Syst. Biol. 46(3):407-425, 1997
PATTERNS OF FLORAL EVOLUTION OF FOUR ASTERACEAE
GENERA (SENECIONEAE, BLENNOSPERMATINAE) AND THE
ORIGIN OF WHITE FLOWERS IN NEW ZEALAND
ULF SWENSON AND KARE BREMER
Department of Systematic Botany, Uppsala University, Villavagen 6, S-752 36 Uppsala, Sweden;
E-mail: [email protected] (US.), [email protected] (K.B.)
Abstract.—Two parsimony analyses based on morphological data of the subtribe Blennospermatinae (Asteraceae, Senecioneae) were performed to generate a hypothesis for the phylogenetic
relationships within the subtribe, which comprises four genera and 27 species of both radiate and
disciform genera distributed around the Pacific Rim. Heterogeneity of the group is concomitant
with coding problems such as absence of organs leading to inapplicable states, also termed missing entries. Morphological data were therefore coded by two differing methods: (1) using the
separate state "absent" or (2) using the state "inapplicable." Substantial support for Blennospermatinae monophyly was obtained. A well-supported sister-group relationship, based on floral
characters, was established between the two genera Blennosperma and Ischnea. Their ancestor
evolved a specialized type of tubeless ray florets and male disc florets. These two genera are
confined to the New World and to New Guinea, respectively. Their sister taxon is the monotypic
North American genus Crocidium, and its status as a separate genus was supported. Abrotanella is
a genus of 19 species confined to alpine habitats in the Southern Hemisphere. Monophyly and the
isolated position of Abrotanella was strengthened. One clade of the genus has evolved functionally
male central florets with a progressing trend toward cypsela reduction. Different floral colors have
evolved in Abrotanella, and the deep yellow color found in the other genera is lost. Among the
flowering plants confined to New Zealand, there is a remarkably high ratio of white-flowered
species. Results of this study indicate that the white-flowered capitulum is a derived character
within Abrotanella originating in New Zealand. A purple-flowered capitulum, also restricted to
Abrotanella, is a repeatedly evolved apomorphic character found in species confined to southern
South America and the sub-Antarctic Campbell and Auckland islands. [Abrotanella; Asteraceae;
Blennosperma; Blennospermatinae; cladistic analysis; Crocidium;floralevolution; flower color; Ischnea; male floret; New Zealand; phylogenetic reconstruction; Senecioneae.]
Phylogenetic analyses using parsimony one species in Chile (Ornduff, 1963, 1964).
methods have corroborated or cast doubt Crocidium is monotypic, annual, and conupon many ideas, hypotheses, and theo- fined to dry places in western North
ries of classification and evolutionary America (Abrams and Ferris, 1960). The
trends in the flowering plants, even within four species of Ischnea are alpine plants rethe largest family, the Asteraceae. Within stricted to the mountains of New Guinea
the subtribe Blennospermatinae of the (Swenson, 1994). Abrotanella is the largest
tribe Senecioneae, many intriguing prob- genus, comprising 19 species of caespitose
lems hitherto not tested by phylogenetic or frequently cushion-forming plants in
methods remain unsolved, e.g., problems (sub)alpine communities. Abrotanella is
of classification, biogeography, and char- confined to the Southern Hemisphere with
acter evolution, such as the frequent evo- a trans-Pacific distribution that includes
lution of white flowers in the New Zealand southern South America, New Zealand, the
flora (Godley, 1979; Webb and Kelly, 1993). sub-Antarctic Campbell and Auckland isThe Blennospermatinae include four lands, Tasmania, and eastern continental
genera: Blennosperma, Crocidium, Ischnea, Australia with New Guinea (Fig. 1; Swenand Abrotanella (Nordenstam, 1977), and son, 1995, 1996). The subtribe thus reflects
their total distribution is almost circum-Pa- interesting distributional patterns at both
cific. Blennosperma grows in a Mediterra- generic and species levels across the Pacific
nean environment, with two species in Ocean at tropical latitudes and along the
western North America (California) and southern border of the Pacific Rim and is
407
408
VOL. 4 6
SYSTEMATIC BIOLOGY
Abrotanella — 4
120*
150'
180*
150*
120*
/
Falkland Islands
60"
FIGURE 1. Total distribution of the Blennospermatinae in the Pacific area. Distribution is shown for Abrotanella ( I ) , with the sub-Antarctic islands and Juan Fernandez Island Masafuera marked with dashed circles,
Blennosperma (H), and Crocidium (H). The distribution of Ischnea in New Guinea is overlapped by the same area
marked for Abrotanella.
an excellent group for biogeographic studies (not discussed here).
When Blennospermatinae was erected,
Rydberg (1914) based the subtribe on the
single genus Blennosperma. Its taxonomic
position has varied over the years, and different authors have allied it to Helenieae,
Heliantheae, Anthemideae, and Senecioneae (for a review, see Ornduff et al.,
1973), but with Crocidium the position now
seems to have settled in the Senecioneae.
The close relationship between Blennosperma and Crocidium is well founded and is
based on pollen ultrastructure (Skvarla
and Turner, 1966; Skvarla et al., 1977) and
secondary metabolites (Ornduff et al.,
1973). Evidence for the position of these
two genera in the Senecioneae is also considerable, including the morphology (Nordenstam, 1977; Bremer, 1987; Gadek et al.,
1989; Karis, 1993a; Bremer, 1994a), chloroplast DNA restriction site data (Jansen et
al., 1990), rbcL sequence data (Kim et al.,
1992), and ndhF sequence data (Kim and
Jansen, 1995; Jansen and Kim, 1996).
The positions of Ischnea and Abrotanella
are more uncertain. Nordenstam (1977)
transferred these two genera to the Blennospermatinae, but whether all four genera
constitute a monophyletic group has been
much debated (Bremer, 1987,1994a; Gadek
et al., 1989; Bruhl and Quinn, 1990, 1991;
Jeffrey, 1992). There are many dissimilarities between these two genera and Blennosperma and Crocidium (Bruhl and Quinn,
1990, 1991), but there is no real evidence
for a position other than in the Blennospermatinae, and some morphological features
indicate a relationship among Blennosperma, Crocidium, and Ischnea (Robinson and
Brettell, 1973; Nordenstam, 1977; Bremer,
1987, 1994a). Pollen characters support inclusion of Ischnea and possibly also Abrotanella in the Blennospermatinae (Skvarla
et al., 1977; Gadek et al., 1989). Inclusion
of Abrotanella is probably the most controversial issue, and H. Robinson (pers.
comm.) has argued that the genus could be
polyphyletic and that the type species, A.
emarginata, is nested within the Senecioni-
1997
SWENSON AND BREMER—EVOLUTION OF THE BLENNOSPERMATINAE
409
nae, whereas the other species may or may ical problems. For example, if a structure
not belong in the Blennospermatinae. Fur- is not present in all taxa, the more charthermore, Hooker (1844, 1846) described acters involved that incorporate that parthree other genera, Scleroleima, Trineuron, ticular structure, the more weight is imand Ceratella, as closely allied to Abrotanel-plicitly assigned to the state "absent,"
la. Currently they are all included in the which is added to each of the characters
same genus, but the relationships have so with this approach. In the Blennospermatifar not been tested.
nae, these problems are unavoidable beIt is often claimed that the flora of New cause Abrotanella lack ray florets and hence
Zealand, or at least parts of it, is a relict all characters connected to that structure
from the ancient Gondwanaland and has are simply absent.
retained primitive reproductive features
This study had four parts. First, we used
(see e.g., Godley, 1979; Lloyd and Wells, two cladistic analyses based on morpho1992; Webb and Kelly, 1993). One debated logical data to test the monophyly of the
issue is why there is such a high ratio of Blennospermatinae and to put forward a
native white-flowered species in New Zea- hypothesis of the phylogenetic relationland and why related species confined to ships within the subtribe. Second, the morthe sub-Antarctic islands are often brightly phological data were analyzed in two
colored (Lloyd, 1985). The question thus ways to evaluate the use of the state "abarises of whether white-flowered species sent" for taxa lacking a particular feature
were ancestral and originally more wide- versus the use of inapplicable states for
spread in the Southern Hemisphere but such characters. Third, we used the resultnow present mainly in New Zealand or ing phylogeny to evaluate Hooker's old
whether they evolved within New Zea- classification and other possible generic
land. Floret color in Abrotanella varies from circumscriptions. Fourth, we examined
yellowish to greenish to purple to com- character evolution, focusing on sexual displetely white but is never the common yel- tribution within the capitula, floret types,
low Asteraceae type. The majority of and floral color in reference to an alleged
white-flowered species are confined to relict flora of the West Pacific area versus
New Zealand (Swenson, 1995), but in the a more recent origin of white-flowered
same region there are also taxa with ca- species in New Zealand.
pitula that contain florets of different colors. From a phylogenetic hypothesis, it
DATA AND METHODS
should be possible to infer which character
Taxa
state is plesiomorphic in the genus.
