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0 Jepson Herbarium and Department of Integrative Biology, 1001 Valley Life Sciences Building #2465, University of California, Berkeley, California 94720-2465 USA
Received for publication October 12, 1999. Accepted for publication February 4, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Arnica • Asteraceae • chromosome evolution • Compositae • dysploidy • Heliantheae • ITS • Madiinae • phylogeny
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Baldwin, 1997
), one of the most spectacular examples of insular radiation in plants, and the mostly Californian, continental tarweeds, a paraphyletic group that includes the closest living relatives of the Hawaiian lineage (Baldwin et al., 1991
; Baldwin, 1996
) and comprises classic examples of different modes of diversification and chromosome evolution (Clausen, 1951
).
Comparative evolutionary studies in Madiinae rest on a foundation of compelling anatomical evidence that the group, as circumscribed by Carlquist (1959)
, is monophyletic. Among the diagnostic morphological characteristics of Madiinae noted by Carlquist (1959)
, the two most easily observed features in plants with radiate heads are (1) receptacular bracts or paleae confined to a ring between the ray and disc florets, a condition found in most taxa of the group, and (2) phyllaries each associated with a ray floret, with the lower, lateral margins of each phyllary at least partially clasping a ray ovary. The abaxial surfaces of the phyllaries are typically covered with sticky glands or gland-tipped hairs; the involucral bract and associated fruit can be externally animal dispersed as a unit.
Carlquist's (1959)
undisputed circumscription of Madiinae has long stood in contrast to our lack of knowledge about the phylogenetic position of Madiinae within Compositae, a deficiency that has impeded understanding of the origin and ancestral characteristics of the tarweed–silversword lineage. Jepson (1901)
treated tarweeds as a tribe (Madieae), presumably in response to the distinctiveness of the group and apparent absence of close relatives. Most subsequent workers (e.g., Keck, 1959
; Stuessy, 1977
; Robinson, 1981
) have treated tarweeds as a subtribe of Heliantheae, usually in close taxonomic association with the "core" of the tribe, i.e., Heliantheae s.s. (sensu stricto) (but not Robinson, 1981
; see below). Madiinae and Heliantheae s.s. both possess receptacular bracts (otherwise rare in Compositae) and often dark-colored anthers, although anther pigments in the two groups appear to be chemically different (Robinson, 1981
).
Carlquist (1958)
intimated a possible close relationship of the tarweed–silversword group to epaleate members of Heliantheae s.l. (sensu lato) (i.e., including helenioid Heliantheae or Helenieae s.l.), such as Palafoxia and Chaenactis, on the basis of trichome similarities. Robinson (1981)
reinforced Carlquist's view, pointing out that Madiinae appears to "bridge the morphological gap between epaleate and paleate groups of Heliantheae" and "in many respects resemble the epaleate group." Results of morphology-based phylogenetic analyses by Bremer (1987)
and Karis (1993a)
placed Madiinae (and the epaleate genera Palafoxia and Chaetymenia in Karis's trees) sister to a clade comprising most other paleate Heliantheae, with Madiinae plus Heliantheae s.s. embedded in a paraphyletic group of epaleate, helenioid Heliantheae. A family-wide molecular phylogenetic analysis of Compositae by Kim and Jansen (1995)
placed Madia elegans (the sole tarweed sampled) within a well-supported clade comprising Eupatorieae and other Heliantheae s.l., with M. elegans part of a large, internally unresolved lineage exclusive of Gaillardiinae s.l. and Coreopsidinae.
