Toward A Phylogenetic Subfamilial Classification For The Compositae

14 Pages·2002·5.7 MB·English

by  J L Panero

PROCEEDINGS OFTHE BIOLOGICAL SOCIETY OF WASHINGTON
115(4):909-922. 2002.
Toward a phylogenetic subfamilial classification for the
Compositae (Asteraceae)
Jose L. Panero and Vicki A. Funk
(JLP) Section of Integrative Biology, The University of Texas, Austin, Texas 78712
(VAF) U.S. National Herbarium, NMNH, Smithsonian Institution MRC 166,
Washington, D.C. 20013-7012
—
Abstract. Molecular studies ofthe flowering plant family Compositae (As-
DNA
teraceae) based on comparative sequence data of chloroplast genes pro-
vide new insights into the evolution and radiation of the family. The results
support the creation of new groups to maintain a classification that reflects
evolutionary history. We are proposing the following new names: subfamilies
Corymbioideae, Gochnatioideae, Gymnarrhenoideae, Hecastocleoideae, and
Pertyoideae; tribes Athroismeae, Corymbieae, Dicomeae, Gochnatieae, Gym-
narrheneae, Hecastocleideae, Polymnieae; subtribe Rojasianthinae. The totals
now stand at 11 subfamilies and 35 tribes. Only one tribe, the Mutisieae, is
non-monophyletic having two branches. Most of the new groups are derived
from taxa included in tribe Mutisieae, long suspected to be a paraphyletic
group. Molecular studies that support these changes are discussed elsewhere
but a summary of their results is presented.
Molecular phylogenetic studies of the of the Compositae using sequence data of
family Compositae (Asteraceae) have been the chloroplast gene ndhF and provide ad-
instrumental in providing important insight ditional evidence for the paraphyly of sub-
into the evolution and radiation of the fam- family Cichorioideae. Their data provided
ily. Assessments of phylogenetic relation- some support for the recognition of three
ships in the family using molecular data be- main groups within subfamily Cichorioi-
gan with restriction fragment length poly- deae s.l. splitting sequentially from above
morphisms of the chloroplast genome. the Barnadesioideae: 1) Mutisieae, followed
These studies identified a 22 kb inversion by 2) Cardueae, and finally, 3) the tribes
present in all members of the Compositae Cichorieae, Liabeae, Vernonieae, and Arc-
except the Mutisieae subtribe Barnadesieae toteae forming a monophyletic group sister
(Jansen & Palmer 1987), which had a chlo- to Asteroideae. The latter group plus Aster-
roplast organization similar to the rest of oideae was recognized by Bremer (1994,
land plants. This result was used to elevate 1996) as the vernonioid group. Since the
the Barnadesieae to subfamily status (Bre- publication of the molecular phylogeny of
mer & Jansen 1992), and the traditional two the Compositae by Kim & Jansen (1995)
&
subfamily system consisting of Cichorioi- only the study by Bayer Starr (1998) has
deae and Asteroideae was expanded to in- provided a competing hypothesis of tribal
clude the Barnadesioideae. Kim & Jansen relationship based on noncoding regions of
(1995) published what can arguably be the chloroplast genome, but this study did
viewed as one ofthe most importantpapers not provide good support for any new pat-
DNA
using sequence data aimed at eluci- terns ofrelationship. Most studies using the
dating the phylogeny ofthe Compositae. In ndhF data matrix to date have concentrated
this paper they identified the major clades on elucidating the placement of a particular
910 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
taxon in the tree of life of daisies (Karis et argue that eventually they might be part of
al. 2001). the Asteroideae and Cichorioideae respec-
The goal of our study was to use several tively, but given the amount of data that
molecular markers to produce a phylogeny support this cladogram and the fact that the
that would clarify the phylogenetic relation- isolated position of these genera has long
ships of members ofthe tribe Mutisieae s.l., been recognized, it is doubtful. Details of
and the circumscription of the subfamily the analyses and a discussion of the result-
Cichorioideae in general. Our data matrix ing clades will be published elsewhere
&
includes the genes and markers ndhF, trnh- (Funk Panero, in prep.; Panero et al., in
trnF, matK, ndhD, rbcl^, rpoB, rpoCl prep.); we publish these names here so that
exonl, 23S-trnl, and ndhl for an approxi- they are available for use in those papers.