Ingroup monophyly is necessary for corCoding morphological characters for use
in phylogenetic reconstruction often en- rect rooting of the phylogenetic trees (Nixtails difficult decisions because every char- on and Carpenter, 1993), and the available
acter used is a hypothesis of homology data indicate that the Senecioneae, includand an interpretation of independent evi- ing the Blennospermatinae, are monophydence of relationships (Wilkinson, 1995). letic (e.g., Nordenstam, 1977; Bremer,
One problem addressed in the literature, 1994a). Monophyly of the Blennospermatipossibly not enough, is the use of inappli- nae, however, is not certain although it is
cable states or missing entries (Pimentel likely that at least part of the subtribe is
and Riggins, 1987; Nixon and Davis, 1991; monophyletic.
To evaluate these hypotheses, we includPlatnick et al., 1991). Such problems have
been addressed by Maddison (1993) and ed all 27 taxa of the Blennospermatinae,
Pleijel (1995) among others, and Maddison three species of the subtribe Senecioninae
suggested invoking a state "absent" in- (Delairea odorata [syn. Senecio mikanioides],
stead of considering characters inapplica- Senecio jacobaea, S. vulgaris), two taxa from
ble in taxa lacking particular features. He Tussilagininae (Doronicum clusii, Tephroseralso pointed out subsequent methodolog- is integrifolia), and a former representative
410
SYSTEMATIC BIOLOGY
VOL. 46
could be broken into two characters, a
treatment also invoking inapplicable states
for taxa with sessile capitula, and hence
could be viewed from two approaches. The
data matrix corresponding to the first analysis is given in Appendix 2 and can be
used to construct the matrix for the second
analysis (not shown).
Use of polymorphic characters poses
other problems in phylogenetic reconstruction, and if coded as missing entries they
introduce erroneous consistency indices
and tree lengths (Nixon and Davis, 1991).
Wiens (1995) reviewed different methods
and uses of polymorphic characters and
Characters and Character States
assessed them with five criteria. His conMorphological studies were performed clusion, although reliability and phylogeon material of all species; those of Ischnea netic signal are lower in such characters,
and Abrotanella were described in detail by was that intraspecific variation ought to be
Swenson (1994, 1995, 1996). Coding infor- reported. We believe polymorphic characmation into characters and character states ters do provide a phylogenetic signal, i.e.,
is the most critical stage in a cladistic anal- resolution, and they are here reported with
ysis of morphological data. General prob- the observed states.
lems regarding missing information, quanMultistate characters may be ordered
titative characters, and ordered versus versus unordered or minimally connected
unordered characters have been discussed versus maximally connected, respectively,
by Pimentel and Riggins (1987), Platnick et sensu Slowinski (1993). If there is reason
al. (1991), Stevens (1991), Wilkinson (1992, to believe a character state is intermediate
1995), Maddison (1993), Slowinski (1993), between two other states, it is justifiable to
and Thiele (1993). Following Yeates (1992), order such characters (Wilkinson, 1992,
autapomorphies were included for species 1995; Slowinski, 1993). In our analyses, all
of the ingroup, except when additional aut- multistate characters were treated as unorapomorphic character states in multistate dered except characters 5, 21, 31, 39, and
characters would produce redundant in- 41. These characters represent transforformation in these characters. Unknown mation series and were coded as ordered.
character states are coded with a question For example, receptacle shape (no. 31) is a
mark. Character evolution was traced us- clearly observable transformation series,
ing the computer program MacClade being flat to convex to conical in shape.
(Maddison and Maddison, 1992).
Leaves.—Leaves are commonly entire in
Two character sets were constructed to the Blennospermatinae, whereas the pinevaluate the use of the states "absent" ver- natifid condition, where both basal and
sus "inapplicable." In the first analysis, we cauline leaves are divided, is rare (no. 5).
followed Maddison's (1993) suggestion More commonly, the species have entire or
and used the state "absent" when an organ sometimes trifid rosulate leaves with diwas not present rather than using a sepa- vided cauline leaves. This state is interrate binary presence/absence character (cf. mediate between entire and pinnatifid,
Pleijel, 1995). The characters are shown in and the character was treated as ordered.
Appendix 1. In the second analysis, char- Characters of leaf venation were omitted
acters of ray florets from the first analysis because assessment of presence, number,
were recoded using missing entries (Ap- and development of vascularization was
pendix 1). One character (no. 17) deals arbitrary.
with the peduncle and its pubescence and
Florets.—Floret composition in the capitof the Senecioneae, Arnica montana, now
placed in the Helenieae (Nordenstam,
1977; Bremer, 1994a). We also sampled
taxa from two other tribes: Solidago virgaurea from Astereae and Inula ensifolia from
Inuleae. Taxa were chosen in conjunction
with available rbcL or ndHF sequence data
from EMBL and NCBI/GenBank and morphological variation and to focus on the
Blennospermatinae. For example, Delairea
odorata, a segregate of Senecio (Jeffrey,
1986), was included because sequence data
are available and, like Abrotanella, it lacks
ray florets.
1997
SWENSON AND BREMER—EVOLUTION OF THE BLENNOSPERMATINAE
ulum varies in the Blennospermatinae.
Abrotanella is the only disciform genus; the
other genera are radiate. The presence of
different floret types raises problems of homology and inapplicable character states.
To overcome these problems, one approach
is to postulate that the uniseriate true ray
florets with a well-developed lamina, as in
Blennosperma, Crocidium, Ischnea, and other
Senecioneae (and most Asteroideae), are
lost in Abrotanella and are nonhomologous
to the outer uniseriate, tubular female florets of Abrotanella. Observations supporting this assumption are (1) outer female
florets with five-lobed corollas, as in the
central florets, have been observed in Abrotanella, although they are extremely rare
(Swenson, 1995); (2) styles of the outer female florets in Abrotanella are very different from the styles of the ray florets of the
other genera; and (3) loss of a whole series
of florets in the capitulum may be regulated by a single gene (Gottlieb, 1984). This
interpretation implies that florets within
series in the capitulum should be compared as follows: first series = ray florets,
second series = outer disc florets, and
third series = central disc florets. In Abrotanella, outer and central disc florets correspond to outer and central florets, respectively. Blennosperma, Crocidium, and
Ischnea possess ray florets, outer disc florets, and central disc florets; the outer and
central types usually are referred to collectively as disc florets. Because ray florets
and their features are absent in Abrotanella,
ray floret characters (nos. 33-35, 43, 49) include a state "absent" for the Abrotanella
species (see Platnick et al., 1991; Maddison,
1993). With this approach, however, the assumption of character independence (see
Wilkinson, 1995) could be violated because
the state "ray florets absent" is used in
several characters. Therefore, in the second
analysis we used missing entries in characters 33-35, 43, and 49 (Appendix 1).
The central disc florets are hermaphroditic and perfect, functionally male, or
male (no. 39). Functionally male florets always have a developed but empty cypsela,
which is sometimes much reduced, whereas the male florets entirely lack a cypsela,
411
i.e., the corolla is attached directly to the
receptacle (Swenson, 1994,1995). This reduction into female-sterile florets and
cypsela abortion was considered a transformation series, and the character consequently was treated as additive.
Vascular corolla tissue.—Corolla veins of
the Asteraceae are, as compared with
those of many other families, very reduced
and only a few patterns are normally
found (cf. Gustafsson, 1995). The most
complex type, considered primitive, is a
combination of marginal and central
strands. The marginal strands follow the
corolla lobe margins, and in the lobe sinuses they fuse pairwise. Thus, with the
central strands there are, in a five-lobed
disc floret, 10 strands continuing downward through the corolla tube to the cypsela. The central strands are absent in most
Asteraceae, but the opposite type, with the
marginal strands absent and the central
strands present, is apparently very rare; it
was reported in Abrotanella by Swenson
(1995). Reduction of strands may also be
partial or complete. Abrotanella is possibly
unique in this respect, because it possesses
all these types of vascular tissues (nos. 50,
51).
A true pappus is present only in Crocidium (no. 56). A pappus of scales is sometimes difficult to distinguish from nonhomologous scalelike projections of the
apical cypsela rim, a condition found in
Abrotanella. The scaly projections on cypsela apices of some Abrotanella species are
often interpreted as a pappus (Moore,
1983; Bremer, 1994a). According to our
analyses, however, most Abrotanella species
with cypsela projections are nested within
clades of basically epappose taxa. We
therefore recommend caution when using
the term pappus and prefer to describe
these projections as a rim, crown, or horns.
Cladistics
The two data matrices erected from the
character lists in Appendix 1 were analyzed using a PAUP* 4.0 prerelease version
(Swofford, 1996). Heuristic search options
were used: 100 replicates of random addition sequences of the taxa with tree-bi-
412
SYSTEMATIC BIOLOGY
section-reconnection (TBR) branch swapping, holding five trees at each step, and
saving all equally parsimonious trees. To
evaluate the strongest characters and to
choose among equally parsimonious trees
(Carpenter, 1988, 1994), both analyses
were succeeded by a successive approximations approach to character weighting
based on the rescaled consistency index
(Farris, 1969,1989). Polymorphic taxa were
scored as uncertain in the prerelease version of PAUP* because of difficulties in the
calculation of the rescaled consistency index (K. Rognes, pers. comm.).
Five different values of branch support
were calculated: Bremer support, reweighted and rescaled branch support,
jackknife, and bootstrap with unweighted
and weighted characters. To ease the tedious work of constructing different topological constraints, the program AutoDecay
was used (Eriksson and Wikstrom, 1995).
