifolia
Gnaphalium uliginosum Clade
1.00/100
Leontopodium microphyllum
A
Leontopodium alpinum
0.66
Logfia gallica
/*
0.83
Filago eriocephala
/*
1.00/100
B
Filago lutescens
0.80
0.99
/69 1.00 Filago fuscescens
/70
/99
Filago pyramidata
FLAG
1.00/100
Antennaria chilensis
C1
clade
Antennaria dioica
Chevreulia acuminata
1.00
0.94
C2
/99
/*
Cuatrecasasiella argentina
0.98
Jalcophila boliviensis
a
/94
Jalcophila ecuadoriensis
0.60
Loricaria colombiana
1.00
/44
/92
Belloa plicatifolia
Belloa schultzii
1.00 0.91
/95
Belloa longifolia
1.00
/* 0.72
/*
/*
Belloa piptolepis
b C3
1.00
Lucilia group
0.77
Belloa kunthiana
/*
/*
Mniodes andina
sensu lato
Luciliocline subspicata
0.86
Luciliocline
santanica
/* 0.97
/*
Luciliocline lopezmirandae
Belloa chilensis
0.75
a
Chionolaena arbuscula
/78
1.00/99
Chionolaena campestris
0.77
Lucilia linearifolia
/71
Berroa gnaphalioides
1.00
Lucilia lycopodioides
/90 0.99/89
1.00
Lucilia nitens
b
/*
Lucilia acutifolia
1.00
0.71
1.00/99
/87
/*
Facelis retusa
C4
1.00
Facelis plumosa
/90
Micropsis dasycarpa
Gamochaeta longipedicellata
1.00/99
Gamochaeta americana
1.00
/94
Stuckertiella capitata
c
0.99
/72 1.00 Gamochaetopsis alpina
/98
Gamochaeta serpyllifolia
0.04
0.84/*
Clade 4
3
Fig. 3 Consensus phylogram obtained from the bayesian combined
analysis (molecular data set ? morphology). Bayesian posterior
probabilities (PP) and Jackknife values from the parsimony analyses
are shown associated with the branches. An asterisk indicates a
branch missing from the parsimony analysis. Resolution of clade C1
in the parsimony analysis. Dotted branches were shortened to have a
clearer topology
(1.00 PP, 99 % JK) including Chevreulia acuminata and
Cuatrecasasiella argentina; clade C.3 (1.00 PP, 92 % JK)
with two subclades, C.3a (0.98 PP; 94 % JK) including
Jalcophila boliviensis and J. ecuadoriensis; and subclade
C.3b (1.00 PP, 95 % JK) including Loricaria colombiana,
Belloa plicatifolia, B. schultzii, B. longifolia, B. piptolepis,
B. kunthiana, Mniodes andina, Luciliocline subspicata, L.
santanica, and L. lopezmirandae. Finally, clade C.4 (1.00
PP, 87 % JK) which could be subdivided into subclades,
subclade C.4a (0.75 PP, 78 % JK) including Belloa chilensis,
Chionolaena arbuscula, C. campestris; subclade C.4b (1.00
PP, 90 % JK) including Lucilia linearifolia, Berroa gnaphalioides, Lucilia lycopodioides, L. nitens, L. acutifolia,
Facelis retusa, F. plumosa, and Micropsis dasycarpa; and
subclade C.4c (1.00 PP, 94 % JK) including Gamochaeta
longipedicellata, G. americana, Stuckertiella capitata,
Gamochaetopsis alpina, and Gamochaeta serpyllifolia.
Two minor clades can be also identified within clade 4
(Fig. 3): clade A (1.00 PP, 100 % JK) and clade B (0.83
PP) composed of the genera Leontopodium, and
123
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S. E. Freire et al.
Logfia + Filago, respectively. These two clades were
recovered as sister clades of clade C.
Discussion
The present analyses of Gnaphalieae are consistent with
previous phylogenies (Bergh and Linder 2009; Ward et al.
2009; Galbany-Casals et al. 2010; Smissen et al. 2011)
showing a relatively small southern African clade, i.e.,
‘Relhania and Oedera clades’ at the base and then a ‘crown
radiation’ including African and non-African taxa. Within
the ‘crown radiation’ two of the four clades recovered are
also equivalent to those found in previous phylogenies
(Bergh and Linder 2009; Ward et al. 2009; Galbany-Casals
et al. 2010; Smissen et al. 2011), i.e., clade 2 formed by
Helichrysum, Anaphalis and Pseudognaphalium, called
HAP clade (for the first letters of the genera, according to
Smissen et al. 2011) which showed the maximum statistical
support (Figs. 2, 3) and the highly supported clade 4,
formed by Filago, Logfia, Leontopodium, Antennaria,
Gamochaeta, called FLAG clade (for the first letters of the
large genera, according to Galbany-Casals et al. 2010)
(Figs. 2, 3), principally distributed in Eurasia and America.
Clade 3 comprises Gnaphalium uliginosum and Plecostachys serpyllifolia (with moderate support in the combined analyses; Fig. 3), both belonging to subtribe
Gnaphaliinae (Anderberg 1991). Unlike Bergh and Linder’s (2009) phylogeny, Plecostachys serpyllifolia, from
South Africa, was not grouped within the FLAG clade.
Clade 1 comprises six taxa (with low support in the
combined analyses; Fig. 3): Vellereophyton dealbatum
(subtribe Gnaphaliinae-Gnaphalium group; Anderberg
1991), from South Africa, as sister species to two subclades: the first one was composed of Edmondia sesamoides
(subtribe Gnaphaliinae-Syncarpha group; Anderberg 1991)
from South Africa, and two Australian species, Ewartia
catipes (subtribe Casssiniinae-Anaphalis group; Anderberg
1991), and Stuartina muelleri (subtribe Gnaphaliinae
-Gnaphalium group; Anderberg 1991); and a second
subclade was composed of two other Australian species,
Acanthocladium dockeri (subtribe Cassiniinae; Anderberg
1991) and Cassinia longifolia (subtribe Casssiniinae-Cassinia group; Anderberg 1991).
From these four clades, only clade 2 (HAP clade) is
recovered in the phylogeny of Gnaphaliinae by Anderberg
(1991) The remaining three clades show, as was previously
noted (Bayer et al. 2000, 2002; Ward et al. 2009; GalbanyCasals 2010; Smissen et al. 2011), with the necessary
caution due to the limited sampling of our study, that DNA
data do not support some of the relationships among groups
of genera and subtribes identified by Anderberg (1991), for
example in clade 4 (FLAG clade), Leontopodium and
123
Logfia ? Filago are related to Antennaria (instead of
Leontopodium and Filago placed in the subtribe Gnaphaliinae, and Antennaria placed in the subtribe Cassiniinae),
or in clade 1, Acanthocladium and Cassinia are related to
Edmondia and Stuartina (instead of Acanthocladium and
Cassinia placed in subtribe Cassiniinae, and Edmondia
together with Stuartina in subtribe Gnaphaliinae, but in
different groups, i.e., Syncarpha group and Gnaphalium
group, respectively).
In general, South American taxa of Gnaphalieae have
not been sampled in previous molecular phylogenetic
analyses. Only Ward et al. (2009) included Jalcophila and
Mniodes in their phylogeny of Gnaphalieae, in which
Jalcophila (J. peruviana), Mniodes (M. andina) and
Gamochaeta (G. pensylvanica) are all part of the ‘crown
radiation’.
Generic composition of the Lucilia group s. lat.