mate total data matrix of 13,380 bp. Com- The changes to the classification of the
bining these chloroplast markers has pro- family proposed herein have been carefully
duced a solid phylogeny ofthe Compositae. reviewed by the authors with the under-
Included here is a strict consensus tree of standing that these changes represent the
the relationships of Compositae based on largest overhaul to the classification of the
our studies for the Cichorioideae (Panero & Compositae since Bentham (1873). Our
Funk, in prep.) and those of Panero et al. confidence in proposing these changes is
(in prep.) for tribe Heliantheae andrelatives based on two things, first, an analysis of
(Fig. 1). This phylogeny includes amajority one of the largest data matrices for any
ofgenera ofthe classical Mutisieae and rep- grou—p of flowering plants produced to
resentatives of most other tribes of Com- date a combination of multiple g—enetic
positae as well as genera deemed, based on markers and a broad sampling oftaxa and
their morphology, to be of difficult place- second, an analysis of these data by con-
ment (see Bremer 1994). The resulting phy- servative methods (i.e., maximum parsi-
logeny has clarified substantially the rela- mony) without the coding of indels or char-
tionships of the Compositae and resulted in acter weighting of any type. Bootstrap sup-
the need to publish new names to maintain port for nearly all of the clades being rec-
a formal taxonomic nomenclature for ognized as new taxa is 100%. Our
monophyletic clades. All groups are now experience with this large data matrix
monophyletic and reflect the evolutionary shows that additions of new data partitions
history ofthe family except for two branch- only solidifies the phylogenetic signal and
es near the base of the tree that constitute branch support. It is clear that past a certain
a paraphyletic Mutisioideae. It is most like- threshold, unique to each dataset and deter-
ly that additional data will provide enough mined by the number ofcharacters and taxa
support to recognize the "Stifftia group" as sampled, the phylogenetic signal stabilizes.
a new subfamily and tribe, however the It is our view that the addition of new data
data are missing several of the genera that partitions in the future will only solidify the
should fall into the "Stifftia group" clade branch support reported here.
and final resolution of the problem will
have to wait until those genera have been Subfamilies
collected and analyzed. Two of the mono- &
Corymbioideae Panero V. A. Funk, sub-
phyletic subfamilies proposed, Corymbioi- fam. nov., Corymbieae Panero & V. A.
deae and Gymnarrhenoideae, contain gen-
Funk, trib. nov.
era whose placement has long been prob-
Type: Corymbium L., Coroll. Gen. 14
lematic. Their isolated placement on the
(1737).
cladogram combined with their unusual
Monotypic (7 species).
morphology supports their being named at
the subfamily (and tribal) level. One might Plantae in foliis sessilibus et in laminis
VOLUME 115, NUMBER 4 911
Tribes Subfamilies
Heliantheae
|
Madieae
100 58
Perityleae
68
51 I
Eupatorieae
72
Millerieae
95
Polymnieae
981 Bahieae
Chaenactideae
98 Tageteae
100 Neurolaeneae
Asteroideae
Coreopsideae
100
Helenieae
Athroismeae
100
Plucheeae
^100
1
Inuleae
54
Anthemideae
Astereae
60
Gnaphalieae
Calenduleae
100
Senecioneae
Corymbieae Corymbioideae
79 Arctoteae
Vernonieae
90
Liabeae Cichorioideae
100
Cichorieae
100 Gundelieae
Gymnarrheneae Gymnarrhenoideae
100 Pertyeae Pertyoideae
E
Cardueae
100 100 Tarchonantheae Carduoideae
Dicomeae
53
Hecastocleideae Hecastocieioideae
Gochnatieae Gochnatioideae
100 Mutisieae (SA) Mutisioideae
iqoj Mutisieae (SA,A) "TheStifftia Group"
t
Bamadesieae Bamadesioideae
^^^^^—^^^^—^^-^^^^^^
Outgroups(Calyceraceae, Goodeniaceae)
Fig. 1. Strict consensus tree of 12 most parsimonious trees for 122 representative Compositae taxa based
on chloroplast DNA sequence data. Bootstrap values indicated above nodes, SA = South America, A = Asia.
Tree is simplified to show only tribe and subfamily placement and arrangement.