Bremer support (also termed decay index)
defines the number of extra steps necessary to lose a group in the consensus (Bremer, 1988; Donoghue et al, 1992; Kallersjo
et al., 1992; Farris, 1996). Reweighted and
rescaled branch (Bremer) support values
calculate the robustness for each branch in
the weighted consensus tree (Bremer,
1994b; Gustafsson and Bremer, 1995). Jackknife (Farris et al., 1996) investigates phylogenetic signal, or structure, in a large
matrix without permutation, contrary to
bootstrap (Felsenstein, 1985), but excludes
a designated fraction of characters, here
30%. Analyses of unweighted characters
with 10,000 jackknife and 10,000 bootstrap
replications were performed with "fast
swap" implemented in PAUP*, saving a
single tree. A second bootstrap analysis,
also with 10,000 replicates, was performed
with TBR branch swapping and weighted
characters. The bootstrap procedure has
been discussed by Sanderson (1989), Carpenter (1992), Hillis and Bull (1993), and
Trueman (1993).
RESULTS
The first analysis, using the character
state "absent" as a separate state (Appendix 1), yielded 568 most-parsimonious
VOL. 46
trees, 235 steps long, with a retention index of 0.811 and consistency indices of
0.536 including and 0.530 excluding autapomorphies. Counting steps within the
polymorphic taxa, the trees are 304 steps
long. Successive weighting of the characters stabilized the results after two iterations and yielded 45 most-parsimonious
trees, a subset of the initial 568 trees.
Implementation of inapplicable states in
the second analysis resulted in 190 mostparsimonious trees, 225 steps long, with a
retention index of 0.810 and a consistency
index of 0.536 whether autapomorphies
are included or excluded, i.e., very close to
the indices in the first analysis. As in the
first analysis, successive weighting of the
characters stabilized the result after two iterations and resulted in 42 most-parsimonious trees. However, these trees are not a
subset of and are two (unweighted) steps
longer than the initial 190 trees. Strict consensus trees from the first and second
analyses converge completely with one exception. The outgroup taxa Senecio jacobaea
and Delairea odorata change places in the
unweighted and weighted analyses using
inapplicable states, and thus the branch is
collapsed in the consensus trees shown in
Figure 2. In this figure, each node is numbered, referring to branch support values
given in Table 1.
Resolution of the unweighted and
weighted strict consensus trees is very
similar except that five branches are collapsed (Fig. 2, wavy lines) in the consensus
of unweighted trees. Four of those branches belong to the outgroup, and the fifth is
within a derived clade of Abrotanella,
which reaches better resolution in the
weighted consensus tree. Thus, resolution
is overall somewhat improved after the
successive approximations approach to
character weighting, considerably so in the
outgroup. In the consensus tree, four trichotomies are shown: three in Abrotanella
and one in Ischnea. The resolutions of these
trichotomies differ in the 45 alternative solutions. Topologies among the equally parsimonious trees are dependent upon different character optimization, and there
are only four and two fully resolved solu-
1997
SWENSON AND BREMER—EVOLUTION OF THE BLENNOSPERMATINAE
Inula ensifolia
Solidago virgaurea
Arnica montana
Tephroseris integrifolia
Doronicum clusii
Senecio jacobaea
Senecio vulgaris
Delairea odorata
Crocidium multicaule
Blennosperma bakeri
Blennosperma chilense
Blennosperma nana
Ischnea brassii
Ischnea korythoglossa
Ischnea capellana
Ischnea elachoglossa
Abrotanella purpurea
Abrotanella trichoachaenia
Abrotanella fertilis
Abrotanella linearifolia
Abrotanella trilobata
Abrotanella muscosa
Abrotanella submarginata
Abrotanella diemii
Abrotanella forsteroides
Abrotanella emarginata
Abrotanella rosulata
Abrotanella rostrata
Abrotanella scapigera
Abrotanella spathulata
Abrotanella inconspicua
Abrotanella nivigena
Abrotanella caespitosa
Abrotanella linearis
Abrotanella pusilla
413
supported, with a Bremer support value of
nine steps independent of coding approach, and after successive weighting the
support is enhanced. Abrotanella is the sister group to the other three genera, including Crocidium. A strong sister-group relationship between Blennosperma and Ischnea
is established.
DISCUSSION
Character Analysis
Different approaches to character coding
gave very much the same result in the two
analyses, except for the topology of the
outgroup and the support values. If ray
floret characters in disciform and discoid
taxa are interpreted as inapplicable, there
are fewer most-parsimonious trees when
the character state "absent" is used for
such characters in disciform and discoid
genera. Furthermore, the trees from the
two analyses differ with respect to the topology of the outgroup. The consensus
from the second search with equal weights
grouped the two Senecio species together,
FIGURE 2. Strict consensus tree of Blennosperma- a topology that changed after reweighting.
tinae from two cladistic analyses of morphological Consensus of this second reweighted analdata presented in Appendices 1 and 2, snowing 45
most-parsimonious trees subsequent to successive ysis is, however, identical to the consensus
weighting. Wavy lines represent collapsed branches in from the first analysis using the "absent"
the consensus tree before successive weighting. Bold states, both before and after successive
branches, supporting Blennosperma, Ischnea, Blennosperweighting. In other words, the only time
ma + Ischnea, Abrotanella, and the Blennospermatinae, that the pair S. jacobaea + S. vulgaris is supall have high support values. Numbers above nodes
ported is when the five floral characters
are support values given in Table 1.
are scored as "missing" in disciform and
discoid taxa and analyzed under equal
tions in Abrotanella and Ischnea, respective- weights, whereas when scored as "absent"
ly. In Abrotanella, there are 15 alternative the characters support the pair S. vulgaris
solutions, counting trichotomies. One of + Delairea odorata.
Another interesting result is that clades
the most-parsimonious fully resolved trees
is shown in Figure 3, with characters op- are often better supported when ray floret
characters in disciform and discoid taxa
timized on the branches.
The subtribe Blennospermatinae forms a are interpreted as inapplicable (Table 1).
monophyletic group regardless of the cod- This effect is particularly pronounced for
ing approach used for the ray florets. Sup- the subtribal and generic nodes. For export for the subtribe is considerable, es- ample, branch support for Blennospermatipecially when ray florets were coded as nae (node 1) and Ischnea (node 7) is eninapplicable (Table 1). Likewise, Abrotanel- hanced by three and two steps,
la, Blennosperma, and Ischnea are well-cir-respectively, in the unweighted trees. Supcumscribed monophyletic genera with port for Abrotanella is not less in the second
good support values (Fig. 2, bold branch- analysis with "inapplicable" ray floret
es). Abrotanella monophyly is very well characters, as might be suspected because
414
VOL. 46
SYSTEMATIC BIOLOGY
TABLE 1. Support values of two cladistic analyses of the Blennospermatinae, using "absent" as a separate
state (analysis 1, Appendix 2) versus "inapplicable" (analysis 2). Numbers correspond to nodes in the strict
consensus tree (Fig. 2). Bs = branch support; bwr = weighted and rescaled branch support; jac = jackknife;
bst = bootstrap; bstw = bootstrap using weighted characters.
Analysis 2
Analysis 1
Node
Bs
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
3
1
9
2
3
2
3
1
1
1
1
1
1
1
1
1
2
1
2
1
0
1
0
0
1
1
0
1
bwr
6.6
2.2
18.1
6.0
3.6
2.6
7.7
0.4
1.4
1.0
0.6
1.0
1.2
2.5
0.9
3.3
2.1
1.0
3.3
0.6
0.1
0.5
1.2
2.9
7.0
6.2
0.6
3.2
jac
bst
bstw
Bs
89
70
96
85
95
91
95
36
74
23
28
26
85
37
37
74
56
60
85
8
6
35
14
18
79
51
27
80
82
65
92
77
93
87
87
36
80
23
28
26
76
37
37
66
46
46
74
7
<5
36
14
18
72
46
27
72
94
73
100
93
99
94
95
57
86
47
47
44
57
73
55
78
73
50
79
28
19
57
0
63
91
89
7
87
6
2
9
3
3
1
5
1
1
1
1
1
1
1
1
2
2
1
2
1
0
1
0
0
.3
0
0
2
of the possibly redundant information introduced by a state "absent" in a number
of characters. Jackknife fractions and bootstrap values using fast swap are not significantly different for the two character
coding approaches. Bootstrap values for
weighted characters are practically identical for the two approaches but, as expected, are slightly higher when compared
with those for equally weighted characters.
Classification
The cladistic analyses of the morphological data of the Blennospermatinae support
Nordenstam's (1977) tentative transfer of
Ischnea and Abrotanella to the subtribe,
which then forms a monophyletic group
with strong support values. Three characters appear as synapomorphies of the subtribe: oblong-elliptic phyllaries (no. 24:2),
bwr
7.0
2.2
14.2
6.0
3.7
2.3
7.8
0.4
1.5
1.0
0.6
1.0
1.1
2.5
0.9
2.1
2.1
0.9
3.4
0.6
0.1
0.5
1.2
3.0
9.6
1.7
0.6
3.2
jac
bst
bstw
95
58
95
83
95
75
94
42
88
25
33
31
86
43
46
72
54
61
85
10
7
41
<5
33
92
80
24
81
90
54
90
76
92
68
86
34
80
23
28
26
76
32
36
65
43
48
74
8
6
35
<5
27
84
17
23
70
99
68
99
92
99
88
95
56
85
48
47
44
55
71
55
78
74
51
79
29
19
57
51
67
99
65
34
90
reduction of true pappus (a parallelism in
Crocidium; no. 56:2), and cypsela apex having a smooth or small rim (no. 60:1).