In light of the lack of resolution within the lineage corresponding to Heliantheae s.l. plus Eupatorieae in Kim and Jansen's (1995)
ndhF tree, we studied relationships of the tarweed–silversword group using a more rapidly evolving set of sequences, in the internal transcribed spacer (ITS) region of nuclear rDNA. We sought understanding of relationships of Madiinae to clarify the ancestral morphological, ecological, and chromosomal characteristics of the group and to determine whether the primarily Californian tarweeds are biogeographically isolated from their closest relatives outside Madiinae or are part of a larger, principally western North American lineage. As a result of a phylogenetic analysis of ITS sequence data from representatives of almost all genera of helenioid Heliantheae recognized by Karis and Ryding (1994)
and various representatives of Heliantheae s.s. and Eupatorieae (Baldwin and Wessa, unpublished data), we identified a primarily Californian clade (Madieae sensu Baldwin; see Table 1) including Madiinae that is the focus of the study reported herein.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) and a clade comprising all other representatives of Heliantheae s.l. plus Eupatorieae (Kim and Jansen, 1995
).
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CTAB (hexadecyltrimethylammonium bromide) procedure (adding a phenol extraction, RNase digestion, and two ethanol precipitations) or the method of Palmer (1986)
, without separation of organelles. The ITS region (i.e., ITS-1, 5.8S, ITS-2 nrDNA) was amplified by PCR (polymerase chain reaction) using primers ITS-I (5'-GTCCACTGAACCTTATCATTTAG- 3'; Urbatsch, Baldwin, and Donoghue, 2000
) and ITS4 (White et al., 1990
) in 25-µL reactions as described by Baldwin (1992)
, with equimolar primer concentrations. PCR reaction conditions in a P-E 9600 thermal cycler (Perkin Elmer, Norwalk, Connecticut, USA) included 40 cycles of denaturation at 97°C for 10 sec, primer annealing at 48°C for 30 sec, and primer extension at 72°C, initially for 20 sec (with an increase of 4 sec to each successive extension). Thermal-cycling was followed by a final extension at 72°C for 7 min. PCR products were visualized by agarose gel electrophoresis and purified by filtration using Ultrafree-MC tubes, UFC3 LTK 00 (Millipore, Bedford, Massachusetts, USA). Cycle-sequencing reactions were conducted using the Thermo Sequenase Dye Terminator Cycle Sequencing Kit, US79765 (Amersham Pharmacia Biotech, Piscataway, New Jersey, USA) using the manufacturer's protocol, with half-volume reactions and addition of 5% DMSO (dimethyl sulfoxide). Cycle-sequencing reaction products were purified using Centri-seps columns, CS-901 (Princeton Separations, Adelphia, New Jersey, USA). DNA sequences were resolved on 4.8% polyacrylamide gels [using Page-Plus acrylamide, E562 (Amresco, Inc., Solon, Ohio, USA)] using an ABI 377 automated sequencer (Applied Biosystems, Inc., Foster City, California, USA). DNA sequences were analyzed using ABI Sequence Analysis software and examined using ABI Sequence Navigator software (Applied Biosystems, Inc., Foster City, California, USA). Nucleotide sequences of both DNA strands were compared to ensure accuracy. Amplified copies of the ITS region were cloned [using the TOPO TA cloning kit, K4550-01 (Invitrogen, Carlsbad, California, USA)] for samples of Arnica cernua because of difficulties in obtaining high-quality sequences directly from pooled PCR products. Cloned ITS-region sequences were re-amplified (prior to sequencing) directly from plated, transformed colonies with M13 primers. Cells were lysed at 94°C for 12 min prior to 30 PCR cycles of 94°C for 1 min, 58°C for 1 min, and 72°C for 2 min. PCR was followed by a final extension period (72°C for 7 min).
For a minor proportion of samples, the ITS region was PCR-amplified and sequenced using the methods of Baldwin and Robichaux (1995)
.
We aligned the ITS-region sequences using a manual, iterative process (see Table 2). Groups well supported on the basis of bootstrap and decay values from an analysis of the initial sequence matrix were used to guide subsequent refinement of the alignment. Alignment was optimized within each group prior to reconciliation of alignment among the groups.