912 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
conduplicatis. Capitula uniflora; bracteis in- obtuse or acute, with short sweeping hairs
volucri biseriatis, dimorphis; bracteis inter- on abaxial side, sweeping hairs restricted to
ioribus 2, involutis; limbis corollarums sal- style and scarcely present below bifurcation
verformibus. point on the style shaft. Achenes linear to
Scapose, perennial herbs, tufted and elliptic, hirsute or villous, silvery white,
forming rosettes. Leaves alternate, sessile, pappus ofshort, crown-like scales variously
sometimes conduplicate, blades lanceolate fused or divided into lobes and bristles.
to linear, leaf bases attenuate, leaf apices Chromosome number: 2N = 16 (Weitz
acuminate, terete, involute or flat in cross 1989).
section, margins entire, venation parallel, The phylogenetic position of the South
leaf surfaces glabrous to villose or hirsute, African genus Corymbium has been histor-
sometimes with glandular trichomes. Inflo- ically controversial (Bentham 1873) and in
rescence ofopen to congested corymbiform the latest revision of the family at the ge-
cymes at the end of scapes that are as tall neric level, the genus is placed in subfamily
or taller than the rosette leaves. Heads with Cichorioideae unassignedto atribe (Bremer
one floret, involucre narrowly cylindrical, 1994). Corymbium is unusual in the Com-
conspicuously gradated, phyllaries in two positae because of its single-flowered
series, chartaceous-coriaceous to herba- heads, heads with two innermost involucral
ceous, green with purple tips or suffused bracts enclosing the flower, the broad, pat-
with purple when young, outer series of2—3 ent lobes of the corolla, and the narrowly
phyllaries, apex acute to acuminate or lanceolate leaves with parallel venation.
rounded, glabrous or pubescent inner series Our studies reveal that the genus occupies
of 2 phyllaries, these approximately 2 to 5 a position next to the base of the subfamily
times longer than those ofouter series, oval Asteroideae. These results together with the
to oblong in outline, involute, enclosing flo- distinctive morphology of Corymbium war-
ret, bifid or trifid, glabrous or pubescent; rant its inclusion in a new subfamily Cor-
receptacle flat. Florets actinomorphic and ymbioideae.
bisexual, salverform, corolla mauve, pink,
or white, lobes longer than tube with a tuft Gymnarrhenoideae Panero & V. A. Funk,
of papillae on the distal end, apiculate at subfam. nov., Gymnarrheneae Panero &
apex with a raised, triangular arch of scler- V. A. Funk, trib. nov.
ified cells immediately below the lobe apex Type: Gymnarrhena Desf., Memoires du
rendering the tip of the apex apiculate; an- museum d'histoire naturelle, Paris. 4:1. t.
thers 5, thecae black, ecaudate, shallowly 1. 1818.
calcarate, anther connective of long, fusi- Monotypic (1 species).
form, conspicuously sclerified cells, endo-
thecium dimorphic, proximal or inner rows Herbae perennes rosettiformes. Synflo-
composed of quadratic cells with bipolar rescentiae simplices vel complexae; capi-
thickenings and single bridges, these cells tulis subterraneis et aeriae; achaeniis di-
separated from distal or outer endothecial morphis.
cells by a single cell row of tightly scleri- Perennial amphicarpic herbs. Leaves
fied isodiametric cells, distal endothecial simple, forming dense rosettes, sessile,
cell rows composed of cells approximately smooth, narrowly lanceolate to nanowly
twice as large as those of the inner endo- ovate, apex narrowly acute to attenuate,
thecium with bipolar thickenings and single margins denticulate, base truncate, surfaces
bridges, anther appendage lacking and re- smooth and glabrous. Inflorescences subter-
duced to a series of elongated cells arising ranean or congested in the center of the
fromthe antherconnective; stylesdissected, leafy rosette. Subterranean heads homoga-
color as in corollas, style branches linear. mous and female, corolla vestisial enclosed
VOLUME 115, NUMBER 4 913
in involucral bracts. Achenes of subterra- nean fruits develop first and the aerial fruits
nean heads laterally flattened, blackish, are produced later and only in wet years.
sparsely hairy; pappus absent or of short The aerial fruits are wind dispersedwhereas
bristles that are flattened at the base ap- the subterranean fruits germinate under-
proaching scale-like, but bristle-like at the ground and appear to be more drought tol-
apex with rounded apices. Aerial heads erant. It is possible that amphicarpy in
bearing florets of two types: male florets in Gymnarrhena and other plants is an adap-
small groups that are loosely connected on tive mechanism developed in response to
very short peduncles and interspersed inconsistent and/or low water-availability
among single female florets each of which (Roller & Roth 1964).