The analysis of the complete molecular data set, and
molecular data combined with morphological characters
showed that the Lucilia group, as previously circumscribed,
is not monophyletic. The combined analysis showed that
the genera of the Lucilia group sensu Anderberg and Freire
are grouped with seven other genera (clade C, Fig. 3):
Gamochaeta is distributed in America with some species
known as cosmopolitan weeds, Stuckertiella, Micropsis,
Loricaria and Mniodes from South America, Chionolaena
found in Central and South America, and Antennaria
mainly distributed in Northern Hemisphere with only three
species known from South America. Four of these genera
were previously placed by Anderberg (1991) in subtribe
Loricariinae (Loricaria and Mniodes) and subtribe Casssiniinae (Antennaria and Chionolaena). The relationship
between these last two taxa of the tribe Cassiniinae and
other members of the Lucilia group was previously suggested by Dillon (2003).
Anderberg and Freire (1991) diagnosed the South
American Lucilia group by its very slender pappus bristles
which are often connate in groups, dorsally pubescent style
branches and polychromous involucral bracts. Only one
morphological synapomorphy, i.e., slender pappus bristles
basally connate or coherent at the base by patent cilia, was
found for the ancestral node that defines the present
arrangement of Lucilia group s. lat. Although, only two of
c. 50 species of Antennaria were sampled in this study, and
it possesses pappus bristles basally with patent cilia (vs.
connate in the remaining taxa of Lucilia group), this genus
was tentatively included here in this group.
Within these mainly American members, called Lucilia
group s. lat., two main groups were recovered with our
sampling. The first one (clade C2 ? C3, Fig. 3), comprises
Chevreulia, Cuatrecasasiella, Jalcophila, Loricaria,
Author's personal copy
Systematics of the Lucilia group
Belloa pro parte, Mniodes and Luciliocline, principally
characterized by having caespitose, subcaespitose or cushion forming habit (rarely shrubs), with leaves arranged in
rosettes or densely imbricate, and achenial trichomes globose or clavate (rarely elongated) (Table 3; Figs. 4, 6g).
The second one (clade C4, Fig. 3) comprised Belloa chilensis, Chionolaena, Lucilia, Berroa, Facelis, Micropsis,
Gamochaeta, Stuckertiella and Gamochaetopsis, principally characterized by having ascending or erect stems
(rarely prostrate), with leaves commonly scattered, and
achenial trichomes elongated (Table 3; Figs. 5, 6i). They
also conform, each one, two geographical well-defined
groups. In fact, the genera of clade C4 occur mainly at low
altitude areas in southern Brazil, Uruguay, eastern Paraguay
and northern Argentina, but except Berroa and Micropsis,
they also include species from some part of the Andes.
Conversely, most genera of the clade C2?C3 are endemic
to the Andes; only Chevreulia includes species from low
altitudes. A minor third group (clade C1, Fig. 3) was also
recovered with our sampling which comprises the genus
Antennaria, from artic to temperate regions of the Northern
hemisphere with only three species in the Andes of South
America, and principally characterized by having dioecious
and often apomictic habit, with ascending or erect stems,
leaves alternate, often rosulate and achenial trichomes
usually clavate.The genus Mniodes was also considered by
Merxmüller et al. (1977) to be a member of the Lucilia
group. However, Anderberg (1991) placed Mniodes with
Loricaria (Fig. 4b) in the subtribe Loricariinae because of
its dioecy habit. Our results show that both genera are
nested within clade C of the Lucilia group (Figs. 1, 2, 3).
The close relationship between Facelis and Micropsis
(Fig. 5c, d) had been previously recognized by Dillon
(2003). Micropsis, which is a genus of five species
restricted to South America, was defined by paleaceous
receptacles where paleae enclose the florets, and consequently associated with the genera of the Filago group by
Anderberg (1991). As such, the strong support in the
combined analysis (Fig. 3) for the clade of Micropsis ? Facelis confirms the inclusion of Micropsis in the
Lucilia group.
The genus Chionolaena (Fig. 5f) was considered by
Merxmüller et al. (1977) to be a member of the Lucilia group.
Later, Anderberg (1991) placed Chionolaena (including
Leucopholis), in the Anaphalis group (subtribe Cassiniinae),
principally diagnosed by having disc florets functionally
male. Subsequently, Dillon (2003) suggested a close potential relationship between Chionolaena and the other members of the Lucilia group. Our results are consistent with
those of Merxmüller et al. and Dillon’s placement of genus
Chionolaena within the Lucilia group (Fig. 3).
Anderberg and Freire (1991) considered Gamochaeta to
be the sister taxon of the Lucilia group. Gamochaeta
(Fig. 5h) was not considered by these authors as belonging
to the Lucilia group, since it possesses truncate style branches apically pilose (vs. style branches dorsally pilose,
Fig. 6a–e). Dillon (2003) suggested a relationship between
Gamochaeta and other members of the Lucilia group, which
was confirmed by our results, which show that Gamochaeta
and its sister genus Stuckertiella (Fig. 5i) are nested with
Gamochaetopsis (Fig. 5g) within clade C (Fig. 3).
In our analyses including molecular markers and a combination of molecular and morphological data, some main
clades correspond to those recognized in previous morphological phylogenies. As such, for discussion of systematic
relationships of Facelis, Chevreulia, Cuatrecasasiella and
Jalcophila we refer to Anderberg and Freire (1991) with
which our phylogenetic inferences are congruent. Gnaphaliothamnus, which was considered as a synonym of Chionolaena (Nesom 2001; Loeuille et al. 2011) or as a distinct
genus (Nesom 1990b, c; Anderberg 1991; Freire 1993), and
Raouliopsis, have not been included in our analyses, so their
phylogenetic positions remain untested.
Placement of the Lucilia group s. lat.
The position of Lucilia group s. lat., as defined in the
present study, is the same in all trees, with Leontopodium,
and Filago within the clade 4, i.e., the FLAG clade
(Figs. 1, 2, 3). Smissen et al. (2011) hypothesized 2n = 14
as the base number for the tribe Gnaphalieae and a 2n = 28
ancestor for the FLAG clade (derived from 2n = 14 by
polyploidy), showing multiple shifts from 2n = 14 to
2n = 28 in the tribe. In this sense, the counts of 2n = 28,
56, 62, 63, 70, 80, 84, 85, 100 in Antennaria, Chouksanova
et al. 1968; Juel 1900; Jörgensen et al. 1958; Löve and
Löve 1982a, b; Packer and McPherson 1974; UrbanskaWorytkiewicz 1967; n = 14 in Chionolaena lavandulifolia
(=Gnaphalium lavandulifolium), De Jong and Longpre
1963; n = 14 in Gamochaeta spiciformis, Moore 1981;
n = ca. 14 in Loricaria thuyoides Turner et al. 1967;
2n = 28 in Lucilia acutifolia and L. nitens, Freire 1986c;
n = 12 in Luciliocline subspicata (=Belloa punae), Fernández Casas and Fernández Piqueras 1981; and n = 11–12
in Stuckertiella capitata, Spooner et al. 1995, are consistent
with Smissen et al. hypothesis and provide good evidence
that the Lucilia group is part of the FLAG clade.
Taxonomic implications
Monophyly of Belloa and its relationships with Luciliocline
and Mniodes
Our results suggest that Belloa sensu Cabrera (1958) and
sensu Anderberg and Freire (1991) is not monophyletic.