Current generic circumscriptions of
Blennosperma (Ornduff, 1964) and of Ischnea
and Abrotanella (Swenson, 1994, 1995) are
corroborated by substantial support values
(Table 1). Three, three or five, and nine extra steps, respectively, are required to lose
monophyly of these genera. Contrary to
the pattern observed in many other
groups, the monotypic genus Crocidium is
not a specialized derivative of some other
genus but is the sister group of a generic
pair, Blennosperma + Ischnea. Thus, its sta-
tus as a separate genus is strengthened.
The radiate genera of the Blennospermatinae, Crocidium, Blennosperma, and Isch-
nea, form a clade, which is the sister group
of Abrotanella. The position of Ischnea,
1997
,,
SWENSON AND BREMER—EVOLUTION OF THE BLENNOSPERMATINAE
415
tiiUlihlhllntllilii
lan?
t
FIGURE 3. One of the 45 most-parsimonious trees from the first analysis based on morphology of the Blennospermatinae, showing synapomorphies and autapomorphies with no homoplasy (•), homoplastic synapomorphies with subsequent reversals (•)/ parallelisms (parallel bars), and reversals (crossed bars). Numbers are
charactencharacter state (Appendix 1).
416
SYSTEMATIC BIOLOGY
VOL. 46
which has been debated by Bruhl and genome, which is tetraploid (Beuzenberg
Quinn (1990, 1991), Gadek et al. (1989), and Hair, 1984). Our analysis thus conand Bremer (1987,1994a), among others, is firms Hooker's (1864) decision to include
set firmly within the Blennospermatinae as all these genera in Abrotanella.
the sister group of Blennosperma in this Relationships within Abrotanella are not
analysis. Supporting values of node 4 (Fig. fully resolved, and the support values for
2) from the two analyses show that two or the various subgroups, with a few excepthree extra steps are required to break up tions, are low (Table 1). Resolution is
the sister-group relationship (Table 1). slightly improved by using the successive
Reweighted and rescaled support values approximations approach to character
are even stronger, and the jackknife shows weighting, but resolution of node 21 is
a high fraction. The two genera share a supported only by very low reweighted
number of synapomorphies, especially flo- and rescaled branch support values; the
ral characters such as tubeless ray florets jackknife fractions and bootstrap values
and male disc florets. Myxogenic twin are practically missing. There is only one
hairs (character 59:2; Nordenstam, 1968) possible full resolution of the clade, the one
are synapomorphic for Crocidium, Blenno- shown in Figure 3. One topologically basal
sperma, and Ischnea but are secondarily lost clade, supported by node 14 and compriswithin Ischnea.
ing 12 species, possesses functionally male
Monophyly of Abrotanella is particularly disc florets with undivided and cupwell supported by many synapomorphies shaped style apices. The remaining species
(Fig. 3). Branch support values for node 3 form a clade in some of the trees (e.g., Fig.
are substantial in all four measures, 3); they have perfect disc florets (a symplewhether characters of ray florets are inter- siomorphy) and style branches with short
preted as absent or as missing entries (Ta- acute sweeping hairs similar to those
ble 1). We find no indication that the genus found in a few genera of the Heliantheae
is heterogeneous, as has been suggested by (Karis, 1993b). Recognition of two subgenH. Robinson (pers. comm.; also cited by era, easily distinguished by perfect and
Bremer, 1987). The many characters distin- functionally male disc florets, respectively,
guishing Abrotanella from the other genera seems tempting, but in alternative trees the
stress an isolated position, however. The species with perfect disc florets form a
hypothesis that Blennospermatinae is paraphyletic grade rather than a clade.
paraphyletic, with Abrotanella being the Consequently, we refrain from any subgesister group to all other Senecioneae, re- neric classification.
ceives no support.
Hooker (1844,1846) described three othEVOLUTION
er genera for some species of Abrotanella.
Corolla Evolution
These genera, Trineuron, Ceratella, and
Scleroleima, included the species A. forster- There are three main types of florets in
oides, A. rosulata, and A. spathulata; A. pus-the Blennospermatinae: central disc florets,
ilia (described later; Hooker, 1853); and A. outer disc florets, and ray florets. The comnivigena (Mueller, 1855). All these species mon type of ray floret found in the subrepresent branches nested within the Abro- family Asteroideae is female with a tube
tanella phylogeny; e.g., A. scapigera, A. ni- and a radiate, apically three-lobed lamina,
vigena, and A. pusilla represent three dif- which has four main veins apically conferent clades. Moreover, A. forsteroides is nected to three arches corresponding to
sister to A. emarginata and shares a vestig- the three apical lobes. In all radiate genera
ial cypsela attached to functionally male of the Blennospermatinae, the three apical
florets (no. 39:2). Both species form huge lobes are reduced and the lamina has a
cushion fields, but in contrast to A. emar- smooth rounded apex (no. 34:1). Reduction
ginata, A. forsteroides possesses several aut- of the vascular tissue has occurred in Blenapomorphies, possibly because of its larger nosperma and Ischnea; the four veins are not
1997
SWENSON AND BREMER—EVOLUTION OF THE BLENNOSPERMATINAE
417
connected apically but terminate as simple Species with intermediate shapes, difficult
strands below the apex of the lamina (no. to classify as a certain type, also are frequently present (no. 38). Typical well-de49:1).
Reduction of ray floret laminae is well veloped outer disc florets of both types can
known in the family, e.g., in Erigeron and be seen in at least two different clades and
Conyza of the Astereae (Cronquist, 1947). thus have evolved at least twice in the geAmong species in these two genera there nus. Well-developed tubular outer florets
is an evolutionary trend from well-devel- with very short lobes occur in the species
oped laminae to short laminae to very pair A. submarginata + A. muscosa and in
small and filiform ray florets where only A. emarginata and A. diemii. Cyathiform
the tube persists. In Blennosperma and Isch- outer disc florets are found in A. forsteroides
nea, evolution has taken the opposite di- and in the clade stemming from node 17
rection, with a reduction of the tube until (Figs. 2, 3). The clade stemming from node
only a small ring of quadrate cells is left 14 is also characterized by functionally
(no. 33:1). A similar reduction of the tube male central disc florets (no. 39, Fig. 4). An
is reported from Werneria (Senecioneae; interesting feature restricted to this clade,
Karis, 1993a); otherwise, it is a rare char- correlated with the typically cyathiform
acter in the family. Corolla reduction outer disc florets and the functionally male
reaches its extreme in B. nana, where some central disc florets, is that they always have
of the ray florets have lost the corolla com- a corolla with a central vascular strand in
pletely and the ray florets consist of the each lobe (no. 51:1). A single central strand
in each lobe and no other strand is an expistil only (no. 36:1).
Disc florets in the subfamily Asteroideae tremely rare condition in the Asteraceae
and in the Senecioneae are normally per- and has been reported only in Abrotanella
fect and shortly five lobed. Evolution of the (Swenson, 1995). The evolutionary advandisc florets has taken several directions in tage of this character is unclear but may be
the Blennospermatinae, including a differ- related to corolla stability and the pollen
entiation between inner and outer disc flo- presentation mechanism. Vascular strands
rets. The radiate genera, Crocidium, Blen- corresponding to (and central within) each
nosperma, and Ischnea, have all evolved a corolla lobe will alternate with the filabroadly campanulate disc floret corolla, in ments and possibly increase corolla and
many species reinforced just below the anther tube stability, resulting in a more
middle by a ring of quadrate cells. All spe- efficient pollen-pump mechanism. This
cies have five-lobed corollas, except I. ko- mechanism in Abrotanella is very effective,
rythoglossa, where the corolla lobes are re- and examination of old florets shows that
duced to four. The function of a the pollen content is close to nil. This hycomparatively broad corolla is probably pothesis of a correlation between corolla
associated with pollination biology, possi- vascularization and the pollen presentation
bly providing space for short but fairly mechanism is supported by the fact that
wide and stout anthers producing much loss of the central vascular tissue has never
pollen. This large amount of pollen would occurred in the functionally male central
necessitate an efficient pollen presentation disc florets (no. 51:1), but in the female outmechanism. In Blennosperma and Ischnea, er disc florets it happened early in evoluthe style apices have a broad conical shape tion (no. 50:3).
and unusually long sweeping hairs, which
Sexual Evolution
are able to brush up the pollen efficiently
through the anther tube (nos. 44:1, 48:3).