is strongly enclosed in a stiff white and Gymnarrhena is an unusual member of
green bract, with a few rows ofchartaceous the Compositae and its history reflects its
phyllaries. Florets with whitish corollas, unique morphology. Bentham (1873), Hoff-
male florets greatly reduced in size with mann (1894), and Cronquist (1955) placed
3^
lobes and anthers, anther apex abbre- this genus in the Inuleae s.l. and Bentham's
viated, filament not elongated into an apical alternate choice was the Astereae. Skvarla
appendage, thecae with base short rounded, et al. (1977) pointed out that the pollen did
ecalcarate, ecaudate; female florets filiform, not support either of the above placements
style branches long with rounded apices. as the genus has Anthemoid pollen andthey
Achenes obconical, ciliate, with elongate suggested a possible placement in the An-
twin hairs, cell walls appear to be thin; pap- themideae. Bremer (1994) listed the genus
pus of long, acuminate, laciniate bristles as belonging to the Cichorioideae s.l. but as
with acute apices; ovaries of male florets "unassigned to tribe" along with several
with a vestigial pappus or lacking. Chro- other problem genera. In our cladograms
mosome number: 2N = 20. Gymnarrhena is consistently located by it-
A monotypic genus extending from self below the Cichorioideae s.s. and above
North Africa to the Middle East. the Pertyoideae ("Asian Mutisieae") clade.
Amphicarpy (the ability to produce aerial
as well as subterranean fruits) is uncommon Gochnatioideae (Benth. & Hook, f.) Panero
in flowering plants being found in only ca. & V. A. Funk, subfam. stat. nov., Goch-
50 species worldwide (Lev-Yadum 2000). natieae (Benth. & Hook, f.) Panero & V.
Data are available that show that ahigh pre- A. Funk, trib. stat. nov. Basionym:
ponderance (eight) of those taxa are found Gochnatiinae Benth. & Hook, f.. Gen. PI.
in Israel. 168, 216. 7-9 Apr 1873.
This taxon has repeatedly been described Type Gochnatia Kunth in HBK, Nov. Gen.
as having male central florets and periph- et Sp. 4:19. t. 309. 1820.
eral female florets, but the male florets are Includes: Cnicothamnus Griseb.(2 species),
not always grouped in the center of the Cyclolepis Gill ex D. Don (1 species),
head. In fact some groups of male florets Gochnatia Kunth in HBK (ca. 60 spe-
are found at the outer edge of the recepta- cies), Richterago Kuntze (including Ac-
cle. It seems more likely that the aerial tinoseris (Endl.) Cabrera, 17 species),
heads are actually groups ofheads, some of and possibly Chucoa Cabrera (1 species).
which are few-flowered male heads and
A
others are single-flowered female heads. Mutisieis in stylis glabris apice rotun-
Thus the monoecious plants bear heads of datis, in appendices antherarum apiculatis et
both sexes grouped in a common synflo- in bracteis involucri multiseriatis differt.
rescence. The fruits of the two types of Many perennial herbs but also shrubs and
heads of Gymnarrhena have different de- trees or rcirely dioecious subshrubs or gy-
velopmental patterns: the larger subterra- nodioecious shrubs or monoecious rosulate
914 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
herbs; branches rarely spiny. Leaves sim- fined to the Americas. The clade has con-
ple, alternate, coriaceous or smooth, lance- sistently appeared in all versions of the
olate, oblanceolate, elliptic, ovate, obovate, analysis. The genera in this subfamily are
spathulate to narrowly linear; apex acute, characterized by glabrous styles and anthers
obtuse, mucronulate to acuminate, and spi- with apiculate appendages. The genus Chu-
nose; margins entire, spinose-dentate, den- coa referred by Cabrera (1955, 1977) to the
tate to denticulate; base attenuate, truncate, Mutisieae subtribe Gochnatiinae may be-
or rounded; surfaces tomentose, glandular long in this group, however, we were un-
punctuate, glabrescent or glabrous; subses- able to obtain recently collected materialfor
sile to petiolate, petiole base expanded lat- analysis and the genus differs from other
erally, sometimes pubescent; veins pinnate genera ofthe Gochnatioideae by having pu-
or parallel. Inflorescence solitary and ter- bescent style branches. Final placement of
minal or few in number to numerous in ra- this genus will have to await further study.
cemes or cymes. Heads pedunculate orrare-
ly sessile; peduncle bracteate; cylindrical or Hecastocleioideae Panero & Funk, subfam.
campanulate; receptacle epaleate, rarely pa- nov, Hecastocleideae Panero & V. A.
leate, flat to shallowly convex; discoid and Funk, trib. nov.
homogamous or radiate and heterogamous; Type: Hecastocleis A. Gray, Proc. Amer.
phyllaries in 4—15 series, imbricate, outer Acad. Arts 17:220. 1882.
ones ovate-lanceolate to lanceolate, inner Monotypic (1 species)
ones subequal to longer than the outer ones,
linear-lanceolate to lanceolate, acute, acu- Ad Mutisieas similes sed in synflorescen-
minate, lanate, sericeous or glabrescent. tiis biordinatis in capitulis solitariis in brac-
Florets few-many (5—300); corolla tubes teis spiniferis et in corollas profunde lobatis
glabrous, pubescent, and/or glandular. Mar- differt.