Instead, these results are consistent with Dillon’s study
123
123
Table 3 Morphological characters of the genera of Lucilia group s. lat. (key characters in bold face)
Monoecious/dioecious
Leaf disposition
Capitula
pedunculate
at maturity
Disc florets
Sweepinghairs of style
branches
Florets
enclosed by
receptacular
paleae
Achenes
Achenial hairs
Pappus
Involucral bracts
Antennaria
Erect or
ascending
herbs
Dioecious (capitula
homogamous)
Alternate
2
All
functionally
male
Dorsally
2
Not
rostrate
Clavate
Dimorphic scabridcoherent at base
Monochromous
Belloa
Caespitose,
prostrate
herbs
Monoecious
Alternate
2
Perfect
Dorsally
2
Not
rostrate
Clavate to
elongated
Scabrrid-basally
connate
Polychromousstereome
entire
Berroa
Ascending
herbs
Monoecious
Alternate
2
Perfect
Dorsally
2
Not
rostrate
Elongated.
8–12
twisted
apically
Plumose (scabrid
above)-basally
connate
Polychromousstereome
entire
Chevreulia
Subcaespitose
Monoecious
Opposite or
rosulate
1
Perfect
Dorsally
2
Rostrate
Clavate
Scabrid-basally
connate
Polychromousstereome
entire
Chionolaeana
Shrubs
Subdiooecious (capitula
heterogamous)
Alternate
2
Functionally
male
Dorsally
2
Not
rostrate
Elongated
Barbellate-basally
connate
Monochromousstereome
entire
Cuatrecasasiella
Subcaespitose
Dioecious (capitula
homogamous)
Opposite
2
All
functionally
male
Dorsally
2
Not
rostrate
Absent
Scabrid-basally
connate
Monchromousstereome
entire
Facelis
Erect or
ascending
herbs
Monoecious
Alternate
2
Perfect
Dorsally
2
Not
rostrate
Elongated
Plumose (scabrid
above)—basally
connate
Polychromousstereome
divided
Gamochaeta
Erect or
ascending
herbs
Monoecious
Alternate
2
Perfect
Apically
2
Not
rostrate
Globose
Scabrid-basally
connate
Polychromousstereome
entire
(divided)
Gamochaetopsis
Prostrate to
ascending
herbs
Monoecious
Alternate
2
Perfect
Apically
2
Not
rostrate
Clavate
Scabrid-basally
connate
Polychromousstereome
divided
Jalcophila
Caespitose
herbs
Monoecious
Rosulate
1
Perfect
Dorsally
2
Not
rostrate
Clavate
Scabrid-basally
connate
Monochromousstereome
entire
Loricaria
Shrubs or
subshrubs
Dioecious (capitula
homogamous)
Densely
imbricatelaterally
compressed
2
All
functionally
male
Dorsally
2 (1)
Not
rostrate
Absent
Dimorphic-scabridbasally connate
Monochromousstereome
entire
Lucilia
Erect or
ascending
herbs
Monoecious or subdioecious
(capitula heterogamous,
rarely homogamous)
Alternate
2
Perfect or
functionally
male
Dorsally
2
Not
rostrate
Elongated
Scabrid (rarely
barbellate above)—
basally connate
Polychromousstereome
entire or
divided
Mniodes
Ascending to
caespitose
herbs
Monoecious or dioecious
(capitula hetero- or
homogamous)
Alternate,
rosulate or
densely
imbricate
2
Perfect or all
functionally
male
Dorsally
2
Not
rostrate
Globose
(rarely
elongated or
absent)
Mono or dimorphic
scabrid-basally
connate
Polychromousstereome
entire
(divided)
Author's personal copy
Habit
S. E. Freire et al.
Genus
Author's personal copy
Monochromousstereome
entire
Scabrid—basally
connate
Globose
2
Alternate
Subdioecious (capitula
heterogamous)
Prostrate to
ascending
herbs
Stuckertiella
2
Functionally
male
Apically
Not
rostrate
Monochromousstereome
entire
Absent or composed
of a short crown—
basally connate
1
Alternate
Monoecious
Caespitose
herbs
Micropsis
2
Perfect
Dorsally
Not
rostrate
Absent or
elongated
Involucral bracts
Monoecious/dioecious
Habit
Genus
Table 3 continued
Leaf disposition
Capitula
pedunculate
at maturity
Disc florets
Sweepinghairs of style
branches
Florets
enclosed by
receptacular
paleae
Achenes
Achenial hairs
Pappus
Systematics of the Lucilia group
(2003) that considered Belloa as a montotypic genus (B.
chilensis). In fact, all the analyses show that the type
species of Belloa (B. chilensis) of the Andes in the southern
part of the continent is nested in the strongly supported
clade C4 (Figs. 1, 2, 3), whereas the remaining sampled
species of Belloa (excluding type) distributed in the Andes
from Venezuela to north western Argentina were grouped
with Jalcophila, Loricaria, Mniodes and Luciliocline in an
also strongly supported clade C3 (Figs. 2, 3). The monotypic genus Belloa is here diagnosed by having prostrate
stems, caespitose, closely leafy, solitary capitula surrounded by the terminal leaves, tubular corollas and clavate
to elongate achenial trichomes (Figs. 5e, 6f, h, i).
Dillon (2003) transferred the remaining species of Belloa (except B. kunthiana) sensu Anderberg and Freire
(1991) to Luciliocline and diagnosed this genus by its
globose achenial trichomes (Fig. 6g). In this sense, Belloa
kunthiana because of its elongated achenial trichomes was
considered by this author as a member of the genus Lucilia
[Lucilia kunthiana (DC.) Zardini]. However, in contrast to
Dillon (2000, 2003), our results here showed Belloa kunthiana placed in the clade together with Belloa pro parte
(excluding type) (Figs. 1, 2, 3), and morphologically B.
kunthiana is more closely related to the other species of
Belloa than to Lucilia because of its prostrate stems with
rosulate leaves and leaf hairs with apical, flagellate cell
slightly swollen at the base (vs. ascending or erect stems
distantly leafy and leaf hairs with apical, flagellate cell
bulbose at the base in Lucilia). This suggests that the
resemblance of Belloa kunthiana to species of Lucilia
regarding its elongated achenial trichomes is due to parallel
evolution, which has led to non-monophyletic groups.
All the analyses showed the species of Luciliocline
sensu Dillon (but including Belloa kunthiana) as a strong
supported clade with Mniodes nested within it and Loricaria as its sister clade (Figs. 1, 2, 3). Mniodes and Loricaria (Fig. 4b–g) have little morphological similarity (i.e.,
leaves densely imbricate), but both were placed in the
subtribe Loricariinae by Anderberg (1991) because of their
dioecious habit. Instead, Mniodes is vegetatively similar to
the highly reduced Belloa species (Fig. 4d, e), and strong
support was recovered for the clade Mniodes andina ? Belloa kunthiana in the analysis of the four molecular data sets (Fig. 2) and low support in the Bayesian
combined analyses (Fig. 3). The phylogeny of the Lucilia
group suggests at least three independent acquisitions of
dioecy in Jalcophila clade, i.e., Loricaria, Mniodes, Cuatrecasasiella and other three independent acquisitions of
subdioecy (disc-florets functionally male) in the Belloa
clade, i.e., Chionolaena, Lucilia (Freire 1989) and Stuckertiella (Table 3). Since sex separation appears as an
evolutionary convergence and may be the consequence of
selective pressures particular to Andean environments, the
123
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S. E. Freire et al.
Fig. 4 Morphological diversity in the Lucilia group s. lat.-clade C2
and C3: a Jalcophila boliviensis (photo S. Beck), b Loricaria
colombiana (photo J.C. Ospina), c Mniodes piptolepis (photo F.