In the radiate genera of the BlennosperIn Abrotanella, the true ray florets are ab- matinae, the ray florets are constantly fesent or completely reduced and the outer male as in most other radiate Asteroideae
disc florets are modified central disc flo- (Karis, 1993a) and therefore not further
rets; this modification involves two differ- discussed here. Disc floret evolution is
ent corolla shapes: tubular and cyathiform. more interesting. The plesiomorphic type
418
VOL. 46
SYSTEMATIC BIOLOGY
'tffM- (L-1 d- (V (L- (L- 0."
t
^f hermaphroditic (39:0)
yellowish - pale green (42:1)
#* functionally male (39:1)
\] whitish - greenish (42:2)
d* functionally male,
cypsela vestigial (39:2)
? floral color unknown
\j white (42:3)
f purple (42:4)
FIGURE 4. Abrotanella realtionships from Figure 3 with distribution, corolla color (character 42), and sex
distribution of central florets (character 39) optimized on the internal and terminal branches. Entirely purple
florets have evolved several times in the genus, but white florets have evolved a single time in an area related
to present New Zealand. Two species, A. emarginata and A. rosulata, have differently colored florets in the same
capitulum, which are represented by two corollas each, the outer floret (left) and the central floret (right). Floret
color for A. dietnii is unknown.
of disc floret is hermaphroditic and fully
fertile (perfect), as found in Crocidium and
in seven species of Abrotanella. Female-sterile disc florets, i.e., functionally male disc
florets, have evolved several times in the
Asteraceae and are known from many
genera, particularly of the subfamily Asteroideae (Bremer, 1994a).
In the Blennospermatinae, loss of disc
floret female fertility has occurred twice,
within Abrotanella (Fig. 4) and in the ancestor of Blennosperma and Ischnea. In Abro-
tanella, female sterility is accompanied by
an undivided cup-shaped style (no. 45:1),
which lacks sweeping hairs and stigmatic
papillae (nos. 46:2, 48:4), and a developed
but empty cypsela. Cypsela reduction is
still in progress and is found in two species, A.
emarginata and A. fbrsteroides,
where the length of the vestigial cypsela is
1997
SWENSON AND BREMER—EVOLUTION OF THE BLENNOSPERMATINAE
419
about 20% that of their closest relatives thulata. Pure white florets, or a loss of color
(no. 39:1, 2; Fig. 4).
pigments, have only evolved once in the
The progenitor of the two sister genera genus. The pure white color characterizes
Blennosperma and Ischnea evolved the most a clade of mainly New Zealand species
specialized male disc florets seen in the (no. 42:3; Fig. 4). Some of these species are
subtribe (no. 39:3), which here are called not entirely white flowered, however, but
male florets because all morphological may have purple-tinged corolla lobes.
parts related to female reproductive func- Three species, A. forsteroides, A. emarginata,
tion are reduced or transformed into or- and A. rosulata, are peculiar in having bigans used in the pollen-pump mechanism. colored florets or capitula, but in very difThe male florets have an undivided, broad, ferent ways. Abrotanella forsteroides has yeland conical style, used only for the pollen lowish or pale green central corollas with
pump, and a completely reduced ovary. a distinct brownish spot on the inner surThere is no cypsela, and the corolla is at- face of the lobes. The possible significance
tached directly to the receptacle. Male flo- of these spots for pollination is unknown.
rets without cypselas are rare in the family Abrotanella emarginata and A. rosulata are
(Burtt, 1977) but occur, for example, also the only species that consistently have difin Osteospermum in the Calenduleae (Nor- ferently colored florets; A. emarginata has
lindh, 1943) and in Lagenocypsela in the As- pale green outer disc florets and purple
tereae (Swenson and Bremer, 1994).
central ones, whereas A. rosulata has purIn contrast to the fairly common loss of ple central disc florets and white outer
disc floret female fertility, loss of disc floret ones. These color combinations are autapomale fertility is much more rare and has morphies and are not considered or shown
occurred once in the Blennospermatinae, in Figure 3 (but see Fig. 4).
i.e., in Abrotanella, where all species have a Reproductive biology in the New Zeaseries of female outer disc florets in addi- land flora was reviewed by Webb and Keltion to the perfect or functionally male cen- ly (1993). More than 60% of the native spetral disc florets (no. 37:1). The segregation cies are white flowered, and if the
of functional sexes between disc and ray mountain flora alone is considered, >78%
florets found in radiate genera is replaced are white (Godley, 1979). Godley comby a most uncommon differentiation with- pared this figure with the 25% white-flowin the true disc florets in Abrotanella, which ered species of the British Isles. The stanlacks ray florets. Other nonradiate genera dard explanation for this difference is the
of the Asteraceae either have an outer se- unspecialized pollinator fauna of New
ries of female florets derived from true ray Zealand, such as the lack of long-tongued
florets (e.g., Erigeron and Conyza; Cron- indigenous bees and the paucity of butterquist, 1947) or generally lack sexual differ- flies (Godley, 1979; Webb and Kelly, 1993).
entiation among the florets.
The question arises whether the whiteflowered species are ancestral and origiFloral Color Evolution
nally more widespread but now present
Floret color in the subfamily Asteroideae mainly in New Zealand or whether they
and in the tribe Senecioneae is mostly yel- are derived and evolved within New Zealow (Bremer, 1994a). The radiate genera of land.
the Blennospermatinae are also yellow
The pattern of white-flowered New Zeaflowered. Within Abrotanella, florets of land species is even more puzzling if the
some species are yellowish, often mixed southern outlying islands are considered.
with a greenish tinge, but they do not have On the sub-Antarctic islands, several spethe deep yellow color found in the radiate cies are brightly colored although their
genera. Purple florets (no. 42:4) have close relatives on the mainland are not;
evolved both in South America, as seen in this is true in spite of an even poorer insect
A. purpurea, A. linearifolia, and A. submar- fauna on these islands than on the New
ginata, and in Australasia, as seen in A. spa- Zealand main islands (Godley, 1979;
420
SYSTEMATIC BIOLOGY
VOL. 46
Lloyd, 1985). In 1976, Raven and Raven confined to the sub-Antarctic islands are
published a study on Epilobium in Austral- derived rather than primitive.
asia and concluded that the group has an
The cladistic analysis is compatible with
Asian origin, that bright colors are ances- the view that the white-flower clade origtral, and that the white-flowered species inated in New Zealand, as indicated by the
evolved in New Zealand. They further position of the white-flower character state
stressed that white-flowered species gave (no. 42:3) at the base of the New Zealand
rise to rose-purple-colored species on clade in Figure 4.
Campbell and Auckland islands. Wardle
Wardle's (1978) hypothesis of the adap(1978) disagreed and suggested that the tive radiation of many vascular plants as a
brightly colored species occurring, for ex- response to an opening up of the New
ample, on the sub-Antarctic islands are Zealand alpine habitats is possibly well
primitive within the genera rather than de- founded. The topology of the white-flower
rived. She stated further that the alpine flo- clade, supported by node 17 in Figure 2,
ra of New Zealand, with many white-flow- includes a set of polymorphic, variable,
ered species, evolved rapidly as a response and nonfixed characters such as leaf apex
to a sudden wide spread of the alpine (no. 10), inflorescence (no. 15), and the deniches during the Quaternary era, i.e., dur- velopment of pedunculate capitula (no. 17;
ing the last 1-3 million years. Lloyd (1985) Fig. 3). Support for interspecific relationquestioned Wardle's conclusion because ships is therefore particularly weak for
the flora of Campbell and Auckland is- nodes 20-22 (Fig. 2; Table 1) and could inlands is thought to be comparatively re- dicate that the group has undergone rapid
cent.
speciation. Furthermore, the comparatively
In summary, there are a number of hy- abundant polymorphism within the spepotheses as to the origin of the white-flow- cies radiating at these nodes could also inered species confined to New Zealand and dicate that they are young taxa.
whether the closely related colored species
Two intriguing questions still remain
confined to sub-Antarctic islands are prim- concerning the type of capitula and the floitive or derived. However, few phylogenet- ral color in Abrotanella. Why do species so
ic studies so far have been performed to often have sessile capitula more or less
test these two groups of hypotheses. In the hidden among the leaves? What adaptive
alpine genus Abrotanella, all of the entirely value could colors other than yellow, paror partly white-flowered species are ticularly purple, have? The pollination bigrouped in a clade of nine species, seven ology of Abrotanella is completely unof which are confined to New Zealand known, so we can only speculate on these
(Fig. 4). Two of these seven species, A. spa- topics. The capitula of Abrotanella are very
thulata and A. rosulata, are confined to the small, <5 mm wide, and are often sessile,
sub-Antarctic Auckland and Campbell is- and most species form cushions or low
lands, and both of these species have pur- mats in windy, moist alpine habitats where
ple central florets. Thus, the pattern of flying insects are scarce. When the sun
white-flowered species in New Zealand, shines, the surface of the cushions or mats
with closely related but brightly colored soon becomes warm, several degrees
species on the sub-Antarctic islands, is re- warmer than the surrounding air, and varpeated in Abrotanella. The cladistic analysis ious types of insects, especially small beeindicates that there is a white-flower clade tles, have frequently been seen crawling on
in New Zealand that includes secondarily the plants (Swenson, pers. obs.). A conevolved purple-flowered species confined spicuous yellow-flowered head on a peto Auckland and Campbell islands. These duncle, suitable for attracting flying inspecies, A. spathulata and A. rosulata, have sects, is probably of low adaptive value in
an apomorphic position in the phylogenet- this environment. Rather, a sessile capituic tree and thus support the view of Lloyd lum positioned among the leaves is more
(1985) that such brightly colored species accessible to the available pollinators.