ginal bilabiate florets (when present) pistil- Stoloniferous shrubs with deep roots,
late, (3+1, 3+2, 4+1), 10-60, white to growing on vertical cliffs in the cracks of
pinkish with or without rose-colored veins; rocks or in very well-drained, sandy soil,
staminodia 4-5, free, hyaline (in gynodioe- young stems bright green turning white-
cious plants flowers of male plants are her- brown with age, glabrous, old stems ash
maphroditic and female plants have flowers gray to brown, trichomes simple, white, re-
without anthers). Disc florets hermaphro- stricted to leaf internodes of rapidly grow-
ditic or functionally male, actinomorphic ing shoots. Leaves alternate, sessile, blades
with 5 deeply divided lobes, yellow, white, narrowly ovate to broadly acicular, leafba-
rose, or orange-yellow; anther-appendages ses attenuate, leaf apices ending in a ligni-
acuminate to apiculate, anther-tails glabrous fied mucro or spine; margins entire with
or pubescent; style slender, shortly bilobed, 2-3 spines on each side of the leaf, spines
glabrous, apex rounded or obtuse. Achenes mostly confined to basal half; central vein
cylindrical, inconspicuously ribbed, villose, lignified with age and turning into a soft
sericeous, sometimes glandular; pappus un- spine as leaf blade falls off at senescence;
iseriate or biseriate, bristles 25-50, simple venation triplinerved with the two second-
(rarely branched), basally free or connate ary veins parallel to the main vein, unarmed
into a fleshy ring; setae serrulate, straw-col- leaves produced from short lateral branches
ored. Chromosome numbers: Cyclolepis 2N ifgrowing conditions are favorable, leafab-
= 54, Cnicothamnus 2N = 44, and Goch- axial and adaxial surfaces concolorous and
natia 2N = 46. essentially glabrous. Inflorescence of mul-
This clade is located above the Mutisieae tiple single-flowered capitula aggregated
s.s. clade and below Hecastocleis and the into compound heads, each aggregation of
Carduoideae clade. Its members are con- 1-5 heads associated with a scarious to co-
VOLUME 115, NUMBER 4 915
riaceous oval to ovate bract with 3-9 spines connective unevenly thickened and there-
on each side, the terminal inflorescence fore producing a "radial" thickening pat-
with 4-10 capitula surrounded by 4-5 tern under light microscopy conditions, this
bracts. Heads with 1 floret, involucre of20- pattern gradually changing to polar thick-
30 phyllaries in 4-5 series, phyllaries nar- ened cells with those cells ending the en-
rowly ovate, prominently apiculate, herba- dothecium having minimal thickened areas,
ceous to scarious, green, densely strigose to pollen tricolpate, smooth. Style glabrous
lanose on mid area to basal attachment; re- with no sweeping hairs, dissected into two,
ceptacle flat. Zygomorphic or liguliform rounded style branches, each style branch
florets absent, actinomorphic florets perfect, ending with a laminar cell proliferation.
corollas purple-white changing to white Achenes oval, black, essentially glabrous,
with age, deeply lobed, lobes narrowly tri- pappus of a crown of scales, minutely lac-
angular and as long as tube, patent at an- erate. Chromosome number: 2N = 16
thesis, tube obtrullate in outline, druses (Powell et al. 1974).
present, veins 5, parallel to each other along Hecastocleis was described by Asa Gray
the tube and splitting below the sinus ofthe (1882) and in the protologue of the species
lobe, the fiber bundle splitting unequally he remarked on the distinctiveness of the
just above the sinus level, producing two genus and of its affinities to the Asian ge-
strong veins and a thin vein that dissipates nus Ainsliaea. This commentary is proba-
in the space between the two main veins bly based on the similarity in corolla mor-
and the corolla lobe edge, the two main phology between the Pertyoideae and He-
veins diverge from each other and reach the castocleis in which corollas are deeply dis-
apex of the lobe where they dissipate into sected and the lobes are spreading. Our
the surrounding tissue, the adaxial corolla molecular studies reveal that Hecastocleis
lobe strongly sclerified, sclerified cell pro- represents an isolated lineage, possibly the
liferation coincides with splitting of pri- survivor of an old radiation of the family
mary veins, the sclerified cells appear in the into the North American continent.
middle lowermiddle portion ofthe lobe and
radiate to the edges to cover approximately Pertyoideae Panero & V. A. Funk, subfam.
fj of the lobe surface, additional layers of nov., Pertyeae Panero & V. A. Funk, trib.