O. Zuloaga), d Mniodes kunthiana (photo E. Urtubey), e Mniodes
schultzii (photo R.I. Meneses), f Mniodes subspicata (photo E.
Urtubey), g Mniodes santanica (photo S. Beck), h Cuatrecasasiella
argentina (photo S. Beck) and i Chevreulia sarmentosa (photo M.
Bonifacino)
homogamous capitula cannot be a character diagnosing
Mniodes.
Although in our combined Bayesian analysis the species
of Luciliocline sensu Dillon appears as two subclades, i.e.,
the subclade Belloa pro parte with the genus Mniodes
closely related to Belloa kunthiana, and the subclade Luciliocline, they are moderately and weakly supported,
respectively (Fig. 3). In addition, as more specimens were
examined, traditional morphological features that characterized each subclade including prostrate stems forming
mats, being closely leafy, and solitary capitula (subclade
Belloa pro parte ? Mniodes), and ascending stems, distantly leafy with capitula arranged in glomerules (subclade
Luciliocline) showed overlapping, i.e., ascending stems
with capitula in glomerules are present in Belloa piptolepis.
Mniodes is the oldest generic epithet attached to this
clade; consequently, here we delimit subclade Belloa pro
parte ? Mniodes ? subclade Luciliocline as Mniodes (A.
Gray) Benth. (Figs. 3, 4c–g). Although there is no
unequivocal synapomorphy for Mniodes, based on our own
observations and literature, the species of this genus are
relatively small plants ranging from pulvinate-caespitose
with stems tightly compacted and densely leafy to subcaespitose with ascending stems densely leafy at the base,
with capitula sessile, globose achenial trichomes only
elongated in B. kunthiana and cytologically with a basic
haploid number of n = 12.
123
Placement of Jalcophila boliviensis
Jalcophila includes four species; two of them (J. boliviensis and J. ecuadoriensis) were sampled in this study. The
first one, J. boliviensis (Fig. 4a), was recognized as a
member of Jalcophila (Anderberg 1991; Anderberg and
Author's personal copy
Systematics of the Lucilia group
Fig. 5 Morphological diversity in the Lucilia group s. lat.-clade C4:
a Berroa gnaphalioides (photo M. Bonifacino), b Lucilia acutifolia
(photo M. Bonifacino), c Facelis retusa (photo M. Bonifacino),
d Micropsis dasycarpa (photo E. Urtubey), e Belloa chilensis (photo
M. Baeza), f Chionolaena costaricensis (photo M. Bonifacino),
g Gamochaetopsis alpina (photo N. Bayón), h Gamochaeta longipedicellata (photo S. Beck) and i Stuckertiella capitata (photo S.
Beck)
Freire 1991) but transferred to Gamochaeta by Dillon
(2003). Gamochaeta and Jalcophila boliviensis are distantly
related to each other in our results (Figs. 1, 2, 3). This
treatment is congruent with the observations of the morphological features and previous treatments (Anderberg and
Freire 1990b, 1991). Style branches of Jalcophila boliviensis
are dorsally papillose unlike those apically pilose in Gamochaeta. Involucral bracts of Jalcophila boliviensis are subequal, whereas in Gamochaeta the outermost bracts are
shorter than the inner bracts. The capitula of Jalcophila boliviensis are pedunculate at maturity unlike those usually
sessile in Gamochaeta. Jalcophila boliviensis shares these
123
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S. E. Freire et al.
Fig. 6 Micrographs of some members of the Lucilia group s. lat.: a–e
style branches of disc florets, a Cuatrecasasiella argentina (Urtubey
et al. 474-SI), b Gamochaeta neuquensis, (Ezcurra 120-SI),
c Gamochaetopsis alpina (Cabrera 5902-LP), d Lucilia nitens,
(Urtubey 390-SI), e Mniodes lopezmirandae (Urtubey and Freire
433-SI); f achene with elongated hairs (Belloa chilensis, Ezcurra
2262-BCRU), g achene with globose hairs (Mniodes lopezmirandae,
Urtubey and Freire 433-SI), h clavate achenial hairs (Gamochaetopsis
alpina, Cabrera 5902-LP), i elongated achenial hairs (Belloa
chilensis, Ezcurra 2262-BCRU) and j globose achenial hairs
(Gamochaeta grazielae, Deble and Deble 4501-SI). Scale bars a–d,
g, i 50 lm, e 100 lm, f 200 lm, h, j 20 lm
characters, i.e., dorsally papillose style branches, subequal
involucral bracts and pedunculate capitula, with J. ecuadoriensis, and both species also have 4-lobed perfect florets. In
addition, Jalcophila boliviensis and J. ecuadoriensis were
sister taxa in all the analyses, implying that the genus might
be monophyletic. The type of Jalcophila was not included in
our present analyses so the relationship between J. boliviensis and the generic type remains to be tested.
123
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Systematics of the Lucilia group
Monophyly of Lucilia and its relationships with Berroa,
Facelis and Micropsis
Lucilia, Berroa, Facelis and Micropsis formed a wellsupported clade within the clade C4 (Fig. 3). Facelis
characterized by its plumose bristles pappus, scabrid
above, and Micropsis characterized by it pappus absent or
composed of a short crown, also formed a well-supported
clade, and the first was monophyletic. The monotypic
genus Berroa, diagnosed by its achenes with elongated
8–12 twisted apically hairs, was placed in a basal politomy
inside clade C4. Conversely, all the analyses showed the
species of Lucilia sensu Anderberg and Freire, traditionally
diagnosed by their elongated achenial trichomes, scabrid
pappus and leaf hairs with apical, flagellate cell bulbose at
the base, as non-monophyletic. In fact, although four of its
eight species sampled in this study have been recognized as
distinct and belonging to Lucilia in previous treatments
(Freire 1986b; Anderberg 1991, Anderberg and Freire
1991; Dillon 2000, 2003), our data show Lucilia linearifolia in a basal politomy and the remaining three species of
Lucilia (L. lycopodioides, L. nitens, L. acutifolia) in a wellsupported clade sister of Facelis ? Micropsis. Lucilia
linearifolia occurs in southern Brazil and northwestern
Argentina and presents discolorous leaves. The remaining
sampled species exhibit similar distribution (except L. nitens that is found in southern Brazil, Uruguay and northeastern Argentina) and present concolorous leaves. Future
studies employing more variable DNA regions, with more
extensive sampling, will be valuable before a recircumscription of Lucilia can be proposed.
Monophyly of Gamochaeta and its relationships
with Stuckertiella and Gamochaetopsis
Our results suggest that Gamochaeta, as currently defined,
is not monophyletic. All the analyses showed the clade
Gamochaeta ? Stuckertiella ? Gamochaetopsis as highly
supported, as well as the clade Gamochaeta serpyllifolia ? Gamochaetopsis (Figs. 1, 2, 3). Stuckertiella is a
genus of two species confined to South America (Peru,
Bolivia, Argentina), and it was characterized by having
4-merous florets. Gamochaetopsis is a monotypic genus
restricted to austral Chile and adjacent Argentina, differentiated by its achenes with short clavate hairs. Gamochaeta includes c. 60 species (three were sampled in this
study) in the New World with some species adventives in
the Old World (Nesom 1990a). The close relationship
between Gamochaeta and Stuckertiella had been previously inferred in a morphological phylogenetic analysis
(Dillon 2000) and diagnosed by truncate apically pilose
style branches and achenes with globose myxogenic twin
hairs. Gamochaetopsis was recognized as an isolated
distinct genus (Anderberg and Freire 1991; Dillon 2000,
2003). The phylogeny of Gamochaeta is one of our
ongoing projects, so before synonymizing Gamochaetopsis
and Stuckertiella with Gamochaeta, we await the outcome
of that work.