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Robustness of our phylogenetic results to alignment uncertainty was examined by parsimony analyses of a sequence matrix with nucleotide states recoded as "N" (any of four nucleotide states) if other similarly likely alignments would have different phylogenetic implications. The foregoing recoding process preserves phylogenetic information in unambiguously aligned taxa (see Bruns et al., 1992
), unlike elimination of entire characters from the analyses. Gaps were treated as missing data in phylogenetic analyses. Inferred indels were recoded as separate, unordered characters except in regions of uncertain alignment (see Table 2).
Parsimony analyses were conducted using a beta-test version of PAUP* 4.0 (b2) (D. L. Swofford, Smithsonian Institution). We attempted to find all minimum-length trees by performing heuristic searches with 100 random addition sequences of the taxa. We estimated reliability of clades by bootstrap and decay analyses, with 20 heuristic searches and random-addition sequences of the taxa for each of the 100 bootstrap replicates and for the decay analyses. Decay of clades with relaxation of parsimony was assessed using the reverse constraints approach as implemented in AutoDecay 4.0 (Eriksson, 1998
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Pairwise distances between ITS sequences
Corrected (HKY85) pairwise ITS-region sequence divergence between members of Arnica and Madiinae ranges from 8.5 to 19.2%. Similar pairwise distances are seen in comparisons between deeply divergent members of Madiinae. ITS-region sequence divergence between members of Achyrachaena, Blepharipappus, Holozonia, Lagophylla, Layia, or Raillardella and members of other Madiinae genera range from 8.5 to 19.8%. Pairwise distances between members of the outgroup (Baeriinae) and ingroup are, on average, considerably higher, ranging from 7.7 to 26.8%.
Results of phylogenetic analyses
Parsimony analysis of the full aligned sequence matrix plus recoded indels yielded 300 maximally parsimonious trees, one of which is shown in Fig. 1. Parsimony analysis of the ITS-region sequence matrix without indels recoded and with all sites of conceivably questionable alignment recoded as missing data yielded 555 maximally parsimonious trees (none shown). Strict consensus trees from the two analyses are topologically congruent, with somewhat less resolution within Madiinae in the consensus of 555 trees.
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, and five smaller groups within the subtribe: (1) Lagophylla minor and L. ramosissima, (2) Carlquistia and Madia sativa, (3) representatives of the three silversword alliance genera (Argyroxiphium, Dubautia, and Wilkesia), (4) Anisocarpus scabridus, Carlquistia, Madia sativa, and silversword alliance representatives, and (5) Hemizonella and Kyhosia. Arnica, with inclusion of Mallotopus and Whitneya, also corresponds to a well-supported clade. Within Arnica, a robust ITS clade unites Arnica mallotopus (= Mallotopus japonicus) with Arnica unalaschcensis. Higher level groupings of special relevance here are the clades uniting (1) Arnica with Madiinae, (2) Eatonella s.s. with Hulsea, (3) Arnica, Eatonella, Hulsea, Venegasia, and Madiinae, and (4) all representatives of Baeriinae exclusive of the x = 19 taxon Constancea (Eriophyllum) nevinii. |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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30 species, was long considered a member of Senecioneae, in part because of its pappus of fine bristles. Nordenstam (1977)
excluded Arnica from Senecioneae upon noting that members of the genus lacked morphological and chemical characteristics common to most members of the tribe and possessed, instead, features in common with or unique to Heliantheae s.l. The position of Arnica in Heliantheae s.l. has been uncertain because members of the genus possess a sesquiterpene lactone chemistry like that of Gaillardiinae s.l., but have carbonized cypselae like those of all taxa of Heliantheae s.l. except Gaillardiinae s.l. (including Marshallia). Karis's (1993b, 1996)
morphology-based cladograms of Asteroideae placed Arnica outside Gaillardiinae in an internally unresolved clade with Madiinae, Eupatorieae, Heliantheae s.s. (including Coreopsidinae), and Pectidinae (= Tageteae).