sclerified cells repeat the same overall dis- nov.
tribution pattern as the lower layers but ap- Type: Pertya Schultz-Bip., Bonplandia, 10:
proximately halfway the length of the lobe. 109. t. 10. 1862
Anthers 5, calcarate and caudate, purplish Includes: Ainsliaea DC. (50 species), Dias-
to pale pink, anther collar with isodiamet- pananthus Miq. (1 species, sometimes
ric, thickly and evenly sclerified cells, these placed in synonomy with Ainsliaea),
changing abruptly to narrowly fusiform Macroclinidium Maxim. (3 species), My-
cells with strongly sclerified walls, the an- ripnois Bunge (1 species), and Pertya
ther collar uneven in composition with nu- Schultz-Bip. (15 species).
merous sclerified cells abaxially and a band
of one to few cells on its adaxial side, an- Ad Mutisieas similes sed in capitulis mi-
ther tails approximately % the total length noribus solitariis vel paucis in corollis non
of the anther thecae with endothecium tis- bilabiatis; lobis 5 profunde dissectis varia-
sue extending approximately '/j to '/, the biliter connatis distinctae.
length of the tail, the distalmost end of the Many perennial herbs but also some
tail twisted in some anthers, the strongly shrubs or vines and one (Myripnois) gyno-
sclerified tissue of the connective gradually dioecious shrub; glabrous to densely pubes-
expands ending in a strongly sclerified an- cent. Leaves simple, scattered and alternate,
ther appendage, those cells proximal to the or congested and rosulate at midpoint or
916 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
basal, subsessile to petiolate, lanceolate, ob- duoideae). This is the only group ofMutis-
lanceolate, elliptic, ovate, obovate, spathu- ieae s.l. taxa that is located above the Car-
late to narrowly-linear or cordate; apex duoideae on the tree and its placement
acute, rounded, acuminate, or mucronulate; shows the diversity and variability of the
margins entire, pubescent, dentate to den- taxa previously contained in the Mutisieae
ticulate; base attenuate or rounded; surfaces s.l.
from densely tomentose, to glabrous; peti- The most interesting feature ofthis group
ole sometimes narrowly winged; blades is the deeply but unequally divided actino-
mostly with 3 or 5 veins but a few pinnate. morphic corolla. Some corollas appeartobe
Inflorescence solitary or heads few in num- actinomorphic, some bilabiate and some are
ber in spike-like or racemiform to thyrsi- intermediate between the two. All corollas
form cymes. Heads discoid or disciform of this group have five equal sized lobes
and homogamous, pedunculate or sessile; with 10 veins. The variation occurs in the
peduncle bracteate sometimes minutely so; fusion of these lobes and it happens at all
involucre cylindrical or campanulate, phyl- levels. Even in the same head where some
laries in 3-8 series, imbricate, outer ones corollas have a 3+2 division and others
ovate-lanceolate to lanceolate, inner ones have a regular corolla while still others
linear-lanceolate to lanceolate, apex acute have 3+1+1 or even 3+1. In some species
or acuminate, minutely pubescent or more ofAinsliaea the corollas have nearly evenly
rarely glabrous. Florets one to few, perfect, divided lobes with all of the lobes skewed
corollas actinomorphic with 5 equal sized, to one side or secund which gives a star-
deeply divided lobes fused unequally tling appearance to the heads.
(sometimes in the same head) with some
fulfilling the criteriaforbilabiate butalways Tribes
w3i+th1+101),vesionsme(tmiomsetscsoemcmunodn; pwahtitteer,nsw3h+it2e, TDyipceo:meDaiecoPmaaneCraoss&., VB.ulAl.. SFoucn.k,Phtirliob.m.no1v2..
suffused with pink, purple, or red, anthers
1817.
calcarate, caudate, antherappendages small,
Includes: Dicoma Cass. (ca. 40 species),
acuminate to acute, anther-tails usually pi-
Erythrocephalum Benth. (13 species),
lose and sometimes very long; style slender,
Gladiopappus Humbert (1 species), Ma-
shortly bilobed, dorsally with short hairs or cledium (Cass.) DC, Cloiselia S. Moore.
papillae, apex slightly rounded to acute.