Taxonomic treatment of the Lucilia group s. lat.
Morphological characters for each genus are shown in
Table 3. This treatment does not include the genera
Gamochaeta, Gamochaetopsis and Stuckertiella which will
be treated in a forthcoming paper.
Belloa J. Rémy in Gay, Fl. Chil. 3(3): 336. 1847. Type:
B. chilensis (Hook. and Arn.) J. Rémy
=Lucilia Cass. sect. Lucilioides DC., Prodr. 7: 46. 1838.
One species, S. America (southern Andes): Belloa
chilensis (Hook. and Arn.) J. Rémy, in Gay, Fl. Chil. 3(3):
336, t. 38. 1847 [=Lucilia chilensis Hook. and Arn.,
Chevreulia nivea Phil., Gnaphalium andicola Kuntze,
Lucilia araucana Phil., L. chilensis Poepp. and Endl., L.
frigida Reiche, L. nivea (Phil.) Cabrera]
Berroa Beauverd, Bull. Soc. Bot. Genève 5: 210. 1913.
Type: B. gnaphalioides (Less.) Beauverd
One species, S. America (S Brazil, Uruguay, C and NE
Argentina): Berroa gnaphalioides (Less.) Beauverd, Bull.
Soc. Bot. Genève 5: 211. 1913 (=Lucilia argentea Hook.
and Arn., L. gnaphalioides Less.)
Chevreulia Cassini, Bull. Soc. Philom. Paris, 1817: 69.
1817. Type: C. sarmentosa (Pers.) S.F. Blake
Six species, S. America (S Brazil, Bolivia, Paraguay,
Uruguay, Chile, N and C Argentina, Falkland Islands):
Chevreulia acuminata Less., Linnaea 5: 261.1830 (=C.
elegans Rusby; C. diemi Cabrera, Notas Mus. La Plata,
Bot. 7: 114. 1942; C. filiformis Hook. and Arn., C. longipes
Wedd.); C. lycopodioides (d’Urv.) DC., Prodr. 7: 45. 1838
(=Gnaphalium lycopodioides d’Urv.); C. pusilla DC.,
Prodr. 7: 45. 1838 (=C. lanceolata J. Rémy); C. revoluta A.
A. Schneid. and R. Trevis., Syst. Bot. 36 (3): 782. 2011; C.
sarmentosa (Pers.) S.F. Blake, Proc. Biol. Soc. Washington
38: 85. 1925 [=Tussilago sarmentosa Pers., Chevreulia
stolonifera Cass., nom. illeg., Chevreulia thouarsii J.
Rémy, nom. illeg., Gnaphalium calycinum Poir., Xeranthemum caespitosum (cespitosum) Thouars].
Chionolaena DC., Prodr. 5: 397. 1836. Type: C. arbuscula DC.
=Leucopholis Gardner, London J. Bot. 2: 10. 1843.
Type: L. phylicoides Gadner
=Parachionolaena M.O.Dillon and Sagást. Arnaldoa 1(2):
42. 1992. Type: P. columbiana (S. F. Blake) Dillon and Sagást.
=Pseudoligandra M.O. Dillon, Taxon 39(1): 127. 1990.
Type: P. chrysocoma (Wedd.) Dillon and Sagást.
Twenty-seven species, C. and S. America (C Mexico,
Costa Rica, Guatemala, N Colombia, S Brazil):
123
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S. E. Freire et al.
Chionolaena adpressifolia Loeuille, Kew Bull. 66: 263.
2011; C. aecidiocephala (Grierson) Anderb. and S.E.
Freire, Notes Roy. Bot. Gard. Edinburgh 46: 40. 1989
[=Anaphalis aecidiocephala Grierson, Gnaphalium aecidiocephalum (Grierson) L.O. Williams]; C. arbuscula DC.,
Prodr. 5: 397. 1836; C. campestris Deble, Kew Bull. 66:
264. 2011; C. canastrensis J.N. Nakaj., Kew Bull. 66: 266.
2011; C. capitata (Baker) S.E. Freire [=Achyrocline capitata Baker, Leucopholis capitata (Baker) Cufod.]; C.
chrysocoma (Wedd.) S.E. Freire, Ann. Missouri Bot. Gard.
80: 415. 1993 [=Oligandra chrysochoma Wedd., Pseudoligandra chrysochoma (Wedd.) M.O. Dillon and Sagást.];
C. columbiana S.F. Blake, J. Wash. Acad. Sci. 25: 312.
1935 [=Parachionolaena columbiana (S.F. Blake) M.O.
Dillon and Sagást.]; C. concinna (A.Gray) Anderb. and
S.E. Freire, Notes Roy. Bot. Gard. Edinburgh 46: 40. 1989
[=Gnaphalium concinnum A. Gray, Anaphalis concinna
(A.Gray) Grierson]; C. costaricensis (G.L. Nesom) G.L.
Nesom, Sida 19: 850. 2001 (=Gnaphaliothamnus costaricensis G.L. Nesom); C. cryptocephala (G.L. Nesom) G.L.
Nesom (=Gnaphaliothamnus cryptocephalus G.L. Nesom);
C. durangensis (G.L. Nesom) G.L. Nesom, Sida 19: 850
(2001); C. eleagnoides Klatt, Leopoldina 23: 88. 1887
(=Gnaphalium eleagnoides (Klatt) S.F. Blake); C. isabellae Baker, in Martius, Fl. Bras. 6(3): 130. 1882 (=C.
glaziovii Baker, C. innovans Wawra); C. jeffreyi H. Rob.,
Phytologia 55: 121. 1984; C. juniperina Loeuille, Kew
Bull. 66(2): 268. 2011; C. latifolia (Benth.)Baker, in
Martius, Fl. Bras. 6(3): 132. 1882 [=Leucopholis latifolia
Benth., Chionolaena breweri Steyerm. and Maguirre, C.
glomerata Baker, Lucilia breweri (Steyerm. and Maguire)
V.M. Badillo]; C. lavandulifolia (Kunth) Benth. and
Hook.f. ex B.D. Jacks., Index Kew. 1: 516. 1893 [=Elichrysum lavandulifolium Kunth, Chionolaena lavandulaceum (DC.) Hemsley, Elichrysum lavandulifolium (Wild.)
D. Don, Gnaphalium lavandulaceum DC., G. lavandulifolium Willd., G. lavandulifolium (Kunth) S.F. Blake]; C.
lychnophorioides Sch. Bip., Jahresber. Pollichia 20-21:
391. 1863; C. macdonaldii (G.L. Nesom) G.L. Nesom, Sida
19(4): 850. 2001 (=Gnaphaliothamnus macdonaldii G.L.
Nesom); C. mexicana S.E. Freire, Ann. Missouri Bot. Gard.
80: 427. 1993; C. phylicoides (Gardner) Baker, in Martius,
Fl. Bras. 6(3): 131. 1882 (=Leucopholis phylicoides
Gardner); C. salicifolia (Bertol.) G.L. Nesom, Sida 19(4):
850. 2001 (=Helichrysum salicifolium Bertol., Gnaphaliothamnus salicifolius (Bertol.) G.L. Nesom); C. sartorii
Klatt, Leopoldina Heft 23: 89. 1887 [=Gnaphalium sartori
(Klatt) F.J. Espinosa-Garcı́a]; C. seemannii (Sch.Bip.) S.E.