1997
SWENSON AND BREMER—EVOLUTION OF THE BLENNOSPERMATINAE
As to the white color, or lack of floral
pigments, a fly-dominated pollinator fauna
is a possible explanation (L. A. Nilsson,
pers. comm.). The white-flowered species
with purple lobes and the purple-flowered
species may have acquired their floral pigmentation as a protection against intense
sunlight. Possibly, there is a simple genetic
on/off regulation of pigment production,
which could explain the parallel evolution
of purple-flowered species and the presence of purple lobes in several white-flowered species. The question still remains:
why do pedunculate capitula (no. 17:2)
reappear twice in this white-flower clade?
We have no unequivocal answer, but there
may be a connection with the habitat of the
pedunculate species, which often grow in
more sheltered environments such as in
subalpine grasslands and under shrubs.
CONCLUSIONS
In conclusion, different coding approaches to the morphological data, using
"absent" as a separate state versus "inapplicable," do not result in any different
consensus of the Blennospermatinae. Fewer trees were found in the unweighted
analysis using the inapplicable characters
approach, giving a consensus that changed
topology in the outgroup after successive
weighting. This topology converged completely with the result obtained when "absent" was used as a separate state. Coding
ray florets as inapplicable strengthens rather than diminishes the branch support values. Thus, in the analysis of the morphological data of the Blennospermatinae,
inapplicable states do not weaken the phylogenetic signal; rather, in most cases the
signal is strengthened.
The monophyly of the Blennospermatinae, although a heterogeneous assemblage
of radiate and disciform genera, is well
founded according to our analysis. The
four genera of the subtribe, Abrotanella,
Crocidium, Blennosperma, and Ischnea, are
all well circumscribed as monophyletic
(Ornduff, 1964; Swenson, 1994, 1995,
1996). A strong sister-group relationship is
established between Blennosperma and Ischnea, which are confined to the New World
421
and New Guinea, respectively. Another
sister-group relationship was found between Abrotanella and the other three radiate genera.
Several types of sexual distributions
within the capitula have evolved in the
Blennospermatinae. The most striking type
is the male flower in Blennosperma and Ischnea, which has a corolla attached directly
to the receptacle and a completely reduced
cypsela. Another evolutionary pathway,
where female reproductive organs are
transformed into structures reinforcing the
male function, comprises the functionally
male florets found in Abrotanella. In a few
species, the trend is continued, as indicated by vestigial cypsela remains.
Floral color is variable in Abrotanella,
from yellowish to pale green to whitishgreenish to pure white and purple. A derived clade within Abrotanella has white
flowers, with most species confined to
New Zealand. Purple-flowered species are
derived in this particular clade and are
nested in other parts of the Abrotanella
clade. White-flowered Abrotanella species
appear to be a novelty in New Zealand,
and purple-flowered species arose several
times, twice in connection with the subAntarctic Campbell and Auckland islands.
ACKNOWLEDGMENTS
We thank Victor Albert, Anders Backhand, and Birgitta Bremer for valuable discussions on character coding and data analysis and Per-Ola Karis for help in
interpretations of morphology. We also thank Richard
Olmstead, David Cannatella, Arne Anderberg, and
two anonymous reviewers for many constructive suggestions in connection with the earlier version of the
manuscript. Anders Nilsson criticized and commented upon our discussion on floral evolution. The study
was supported by a Swedish Natural Science Research
Council grant for studies on Asteraceae evolution. Several travel grants, from Enander and Harald E. Johansson funds, the Royal Swedish Academy of Sciences, and Anna Maria Lundin fund, Smalands
Nation (Uppsala University), supported Ulf Swenson's
field studies in South America, Australia, and New
Zealand.
REFERENCES
ABRAMS, L., AND R. S. FERRIS. 1960. Illustrated flora
of the Pacific states, Volume 4. Oxford Univ. Press,
London.
BEUZENBERG, E. J., AND J. B. HAIR. 1984. Contributions
422
SYSTEMATIC BIOLOGY
to a chromosome atlas of the New Zealand flora—
27. N.Z. J. Bot. 22:353-356.
BREMER, K. 1987. Tribal interrelationships of the Asteraceae. Cladistics 3:210-253.
BREMER, K. 1988. The limits of amino acid sequence
data in angiosperm phylogenetic reconstruction.
Evolution 42:795-803.
BREMER, K. 1994a. Asteraceae, cladistics and classification. Timber Press, Portland, Oregon.
BREMER, K. 1994b. Branch support and tree stability.
Cladistics 10:295-304.
BRUHL, J. J., AND C. J. QUINN. 1990. Cypsela anatomy
in the "Cotuleae" (Asteraceae—Anthemideae). Bot.
J. Linn. Soc. 102:37-59.
BRUHL, J. J., AND C. J. QUINN. 1991. Floral morphol-
ogy and a reassessment of affinities in the "Cotuleae" (Asteraceae). Aust. Syst. Bot. 4:637-654.
BURTT, B. L. 1977. Aspects of diversification in the
capitulum. Pages 41-59 in The biology and chemistry of the Compositae (V. H. Heywood, J. B. Harborne, and B. L. Turner, eds.). Academic Press, London.
CARPENTER, J. M. 1988. Choosing among multiple
equally parsimonious cladograms. Cladistics 4:291296.
CARPENTER, J. M. 1992. Random cladistics. Cladistics
8:147-153.
CARPENTER, J. M. 1994. Successive weighting, reliability and evidence. Cladistics 10:215-220.
CRONQUIST, A. 1947. Revision of the North American
species of Erigeron, north of Mexico. Brittonia 6:121302.
VOL. 46
phology and phylogenetic interrelationships of the
Asteraceae, Calyceraceae, Campanulaceae, Goodeniaceae, and related families (Asterales). Am. J. Bot.
82:250-265.
HILLIS, D. M., AND J. J. BULL. 1993. An empirical test
of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst. Biol. 42:182192.
HOOKER, J. D. 1844. Botany of the Antarctic voyage
of the Erebus & Terror, Volume 1. Flora Antarctica.
Reeve Brothers, London.
HOOKER, J. D. 1846. A new genus of Compositae.
Lond. J. Bot. 5:444-446.
HOOKER, J. D. 1853. Botany of the Antarctic voyage
of the Erebus & Terror, Volume 2. Flora of New Zealand, Volume 1. Reeve Brothers, London.
HOOKER, J. D. 1864. Handbook of the New Zealand
flora. London.
JANSEN, R. K., K. E. HOLSINGER, H. J. MICHAELS, AND
}. D. PALMER. 1990. Phylogenetic analysis of chloroplast DNA restriction site data at higher taxonomic levels: An example from the Asteraceae. Evolution
44:2089-2105.
JANSEN, R. K., AND K.-J. KIM. 1996. Implications of
chloroplast DNA for the classification and phylogeny of the Asteraceae. Proc. Int. Compositae Conf.
1996:317-339.
JEFFREY, C. 1986. The Senedoneae in east tropical Africa. Kew Bull. 41:873-943.
JEFFREY, C. 1992. Notes on Compositae, VI. The tribe
Senecioneae (Compositae) in the Mascarene Islands
with an annotated world check-list of the genera of
DONOGHUE, M. L., R. G. OLMSTEAD, J. F. SMITH, AND
the tribe. Kew Bull. 47:49-109.
J. D. PALMER. 1992. Phylogenetic relationships of KALLERSJO, M., J. S. FARRIS, A. G. KLUGE, AND C. BULT.
Dipsacales based on rbch sequences. Ann. Mo. Bot.
1992. Skewness and permutation. Cladistics 8:275Gard. 79:333-345.
287.
ERIKSSON, T., AND N. WIKSTROM. 1995. AutoDecay,
version 3.O.*. Botaniska Institutionen, Stockholm KARIS, P. Q 1993a. Morphological phylogenetics of
the Asteraceae—Asteroideae, with notes on charUniv., Stockholm.
acter evolution. Plant Syst. Evol. 186:69-93.
FARRIS, J. S. 1969. A successive approximations approach to character weighting. Syst. Zool. 18:374- KARIS, P. Q 1993b. Heliantheae sensu lato (Asteraceae), clades and classification. Plant Syst. Evol. 188:
385.
139-195.
FARRIS, J. S. 1989. The retention index and the reKIM, K.-J., AND K. JANSEN. 1995. ndhF sequence evoscaled consistency index. Cladistics 5:417-419.
lution and the major clades in the sunflower family.
FARRIS, J. S. 1996. Names and origins. Cladistics 12:
Proc. Natl. Acad. Sri. USA 92:10379-10383.
263-264.
FARRIS, J. S., V. A. ALBERT, M. KALLERSJO, D. LIPSCOMB,
AND A. G. KLUGE. 1996. Parsimony jackknifing outperforms neighbor-joining. Cladistics 11:99-124.
FELSENSTEIN, J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution
39:783-791.
GADEK, P. A., J. J. BRUHL, AND C. J. QUINN. 1989. Ex-
KIM, K.-J., R. K. JANSEN, R. S. WALLACE, H. J. MICHELS,
AND J. D. PALMER. 1992. Phylogenetic implications
of rbch sequence variation in the Asteraceae. Ann.
Mo. Bot. Gard. 79:428-445.