(2 species), Pasaccardoa Kuntze (4 spe-
Achenes cylindrical, ribbed, glabrous to
cies), Pleiotaxis Steetz (26 species).
densely villose; pappus of scabrid bristles
or in Pertya, plumose bristles. Chromosome Ad Mutisieas similes sed in ramis stylo-
numbers: Ainsliaea 2N = 24, 26, 30; Pertya rum base caespitose pilosis et in cellulis su-
2N = 24, 26, 28. perficialibus corollarum typis senecioidis
All the members of this clade are found differt.
in Asia, from Afghanistan through India to Perennial herbs, shrubs or small trees,
China, Taiwan, Japan, and SE Asia. The young stems glabrous or pubescent, tri-
only two wholly Asian genera of the Mu- chomes multicellular. Leaves alternate, pe-
tisieae not in this clade are Leucomeris dunculate or sessile, blades linear to broad-
D.Don and Nouelia Franch., which form a ly ovate, glabrescent to densely pubescent
clade only known from southwestern China on abaxial surface, margins entire to ser-
and adjacent regions. This China clade is rate, leaf bases various, leaf apices some-
found near the base of the tree in the Mu- times terminating in a spine or mucro. In-
tisieae s.s. (Fig. 1). The Pertya clade is well florescence terminal, solitary, or open thyr-
supported and is located above the Car- siform cymes. Heads homogamous or het-
dueae plus "African Mutisieae" clade (Car- erogamous, involucre campanulate to
VOLUME 115, NUMBER 4 917
hemispherical or obconic with innermost rugose, corolla epidermis pattern as op-
row of phyllaries producing a strong con- posed to the crested outer walls typical of
striction at the end of the involucre, phyl- Mutisieae. However, the occurrence of a
laries in multiple series, herbaceous to scar- particular corolla cell morphology is not an
ious sometimes innermost phyllaries her- unequivocal indicator of—phyletic relation-
baceous with scarious margins, sometimes ship within the family see for instance
with a prominent midrib, patent or spread- genera such as Ainsliaea and Pertya, in-
ing; receptacle epaleate, rarely paleate. Flo- cluded by Hansen in Mutisieae but here re-
rets actinomorphic or sometimes peripheral ferred to the Pertyoideae.
florets zygomorphic and usually termed bi- The genus Oldenburgia Less, is not in-
labiate with 3 ofthe lobes greatly expanded cluded in tribe Dicomeae as it appears from
and appearing liguliform, corollas, white, present data to be sister to the Tarchonan-
yellow, cream or various shades of pink, thus—Brachylaena clade (Tarchonantheae)
mauve or lilac, tube narrow variously gla- and collectively the three genera are sister
brous to pubescent, lobes conspicuous and to the Cardueae. Ortiz (2000) considered
longer than tube, either erect or spreading; Oldenburgia a basal lineage ofthe tribe and
anthers 5, caudate and calcarate, tails with used this taxon along with Gochnatia as
or without antrorse ramifications, append- outgroups in his phylogenetic analyses of
age apiculate to acute or slightly acuminate, Dicoma and related genera. Bond (1987)
pollen smooth or echinate; styles with two considered Oldenburgia not to be closely
or four veins, style branches straight or related to any other members of tribe Di-
curved, with sweeping hairs restricted tobi- comeae and believed its sister taxon to be
furcation point and above, lowermost tri- found among American members of tribe
chomes slightly to conspicuously longer
Mutisieae subtribe Gochnatiinae. Addition-
than those at the distal end of style branch-
al data are needed to ascertain the phylo-
es. Achenes ellipsoid to obovoid or obcon-
genetic position of Oldenburgia.
ic, glabrescent to densely pubescent, pubes- The Dicomeae is recognized because it
cence on ribs or in the space between them,
members are morphologically distinct from
carpopodium absent or rarely present,
their sister clade the Oldenburgia—Taxchon-
achene wall smooth to ribbed, pappus pres-
antheae—Cardueae and there are no morpho-
ent or absent, isomorphic or dimorphic,
logical characters that unify these taxa.
sometimes in several rows, persistent or ca-
ducous. Chromosome numbers: Dicoma 2N Also, the sister relationship ofthe Tarchon-
= 22; Pleiotaxis 2N = 20. antheae and Oldenburgia with the Cardueae
This tribe contains most genera centered is weak and additional data may show that
around Dicoma and found in Africa. These the Tarchonantheae and Oldenburgia are
genera were previously classified in Mutis- sister to the Dicomeae and not the Car-
dueae.
ieae subtribe Gochnatiinae. The major ex-
ception is the genus Gerbera L. and allies
that remain in Mutisioideae. Our molecular Athroismeae Panero, trib. nov.
studies support the exclusion of this Dico- Type: Athroisma, DC, Guill. Arch. Bot. 2:
ma clade from the Mutisieae as proposed 516. 1833.