Freire, Ann. Missouri Bot. Gard. 80: 432. 1993
(=Gnaphalium seemannii Sch.Bip.); C. stolonata (S.F.
Blake) Pruski, Phytoneuron 2012-1: 4 (=Gnaphalium stolonatum S.F. Blake); C. wittigiana Baker, in Martius, Fl.
Bras. 6(3): 129. 1882.
123
Cuatrecasasiella H. Rob., Fl. Neotrop. Monogr.
2(Suppl.): 14. 1985. Type: C. isernii (Cuatrec.) H. Rob.
Two species, S. America (Andes from Ecuador to N
Argentina): Cuatrecasasiella argentina (Cabrera) H. Rob.,
Fl. Neotrop. Monogr. 2(Suppl.): 15. 1985 (=Luciliopsis
argentina Cabrera); C. isernii (Cuatrec.) H. Rob., Fl.
Neotrop. Monogr. 2(Suppl.): 15. 1985 (=Luciliopsis isernii
Cuatrec.).
Facelis Cass., Bull. Sci. Soc. Philom. Paris (1819): 94.
1819. Type: Facelis retusa (Lam.) Sch. Bip.
Three species, S. America (S Brazil, Peru, Bolivia,
Paraguay, Chile, Uruguay, Argentina): Facelis lasiocarpa
(Griseb.) Cabrera, Physis (Buenos Aires) 10: 280. 1931
(=Filago lasiocarpa Griseb., Facelis capillaris Rusby, F.
schultziana Beauverd, Lucilia erecta Benoist); F. plumosa
(Wedd.) Sch. Bip., Linnaea 34: 532. 1866 (=Lucilia plumosa Wedd., Facelis weddelliana Beauverd, nom. nov. pro
Lucilia plumosa Wedd.); F. retusa (Lam.) Sch. Bip., Linnaea 34(5): 532.1865 [=Gnaphalium retusum Lam., Facelis apiculata Cass., nom. illeg. pro Gnaphalium retusum
Lam., F. retusa (Lam.) Sch. Bip. var. andicola (Nees)
Beauverd, F. retusa (Lam.) Sch. Bip. var. candelabrum
Beauverd, F. retusa (Lam.) Sch. Bip. var. patula Beauverd,
F. retusa (Lam.) Sch. Bip. fo. congesta Beauverd, F. retusa
(Lam.) Sch. Bip. fo. gigantea Beauverd, F. retusa (Lam.)
Sch. Bip. fo. laxa Beauverd, F. retusa (Lam.) Sch. Bip. fo.
nana Beauverd, F. retusa (Lam.) Sch. Bip. fo. planifolia
Beauverd, Helichrysum retusum Spreng., Leptalea apiculata (Cass.) D. Don ex Hook. and Arn., Pteropogon chilense Fisch. and Meyer, nom. nud., P. andicola Nees].
Jalcophila M.O. Dillon and Sagást., Brittonia 38(2):
162. 1986. Type species: J. peruviana M.O. Dillon and
Sagást.
Four species, S. America (Andes of Colombia, Ecuador,
Peru, and Bolivia): Jalcophila boliviensis Anderb. and S.E.
Freire, Brittonia 42: 139. 1990 (=Gamochaeta boliviensis
(Anderb. and S.E. Freire) M.O. Dillon and Sagást.); J.
colombiana S. Dı́az and Veléz-Nauer, Revista Acad. Colomb. Ci. Exact. 19(72): 25. 1994; J. ecuadoriensis M.O.
Dillon and Sagást., Brittonia 38(2): 165. 1986; J. peruviana
M.O. Dillon and Sagást., Brittonia 38(2): 163. 1986.
Loricaria Wedd., Chlor. And. 1: 165, t. 27 A, B, C.
1856. Lectotype (designated by Cuatrecasas, 1954: 152): L.
thuyoides (Lam.) Sch. Bip.
=Tafalla D.Don, Edinb. N. Phil. Journ.: 273. 1831, non
Ruiz and Pav. 1794. Type: no stated.
Twenty two species, S. America (Andes from Colombia
to Bolivia): Loricaria anceps Sch.Bip., Bonplandia 8: 259.
1860; L. antisanensis Cuatrec., Feddes Repert. Spec. Nov.
Regni Veg. 56: 157. 1954; L. azuayensis Cuatrec., Feddes
Repert. Spec. Nov. Regni Veg. 56: 158. 1954; L. cinerea
D.J.N. Hind, Kew Bull. 59(4): 541. 2005; L. colombiana
Cuatrec., Trab. Mus. Nac. Ci. Nat., Ser. Bot. 29: 33,
Author's personal copy
Systematics of the Lucilia group
Fig. 12. 1935; L. complanata (Sch. Bip.) Wedd., Chlor.
And. 1: 167. 1856 (=Baccharis complanata Sch.Bip.); L.
ferruuginea (Ruiz and Pav.) Wedd., Chlor. And. 1: 166.
1856 (=Molina ferruginea Ruiz and Pav.); L. graveolens
(Sch.Bip.) Wedd., Clor. And. 1: 167. 1856 (=Baccharis
graveolens Sch.Bip.); L. ilinisssae (Benth.) Cuatrec., Feddes Repert. Spec. Nov. Regni Veg. 56: 162. 1954 (=Baccharis illissae Benth.); L. lagunillensis Cuatrec., Feddes
Repert. Spec. Nov. Regni Veg. 56: 162. 1954; L. leptothamna (Mattf.) Cuatrec., Feddes Repert. Spec. Nov.
Regni Veg. 56: 163. 1954 (=Tafalla leptothamna Mattf.);
L. lucida Cuatrec., Feddes Repert. Spec. Nov. Regni Veg.
56: 163. 1954; L. lycopodinea Cuatrec., Feddes Repert.
Spec. Nov. Regni Veg. 56: 164. 1954; L. macbridei Cuatrec., Feddes Repert. Spec. Nov. Regni Veg. 56: 164.
1954; L. ollgaardii M.O. Dillon and Sagást., Phytologia 59:
228. 1986; L. pauciflora Cuatrec., Feddes Repert. Spec.
Nov. Regni Veg. 56: 165. 1954; L. puracensis Cuatrec.,
Feddes Repert. Spec. Nov. Regni Veg. 56: 166. 1954; L.
reticulosa Kuntze, Revis. Gen. Pl. 1: 352. 1891; L. scolopendra Kuntze, Revis. Gen. Pl. 1: 352. 1891; L. thuyoides
(Lam.) Sch.Bip., Bonplandia 8: 260. 1860 [=Conyza thujoides Lam., Baccharis thujoides (Lam.) Pers., Loricaria
(Tafalla) microphylla Hieron., L. stenophylla Wedd., L.
stuebelii Hieron., L. thyoides (Lam.) Sch.Bip., L. thujoides
(Lam.) Kuntze, Molina incana Ruiz and Pav., Tafalla
thyoides (Lam.) D.Don; synonyms according to Hind
2011]; L. thyrsoidea (Cuatrec.) M.O. Dillon and Sagást.,
Phytologia 59: 230. 1986; L. unduaviensis Cuatrec., Feddes
Repert. Spec. Nov. Regni Veg. 56: 170. 1954. (revision
needed).
Lucilia Cass., Bull. Sci. Soc. Philom. Paris: 32. 1817.
Type: Serratula acutifolia Poir. = L. acutifolia (Poir.)
Cass.
=Oligandra Less., Syn. Gen. Comp.: 123. 1832. Type:
O. lycopodioides Less.
=Pachyrhynchus DC., Prodr. 6: 255. 1838. Type:
Pachyrhynchus xeranthemoides DC.