LLOYD, D. G. 1985. Progress in understanding the natural history of New Zealand plants. N.Z. J. Bot. 23:
707-722.
ine structure in the "Cotuleae" (Anthemideae, Asteraceae). Grana 28:163-178.
GODLEY, E. J. 1979. Flower biology in New Zealand.
N.Z. J. Bot. 17:441-466.
GOTTLIEB, L. D. 1984. Genetics and morphological
evolution in plants. Am. Nat. 123:681-709.
GUSTAFSSON, M. H. G. 1995. Petal venation in the Asterales and related orders. Bot. J. Linn. Soc. 118:118.
LLOYD, D. G., AND M. S. WELLS. 1992. Reproductive
GUSTAFSSON, M. H. G., AND K. BREMER. 1995. Mor-
MacClade: Analysis of phylogeny and character
biology of a primitive angiosperm, Pseudowintera colorata (Winteraceae), and the evolution of pollination
systems in the Anthophyta. Plant Syst. Evol. 181:
77-95.
MADDISON, W. P. 1993. Missing data versus missing
characters in phylogenetic analysis. Syst. Biol. 42:
576-581.
MADDISON, W. P., AND D. R. MADDISON. 1992.
1997
SWENSON AND BREMER—EVOLUTION OF THE BLENNOSPERMATINAE
evolution, version 3.0. Sinauer, Sunderland, Massachusetts.
MOORE, M. M. 1983. Flora of Tierra del Fuego. Anthony Nelson, England.
MUELLER, F. 1855. Descriptive characters of new alpine plants from continental Australia. Trans. Philos. Soc. Victoria 1:96-111.
NIXON, K. C, AND J. I DAVIS. 1991. Polymorphic taxa,
missing values and cladistic analysis. Cladistics 7:
233-241.
NIXON, K. C, AND J. M. CARPENTER. 1993. On out-
groups. Cladistics 9:413^26.
NORDENSTAM, B. 1968. The genus Euryops. Part II. Aspects of morphology and cytology. Bot. Not. 121:
209-232.
NORDENSTAM, B. 1977. Senecioneae and Liabeae—
Systematic review. Pages 799-830 in The biology
and chemistry of the Compositae (V. H. Heywood,
J. B. Harborne, and B. L. Turner, eds.). Academic
Press, London.
NORLINDH, T. 1943. Studies in the Calenduleae I.
Gleerup, Lund, Sweden.
ORNDUFF, R. 1963. Experimental studies in two genera of Helenieae (Compositae): Blennosperma and
Lasthenia. Q. Rev. Biol. 38:141-150.
ORNDUFF, R. 1964. Biosystematics of Blennosperma
(Compositae). Brittonia 16:289-295.
423
SWENSON, U. 1994. The genus Ischnea (Asteraceae, Senecioneae) in New Guinea. Plant Syst. Evol. 191:
247-263.
SWENSON, U. 1995. Systematics of Abrotanella, an amphi-Pacific genus of Asteraceae (Senecioneae). Plant
Syst. Evol. 197:149-193.
SWENSON, U. 1996. Abrotanella rostrata (Asteraceae, Senecioneae)—A new species for New Zealand. N.Z.
J. Bot. 34:47-50.
SWENSON, U, AND K. BREMER. 1994. The genus La-
genocypsela (Asteraceae, Astereae) in New Guinea.
Aust. Syst. Bot. 7:265-273.
SWOFFORD, D. L. 1996. PAUP*: Phylogenetic analysis
using parsimony (*and other methods), version 4.0.
Sinauer, Sunderland, Massachusetts.
THIELE, K. 1993. The holy grail of the perfect character: The cladistic treatment of morphometric data.
Cladistics 9:275-304.
TRUEMAN, J. W. H. 1993. Randomization confounded:
A response to Carpenter. Cladistics 9:101-109.
WARDLE, P. 1978. Origin of the New Zealand mountain flora, with special reference to trans-Tasman relationships. N.Z. J. Bot. 16:535-550.
WEBB, C. J., AND D. KELLY. 1993. The reproductive
biology of the New Zealand flora. Trends Ecol. Evol.
8:442^47.
WIENS, J. J. 1995. Polymorphic characters in phylogenetic systematics. Syst. Biol. 44:482-500.
ORNDUFF, R., N. A. M. SALEH, AND B. A. BOHM. 1973.
The flavonoids and affinities of Blennosperma and WILKINSON, M. 1992. Ordered versus unordered
characters. Cladistics 8:375-385.
Crocidium (Compositae). Taxon 22:407-412.
PIMENTEL, R. A., AND R. RlGGlNS. 1987. The nature of WILKINSON, M. 1995. A comparison of two methods
of character construction. Cladistics 11:297-308.
cladistic data. Cladistics 3:201-209.
YEATES, D. 1992. Why remove autapomorphies? ClaPLATNICK, N. I., C. E. GRISWOLD, AND J. A. CODDINGdistics 8:387-389.
TON. 1991. On missing entries in cladistic analysis.
Cladistics 7:337-343.
Received 12 January 1996; accepted 25 March 1997
PLEIJEL, F. 1995. On character coding for phylogeny Associate Editor: Richard Olmstead
reconstruction. Cladistics 11:309-315.
RAVEN, P. H., AND T. E. RAVEN. 1976. The genus EpAPPENDIX 1
ilobium (Onagraceae) in Australasia: A systematic
CHARACTERS
AND CHARACTER STATES
and evolutionary study. N.Z. Dep. Sci. Indust. Res.
First Cladistic Analysis of the Blennospermatinae
Bull. 216:1-321.
ROBINSON, H., AND R. D. BRETTELL. 1973. Tribal re1. Plants not caespitose or cushion forming (0); caesvisions in the Asteraceae. IX. The relationship of
pitose or cushion forming (1).
Ischnea. Phytologia 26:153-158.
2. Plants perennial (0); annual (1).
RYDBERG, P. A. 1914. Carduaceae: Helenieae. North
3. Leaves cauline (0); cauline, rosulate (1); rosulate to
Am. Flora 34:1-80.
densely imbricate (2).
SANDERSON, M. J. 1989. Confidence limits on phytog4. Leaves oblong-elliptic (0); widely oblong-elliptic,
enies: The bootstrap revisited. Cladistics 5:113-129.
minute (1); oblanceolate-linear (2); obovate (3);
SKVARLA, J. J., AND B. L. TURNER. 1966. Pollen wall
cordate (4).
ultrastructure and its bearing on the systematic po5. All leaves entire (0); basal leaves trifid or entire
sition of Blennosperma and Crocidium (Compositae).
and cauline leaves divided (1); all leaves pinnatifid
Am. J. Bot. 53:555-563.
(2).
SKVARLA, J. J., B. L. TURNER, V. C. PATEL, AND A. S.
6. Leaves sessile (0); with a sheathlike petiole (1);
TOMB. 1977. Pollen morphology in the Compositae
petiole forming a true sheath (2); with petiole, not
and morphologically related families. Pages 141sheathlike (3).
248 in The biology and chemistry of the Compositae
7. Leaves scabrate hairy (0); septate hairy on surface
(V. H. Heywood, J. B. Harborne, and B. L. Turner,
(1); septate hairy on margin only (2); glabrous (3).
eds.). Academic Press, London.
8. Leaves flat (0); recurved (1); keeled (2).
SLOWINSKI, J. B. 1993. "Unordered" versus "ordered"
9. Leaf margin dentate (0); denticulate (1); entire (2).
characters. Syst. Biol. 42:155-165.
10. Leaf apex obtuse or/to acute (0); retuse (1); apicSTEVENS, P. F. 1991. Character states, morphological
ulate (2); acuminate (3).
variation, and phylogenetic analysis: A review. Syst. 11. Leaf apex without a scariose or hyaline texture (0);
Bot. 16:553-583.
with a scariose or hyaline texture (1).
424
SYSTEMATIC BIOLOGY
12. Leaf axils glabrous (0); with tufts of hairs (1).
13. Leaf cavities without multicellular glands (0); with
multicellular glands (1).
14. Stomata on adaxial and abaxial leaf surfaces (0);
on adaxial leaf surface (1); on abaxial leaf surface
(2).
15. Inflorescence branched (0); unbranched (1).
16. Flowering stem glabrous (0); whitish hairy (1);
brownish hairy (2).
17. Flowering capitula on a hairy peduncle (0); on a
glabrous peduncle (1); subsessile to sessile in anthesis, peduncle elongating after anthesis (2); subsessile to sessile even after anthesis (3).
18. Peduncle with leaflike bracts of one type (0); with
leaflike bracts of two types (1); without bracts (2).
19. Capitula ecalyculate (0); calyculate (1).
20. Involucre of unequal and strongly imbricate phyllaries (0); of ± equal and hardly imbricate phyllaries (1).
21. Phyllaries >4-seriate (0); 2- or 3-seriate (1); 1-seriate (2).
22. Phyllaries at base free (0); fused (1).
23. Phyllaries in fruiting stage not forming a hard
cup (0); fused and forming a hard cup (1).
24. Phyllaries lanceolate (0); linear (1); oblong-elliptic
(2); obovate (3).
25. Phyllaries with pubescent margins (0); surface (1);
apex (2); surface and apex (3); glabrous (4).