by Hansen (1991) and their inclusion in Includes: Athroisma DC. (12 species), Ble-
subfamily Carduoideae. Hansen (1991) pharispermum Wight ex DC. (15 spe-
stressed corolla cell morphology and col- cies), Leucoblepharis Arnott (1 species).
lective patterns derived from these cells as
his strongest evidence to support the exclu- Capitula discoidea vel disciformia palea-
sion of the African Mutisieae from South ta, floribus peripheralibus 0—2 femineis in
American Mutisieae. These genera show a coroUis tubiformibus; thecis antherarum
918 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
base brenter caudatis, parietibus achaenio- chomes with apical diverging cells straight
rum phytomelaniniferous. or recurved, ovaries of functionally stami-
Perennial herbs, shrubs or small trees, nate flowers in Blepharispermumobconical,
young branches glabrous to pubescent, old brown, pappus of fertile flower achenes ei-
stems gray to brown. Leaves alternate or ther a crown of twin trichomes sometimes
fasciculate in brachyclasts, petiolate or ses- with recurved apices or of deeply lacerated
sile, petioles sometimes with a basal spine; fused squamellae. Chromosome numbers:
blades linear, lanceolate to ovate, obovate, Athroisma 2N = 20 (Eriksson 1993); Ble-
bases attenuate, apices acuminate to retuse, pharispermum 2N = 20 (Eriksson 1992).
cuneate or truncate, margins entire, dentate The Athroismeae contains the genera
or serrate, venation triplinerved or with a Athroisma DC, Blepharispermum Wight ex
single vein, abaxial surface with sessile DC, and Leucoblepharis Arnott centeredin
glandular trichomes. Inflorescence a con- eastern tropical Africa. These genera were
gested glomerule-like cyme solitary or ar- considered to be members of the Inuleae
ranged in open, thyrsiform cymes. Heads until they were placed in the Heliantheae
disciform, heterogamous, involucre narrow- (Eriksson 1991). Eriksson allied the genera
ly campanulate, narrowly conical, phylla- of his Blepharispermum group to members
ries 0-2, involute, narrowly elliptical, ovate of subtribe Ecliptinae, more specifically to
to oval, apiculate, shallowly to strongly the genera Salmea DC. and Acmella Rich,
keeled, apical end entire, trilobed or vari- ex Pers. (Eriksson 1992). This choice of a
ously lobed, or ciliate, hyaline, scarious, ab- sister group in America is a logical one giv-
axial surface glabrous, pubescent and/or en that these genera share a series of su-
glandular; receptacle paleate; pales normal- perficially similar characteristics with the
ly narrower and longer than phyllaries or in Blepharispermum group such as a combi-
the case ofAthroisma wider than the phyl- nation of carbonized achenes, T-shaped
laries, commonly with a round apex, rarely twin hairs on the achenes, the suborbicular
apiculate. Florets all actinomorphic, female to broadly elliptical shape of the achenes,
florets present or absent, 2 to several, co- and the white corollas. The genera Salmea
rollas tubular, hermaphrodite florets 2—25, and allies such as Acmella and Spilanthes
in Blepharispermum functionally staminate Jacq. differ from the Blepharispermum
and only 2-^ present, corolla campanulate, group in having laterally compressed
white, greenish-white, purple, tube white or achenes, heads with numerous hermaphro-
greenish, glabrous orpubescent mostly with ditic disc flowers with peripheral ray flow-
twin hair glands, lobes (4—) 5; anthers 5, ers instead of pistillate, tubular flowers pe-
ecalcarate, caudate, thecae white, to pale ripheral to the heads in the Blepharisper-
purple, endothecium with polarized thick- mum group, anthers with round and not sag-
enings, appendage a continuation of the ittate appendages, and anthers without tails.
connective and shallowly constricted above It is indeed this last characteristic that ex-
thecae level sometimes with apical gland; cludes the Blepharispermum group from
styles divided or filiform, filiform styles as- tribe Heliantheae, as there are no taxa in
sociated with functionally staminate flow- Heliantheae with such anther tails.
ers, stigmatic area in divided styles is di- Results from molecular studies of He-
vided into two rows which are confluent at liantheae sensu lato and related genera (Pa-
style branch apex, sweeping hairs present at nero et al. in prep) show that the Blephar-
style apex or slightly below rarely present ispermum group (represented by Blephar-
below the style branch bifurcation. Achenes ispermum and Athroisma in our studies) is
black, radially flattened, ovate to oval, el- basal to the Heliantheae sensu lato. This re-
liptic to suborbicular in outline, lateral ridg- sult supports the recognition of this group
es ciliate, trichomes fused at base, twin tri- as a new tribe in the Compositae. Molecular