=Hymenopholis Gardner, London J. Bot. 7: 88.1848.
Type: Hymenopholis imbricata Gardner
Eight species, S. America (S Brazil, Paraguay, Uruguay,
N and C Argentina, Andes of Bolivia, Argentina and
Chile): Lucilia acutifolia (Poir.) Cass., Dict. Scienc. Nat.,
ed. 2. 27: 264. 1823 (=Serratula acutifolia Cass., L.
jamesonii Baker, L. lundii Baker, L. microphylla Cass.,
Pachyrhynchus xeranthemoides DC.); L. eriophora J.
Rémy, in Gay, Fl. Chil. 3: 335. 1848; L. ferruginea Baker
in Martius, Fl. Bras. 6 (3): 114. 1882; L. linearifolia Baker,
in Martius, Fl. Bras. 6 (3): 114. 1882; L. lycopodioides
(Less.) S.E. Freire, Taxon 38: 298. 1989 (=Oligandra
lycopodioides Less., Hymenopholis imbricata Gardner, L.
flagelliformis Wedd., L. glomerata Baker); L. nitens Less.,
Linnaea 5: 363. 1830; L. recurva Wedd.; Chlor. And. 1:
156. 1856; L. tomentosa Wedd., Chlor. And. 1: 157. 1856
(=L. squarrosa Baker).
Doubtful species: Lucilia saxatilis V.M. Badillo, Ernstia
50: 9, 1988. According to the original diagnosis which is
accompanied by an illustration, is likely refererable to
genus Gamochaeta by its small capitula arranged in
glomerules, forming short spikes (vs. capitula arranged in
leafy racemes in Lucilia), but no details of style branches
are found nor description neither illustration. Consequently, until the type of Badillo’s name is located or
materials can be provided, the identity of L. saxatilis is
uncertain.
Micropsis DC., Prodr. 5: 459.1836. Type: M. nana DC.
Five species, S. America (S Brazil, Paraguay, Uruguay,
NE Argentina, and C Chile): Micropsis australis Cabrera,
Notas Mus. La Plata 3, Bot. 20: 147. 1938; M. dasycarpa
(Griseb.) Beauverd, Bull. Soc. Bot. Genève, sér. 2, 5: 224.
1913 (=Filago dasycarpa Griseb.); M. nana DC., Prodr. 5:
460. 1836; M. ostenii Beauverd, Bull. Soc. Bot. Genève,
sér. 2, 5: 226. 1913 (=M. bonariensis Manganaro); M.
spathulata (Pers.) Cabrera, Notas Mus. La Plata 9, Bot. 46:
254. 1944 (=Gnaphalium involucratum Lam., nom. illeg.
hom., non Foster, G. bracteatum Willd., nom. illeg. hom.,
non Lamarck, Evax spathulata Pers., Micropsis involucrata
Cabrera).
Mniodes (A.Gray) Benth., Gen. Pl. 2(1): 301. 1873.
Antennaria Gaertn. sect. Mniodes A. Gray, Proc. Acad.
Arts. 5: 138. 1861. Lectotype (designated by Cuatrecasas,
1954: 3): M. andina (A. Gray) Cuatrec.
=Merope Wedd., Chlor. And. 1: 160. 1856, pro parte,
nom. illeg. [excl. M. erythractis Wedd. = Gamochaeta
erythractis (Wedd.) Cabrera], non Merope M.J.Roemer
1846 (Rutaceae). Lectotype (designated by Anderberg and
Freire, 1991: 189): M. piptolepis Wedd.
=Belloa pro parte, non J. Rémy, syn. nov.
=Luciliocline Anderb. and S.E. Freire, Bot. J. Linn. Soc.
106: 187. 1991. Type: L. lopezmirandae (Cabrera) Anderb.
and Freire, syn. nov.
Seventeen species, S. America (Andes from Venezuela
to NW Argentina): Mniodes andina (A. Gray) A.Gray ex
Cuatrec., Fol. Biol. Andina 1: 3. 1954 (=Antennaria andina
A. Gray); M. aretioides (Sch. Bip.) Cuatrec., Fol. Biol.
Andina 1: 3. 1954 [=Baccharis aretioides Sch. Bip., Antennaria aretioides (Sch. Bip.) A. Gray, Merope aretioides
(Sch. Bip.) Wedd.]; M. coarctata Cuatrec., Fol. Biol. Andina 1: 4. 1954; Mniodes burkartii (Cabrera) S.E. Freire,
Chemisquy, Anderb. and Urtubey, comb. nov. Basionym:
Gnaphalium burkartii Cabrera, Notas Mus. La Plata, Bot.
13, Bot. no. 56: 10, Fig. 2. 1948 [=Belloa burkartii (Cabrera) Cabrera, Lucilia burkartii (Cabrera) S.E. Freire, Luciliocline burkartii (Cabrera) Anderb. and S.E. Freire];
Mniodes catamarcensis (Cabrera) S.E. Freire, Chemisquy,
Anderb. and Urtubey, comb. nov. Basionym: Belloa
123
Author's personal copy
S. E. Freire et al.
catamarcensis Cabrera, Bol. Soc. Argent. Bot. 7: 81,
Fig. 1. 1958 [=Lucilia catamarcensis (Cabrera) S.E. Freire,
Luciliocline catamarcensis (Cabrera) Anderb. and S.E.
Freire]; Mniodes kunthiana (DC.) S.E. Freire, Chemisquy,
Anderb. and Urtubey, comb. nov. Basionym: Conyza
kunthiana DC., Prodr. 5: 379. 1836, nov. nom. [=Conyza
pusilla Kunth 1820 non C. pusilla Houtt. 1782, Belloa
kunthiana (DC.) Anderb. and S.E. Freire, Lucilia conoidea
Wedd., L. kunthiana (DC.) Zardini, Lucilia pusilla Hieron.
1900 nov. nom., L. venezualensis Steyerm., L. violacea
Wedd., Merope kunthiana (DC.) Wedd.]; Mniodes lehmannii (Hieron.) S.E. Freire, Chemisquy, Anderb. and
Urtubey, comb. nov. Basionym: Lucilia lehmannii Hieron,
Bot. Jahrb. 19(5): 51. 1894 [=Belloa lehmannii (Hieron.)
Anderb. and S.E. Freire]; Mniodes longifolia (Cuatrec. and
Aristeg.) S.E. Freire, Chemisquy, Anderb. and Urtubey,
comb. nov. Basionym: Lucilia longifolia Cuatrec. and
Aristeg., Fl. Venez. 10(1): 367. 1964 [=Belloa longifolia
(Cuatrec. and Aristeg.) M.O. Dillon and Sagást., Luciliocline longifolia (Cuatrec. and Aristeg.) M.O. Dillon and
Sagást.]; Mniodes lopezmirandae (Cabrera) S.E. Freire,
Chemisquy, Anderb. and Urtubey, comb. nov. Basionym:
Belloa lopezmirandae Cabrera, Bol. Soc. Argent. Bot. 7:
83, Fig. 2. 1958 [=Lucilia lopezmirandae (Cabrera) S.E.
Freire, Luciliocline lopezmirandae (Cabrera) Anderb. and
S.E. Freire, Belloa turneri Sagást. and M.O. Dillon, Luciliocline turneri (Sagást. and M.O. Dillon) M.O. Dillon and
Sagást.]; Mniodes pickeringii (A.Gray) S.E. Freire,
Chemisquy, Anderb. and Urtubey, comb. nov. Basionym:
Lucilia pickeringii A. Gray, Proc. Amer. Acad. Arts 5: 138.