26. Phyllaries without glandular hairs (0); with glandular hairs (1).
27. Phyllary margin herbaceous (0); scariose (1).
28. Phyllary apex acute (0); apiculate (1); obtuse (2);
retuse (3).
29. Vascular strand(s) in phyllaries >5 (0); 3 (1); 1 (2);
0(3).
30. Phyllaries without translucent (secretory) ducts
(0); with translucent ducts (1).
31. Receptacle flat (0); convex (1); conical (2).
32. Receptacle naked (0); hairy (1).
33. Ray florets laminate with a developed tube (0);
laminate but tube reduced to a ring (1); ray florets
absent (2).
34. Ray floret apex 3-lobed (0); rounded without lobes
(1); lamina absent (2).
35. Tube or ring of ray florets with trichomes (0); glabrous (1); ray florets absent (2).
36. All florets with developed corolla (0); some florets
lack a corolla (1).
37. Outer disc florets perfect (0); female (1); male (2).
38. Outer and central disc floret corolla of similar
morphological type (0); of two distinct morphological types (1).
39. Central disc florets perfect (0); functionally male,
cypsela well developed (1); functionally male, cypsela vestigial (2); male (3).
40. Central disc florets campanulate (0); broadly campanulate with no or short tube (1); broadly campanulate with a long tube (2); tubular (3).
41. Disc florets 5-lobed (0); 4-lobed (1); 3-lobed (2).
42. Disc florets yellow (0); yellowish or pale green (1);
whitish or green, often with purple lobes (2); pure
white, sometimes with purplish lobes (3); purple
(4).
VOL. 46
43. Style branches of ray florets long, linear, truncate
(0); narrowly elliptic, obtuse (1); short, obovate (2);
ray florets absent (3).
44. Style of outer disc florets divided (0); undivided
with a conical apex (1).
45. Style of central florets divided, truncate (0); undivided with a truncate to cup-shaped apex (1);
undivided with a conical apex (2).
46. Style branches of central disc florets with a continuous surface of stigmatic papillae (0); with stigmatic papillae in two separate lines (1); without
stigmatic papillae (2).
47. Style branches without apical collar of hairs (0);
with a short apical tuft of hairs (1).
48. Sweeping hairs of central florets long, acute, decurrent (0); short, acute, not decurrent (1); short,
smooth, obtuse (2); fairly long, obtuse to apiculate,
striate (3); reduced (4).
49. Vascular tissue in ray floret lamina interconnected
at apex (0); not interconnected at apex (1); ray florets absent (2).
50. Vascular tissue in outer disc floret corolla lobes
marginal (0); central (1); rudimentary, in base of
corolla only (2); completely reduced (3).
51. Vascular tissue in central floret corolla lobes marginal (0); central (1); marginal and central (2);
completely reduced (3).
52. Anther tails caudate, branched (0); caudate, unbranched (1); ecaudate (2).
53. Anther appendage deltoid (0); oblong (1); obovate
(2); subulate (3).
54. Endothecium radial (0); polarized (1).
55. Filament collars cacalioid (0); senecioid (1).
56. Pappus of pluriseriate bristles (0); uniseriate bristles (1); completely reduced (2).
57. Cypselas ellipsoid (0); obovoid (1); obovate, flattened, curved (2); terete (3).
58. Cypselas with nerves (0); ribs (1); thickened translucent ribs (2).
59. Cypselas with simple hairs (0); nonmyxogenic
twin hairs (1); myxogenic twin hairs (2); papillose
(3); glabrous (4).
60. Cypsela apex with a widening, marked ring (0);
smooth and/or with a small rim (1); with a crown
or awns (2); with horns (3).
61. Cypsela apex not beaked (0); beaked (1).
62. Cypsela without carpopodium (0); with carpopodium (1).
Second Cladistic Analysis of the Blennospermatinae
These characters and character states differ from
those used in the first analysis. Taxa without a putative organ (peduncles or ray florets) are coded as inapplicable for characters and assigned a question
mark in the matrix (not shown).
17a. Flowering capitula pedunculate (0); subsessile to
sessile in anthesis, pedunculate after anthesis (2);
subsessile to sessile even after anthesis (3).
17b. Peduncle hairy (0); glabrous (1).
33a. Capitula radiate (0); disciform (1); discoid (2).
33b. Ray floret lamina with a developed tube (0); tube
reduced to a ring (1).
1997
34.
35.
38.
425
SWENSON AND BREMER—EVOLUTION OF THE BLENNOSPERMATINAE
Ray floret apex 3-lobed (0); rounded without
lobes (1).
Tube or ring of ray florets with trichomes (0);
glabrous (1).
Not included, replaced by character 33a.
43. Style branches of ray floret long, linear, truncate
(0); narrowly elliptic, obtuse (1); short, obovate
(2).
49. Vascular tissue in ray floret lamina interconnected at apex (0); not interconnected at apex (1).
APPENDIX 2
Data matrix assembled using the characters from the first analysis (Appendix 1) for the outgroup (first eight
taxa) and the Blennospermatinae (Asteraceae; Senecioneae). Polymorphic or variable taxa are coded with letters
in the matrix: a = 0/1; b = 1/2; c = 0/2; d = 2/3; e = 0/1/2; f = 1/3; g = 1/2/3; h = 1/4; i = 2/4; j =
3/4; ? = missing data.
Character numbers
l
Taxon
1234567890
1111111112
1234567890
Inula ensifolia
Solidago virgaurea
Arnica montana
Dekdrea odorata
Doronicum clusii
Senecio jacobaea
Senecio vulgaris
Tephroseris integrifolia
Abrotanella caespitosa
Abrotanella diemii
Abrotanella emarginata
Abrotanella fertilis
Abrotanella forsteroides
Abrotanella inconspicua
Abrotanella linearifolia
Abrotanella linearis
Abrotanella muscosa
Abrotanella nivigena
Abrotanella purpurea
Abrotanella pusilla
Abrotanella rostrata
Abrotanella rosulata
Abrotanella scapigera
Abrotanella spathulata
Abrotanella submarginata
Abrotanella trichoachaenia
Abrotanella trilobata
Blennosperma bakeri
Blennosperma chilense
Blennosperma nanum
Crocidium multicaule
Ischnea brassii
Ischnea capellana
Ischnea elachoglossa
Ischnea korythoglossa
0002003020
OOOOOOOOcO
0010011020
0004033000
0000031000
0000231000
010020f000
0010031000
1022012020
1021013020
1021023021
102201d020
1021013013
1022012022
1022013022
101201202e
1022013021
102201202a
1022013020
101201d022
101201d220
102101302c
101201g222
101201d220
1022013021
1022013020
1022013022
0102113021
0100111021
0100213021
011d013021
1012113121
1013233121
1012013121
1012113121
0000000000
0000000000
0000010001
0002001011
0002110201
0100010011
0100010011
0100010001
0010102001
0017103201
1010103201
0010102c01
1010102201
0010103201
0010102c01
OOlOacaOOl
1010103201
00101c2001
0010102201
0010101001
0010021101
0010003101
0010021101
0010021101
1010103201
0010102201
0010102c01
0100000201
0a00010201
0100aa0201
0100101201
0001101201
0107101201
0a011cl201
0107101201
2222222223
1234567890
3333333334
1234567890
4444444445
1234567890
5555555556
1234567890
66
12
0000000000
0000101020
1000110000
2000201020
1000110000
2000201020
2000201020
2000100000
1002401221
1002401220
b002401220
1003401321
b012400230
100b401221
1002401220
1002401b21
1002401220
1002401221
1002401220
100b401121
1002401221
100b401021
100b401121
1002401b21
1002401220
10024012e0
1002401230
21022012a0
2102301210
2102301210
b00220a200
100di002aO
1002200200
100di002a0
1002200010
1000100000
1000000000
1100000002
0022200002
1100100000
0000100002
0022200002
1000100002
0022201110
0022201110
0022201120
0022201103
0022201120
0022201110
0022201103
0022201110
0022201103
0022201110
0022201100
0022201110
0022201110
0022201110
0022201110
0022201110
0022201103
0022201100
0022201103
1011102031
1011102031
1011112031
2001100001
1011102031
1011102031
a011102031
0011102031
0000000000
0000010000
0000010200
0030011220
0000001100
0000011200
a030011220
0000001200
1330120421
b?30120423
bh30120423
bl30000123
1130120420
1330120421
1430000123
133012042d
b230000123
b330120421
1430000122
1330120423
b330120423
1J30120423
a330120421
b430120423
b430000123
bl30000122
2230000123
0011220310
a011220310
0011220310
0010010300
0021220310
0021220310
0021220310
1021220310
0030000100
0100003010
0200000100
0110110140
0101010140
0110110110
0210110110
0201010110
1111021141
0117721131
011102al41
1111020141
C111021141
111102al41
311102al41
1111020141
0111021112
1111021231
211aO2aO42
111102al43
1111020231
1111021233
1111021231
1111021231
311102all2
211aO2aO12
311102al42
0201021121
0201021121
0201021121
0201011121
0221022021
0221022041
0221022041
0221022041
00
00
00
00
00
00
00
00
00
00
00
00
00
00
00
aO
00
00
00
00
11
00
00
00
00
00
00
00
00
00
00
00
00
00
00