1862 [=Belloa pickeringii (A.Gray) Sagást. and M.O.
Dillon, Luciliocline pickeringii (A.Gray) M.O. Dillon and
Sagást.]; Mniodes piptolepis (Wedd.) S.E. Freire, Chemisquy, Anderb. and Urtubey, comb. nov. Basionym: Lucilia
piptolepis Wedd., Chlor. And. 1: t. 26, f. B. 1856 [=Belloa
piptolepis (Wedd.) Cabrera, Gnaphalium piptolepis
(Wedd.) Griseb., Luciliocline piptolepis (Wedd.) M.O.
Dillon and Sagást.]; Mniodes plicatifolia (Sagást. and
M.O. Dillon) S.E. Freire, Chemisquy, Anderb. and Urtubey, comb. nov. Basionym: Belloa plicatifolia Sagást. and
M.O. Dillon, Phytlogia 58: 384, f.3F-K. 1985 [=Lucilia
plicatifolia (Sagást. and M.O. Dillon) S.E. Freire, Luciliocline plicatifolia (Sagást. and M.O. Dillon) M.O. Dillon
and Sagást.]; M. pulvinulata Cuatrec., Fol. Biol. Andina 1:
5. 1954 (=M. ferreyrae Cuatrec.); Mniodes radians
(Benth.) S.E. Freire, Chemisquy, Anderb. and Urtubey,
comb. nov. Basionym: Gnaphalium radians Benth., Pl.
Hartw.: 207, tab. 35b. 1845 [=Belloa radians (Benth.)
Sagást. and M.O. Dillon, Lucilia radians (Benth.) Cuatrec.,
Luciliocline radians (Benth.) M.O. Dillon and Sagást.];
Mniodes santanica (Cabrera) S.E. Freire, Chemisquy,
Anderb. and Urtubey, comb. nov. Basionym: Gnaphalium
santanicum Cabrera, Notas Mus. La Plata, Bot. 13, Bot. no.
123
56: 12, Fig. 3. 1948 [=Belloa santanica (Cabrera) Cabrera,
Lucilia santanica (Cabrera) S.E. Freire, Luciliocline santanica (Cabrera) Anderb. and S.E. Freire, Belloa spathulifolia Sagást. and M.O. Dillon, Luciliocline spathulifolia
(Sagást. and M.O. Dillon) M.O. Dillon and Sagást.];
Mniodes schultzii (Wedd.) S.E. Freire, Chemisquy, Anderb. and Urtubey, comb. nov, Basionym: Merope schultzii
Wedd., Chlor. And. 1: 163. 1856 [=Belloa cerrateae
(Ferreyra) M.O. Dillon and Sagást., B. schultzii (Wedd.)
Cabrera, Lucilia schultzii (Wedd.) A.Gray, Luciliocline
schultzii (Wedd.) M.O. Dillon and Sagást., Mniodes cerrateae Ferreyra]; Mniodes subspicata (Cabrera) S.E. Freire, Chemisquy, Anderb. and Urtubey, comb. nov.
Basionym: Belloa subspicata Wedd., Chlor. And. 1: 159.
1856 [=Lucilia subspicata (Wedd.) Hieron., Luciliocline
subspicata (Wedd.) Anderb.].
Note: Mniodes tunariensis (Kuntze) Hieron. ex Weberb. = Novenia acaulis (Benth. and Hook. f. ex B.D.
Jacks.) S.E. Freire and F.H. Hellw.
Concluding remarks
Our study, using plastid (rpl32-trnL, trnL-F) and nuclear
(ITS and ETS) DNA loci, together with morphological
characters, and using a broad sampling of the tribe, suggested that the South American Lucilia group sensu Anderberg and Freire (1991) is paraphyletic and that the
genera Antennaria, Chionolaena, Gamochaeta, Loricaria,
Micropsis, Mniodes, and Stuckertiella should be included
for the establishment of the monophyly in the group. This
mainly American Lucilia group s. lat. is diagnosed by
having slender pappus bristles that are basally connate or
coherent at the base by patent cilia. The phylogeny found
here corroborates previous generic circumscription (Anderberg, 1991) of most of its genera, i.e., Berroa, Chevreulia, Cuatrecasasiella, Facelis, and Micropsis. Belloa is
recovered as a monotypic genus in correspondence with
Dillon’s study (2003). Luciliocline and the remaining
species of Belloa sensu Anderberg and Freire (1991) are
placed in the genus Mniodes. Thirteen new combinations
are proposed: Mniodes burkartii (Cabrera) S.E. Freire,
Chemisquy, Anderb. and Urtubey; Mniodes catamarcensis
(Cabrera) S.E. Freire, Chemisquy, Anderb. and Urtubey;
Mniodes kunthiana (DC.) S.E. Freire, Chemisquy, Anderb.
and Urtubey; Mniodes lopezmirandae (Cabrera) S.E. Freire, Chemisquy, Anderb. and Urtubey; Mniodes lehmannii
(Hieron.) S.E. Freire, Chemisquy, Anderb. and Urtubey;
Mniodes longifolia (Cuatrec. and Aristeg.) S.E. Freire,
Chemisquy, Anderb. and Urtubey; Mniodes pickeringii
(A.Gray) S.E. Freire, Chemisquy, Anderb. and Urtubey;
Mniodes piptolepis (Wedd.) S.E. Freire, Chemisquy,
Anderb. and Urtubey; Mniodes plicatifolia (Sagást. and
Author's personal copy
Systematics of the Lucilia group
M.O. Dillon) S.E. Freire, Chemisquy, Anderb. and Urtubey; Mniodes radians (Benth.) S.E. Freire, Chemisquy,
Anderb. and Urtubey; Mniodes santanica (Cabrera) S.E.
Freire, Chemisquy, Anderb. and Urtubey; Mniodes schultzii (Wedd.) S.E. Freire, Chemisquy, Anderb. and Urtubey,
and Mniodes subspicata (Wedd.) S.E. Freire, Chemisquy,
Anderb. and Urtubey. Lucilia sensu Anderberg and Freire
(1991) is non-monophyletic; future studies employing
more variable DNA regions with extensive sampling will
be valuable before a recircumscription of Lucilia can be
proposed. The monotypic genera Stuckertiella and Gamochaetopsis are closely nested within the large genus
Gamochaeta; however, greater taxonomic sampling is
required before to make taxonomic changes for these
genera.
Acknowledgments We give special thanks to reviewers for critical
reading of the manuscript. The authors are grateful to Cecilia Ezcurra
(BCRU), Néstor Bayón (LPAG), Andreas Tribsch (SZU), and Juan C.
Ospina (SI) for providing us materials of Belloa chilensis, Gamochaetopsis alpina, Gnaphalium uliginosum, and Loricaria colombiana, respectively. We also appreciate the help of the curator of the
herbaria BCRU, BHCB, CONC, LP, LPAG, LPB, SZU, MO, SI, SPF
for permitting access to their collections. Thanks are due to Jorge A.
Hurst for some DNA extractions. Also thanks to Fernando O. Zuloaga, Mauricio Bonifacino, Marcelo Baeza, Juan C. Ospina, and
Néstor Bayón, for permission to use their photographs included in
Figs. 4 and 5. The research and fieldwork to NW Argentina and
Northern Bolivia were supported by the Consejo Nacional de Investigaciones Cientı́ficas y Técnicas (CONICET), Argentina (PIP
112-200801-02196).
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