Circumscription of Arnica
The monotypic, California-endemic Whitneya was long associated with the Gaillardiinae s.l. genera Baileya and Psilostrophe in subtribe Riddeliinae because of persistent ray corollas in the three genera. Upon determining that Arnica and Whitneya share the same base chromosome number (x = 19), Ornduff et al. (1967)
postulated a close relationship of Whitneya to Arnica, an hypothesis supported by Turner and Powell (1977)
and by Nordenstam (1977)
, who stated "(w)ithout any doubt referable to the Arnica group are the related genera Whitneya (n = 19) and Mallotopus (n = 9)." Our data uphold Nordenstam's view, and Whitneya dealbata has recently become Arnica dealbata (Baldwin, 1999
). Mallotopus, a monotype endemic to Japan, is already commonly treated as a species of Arnica, A. mallotopus. The earlier somatic count of 2n = 18 from A. mallotopus contrasts with a count of 2n = 19 II from microsporocytes at diakinesis (Baldwin, unpublished data). Arnica unalaschcensis, strongly united with A. mallotopus in the ITS trees, is also indigenous (but not endemic) to Japan.
Possible shared derived morphological characteristics of Madiinae and Arnica
Unusual morphological characteristics in Heliantheae s.l. that may be synapomorphic for Arnica and Madiinae include association of each phyllary with a ray floret (only outer phyllaries are associated with ray florets in members of Arnica with a biseriate involucre) and a pappus of plumose bristles (lost in Whitneya and putatively modified or lost in various members of Madiinae). Opposite leaves borne distally on the stems, a widespread condition in Heliantheae s.l., may also be apomorphic for the Arnica + Madiinae group, given the alternate or highly condensed phyllotaxy of the closely related genera Eatonella s.s., Hulsea, and Venegasia.
Secondary chemistry and medicinal properties of Madiinae and Arnica
Sesquiterpene lactones, e.g., helenalin, have been implicated as the major active ingredients in anti-inflammatory preparations of Arnica montana and various North American arnicas, e.g., A. chamissonis (Lyss et al., 1997, 1999
). No lactones are reported from Madiinae (or Baeriinae) (Bohlmann, 1990
); extracts from some tarweeds reportedly have been used by indigenous Americans for treatment of rheumatism and gout (Zardini, 1992
; Schmeda-Hirschmann, 1995
). Flavonoids, e.g., quercitin, suggested as minor contributors to medicinal properties of Arnica (Lyss et al., 1999
), are structurally diverse in Madiinae (Crins and Bohm, 1990
). As the sister group of Arnica, Madiinae may be worth investigating for medicinally useful compounds.
Inferences on ancestry of Madiinae and Arnica
The nested phylogenetic position of the tarweed–silversword lineage within a paraphyletic group of ecologically similar taxa (Arnica, Eatonella, Hulsea, and Venegasia) in the ITS tree has surprising implications for ancestral life history and habitat preferences of tarweeds. The vast majority of tarweeds are ephemeral herbs of low-elevation, seasonally xeric sites (with notable exceptions, see below), but on consideration of outgroup relationships we suggest that tarweeds may have descended from a mid- to high-elevation dwelling, perennial ancestor. All species of Arnica and Venegasia are perennials, as are Constancea (Eriophyllum) nevinii and most taxa of Hulsea (other hulseas are facultative perennials or biennials; the monotypic Eatonella is an annual). Arnica and Hulsea are primarily of montane to alpine habitats in temperate western North America or, in some Arnica species, high-latitudinal sites in North America and Eurasia (Eatonella has a broad ecological range, from subalpine woodlands to high desert basins; the monotypic Venegasia is a central- to south-coastal Californian taxon of moist, low-elevation sites—see Turner and Zippin, 1992
).
The predominantly Californian distribution of most taxa in the clade comprising Baeriinae, Madiinae, and the x = 19 "arnicoid" genera leads us to conclude that tarweeds probably originated in the California Floristic Province and are part of a much larger, principally Californian radiation of helenioid Heliantheae. Our novel hypothesis that Arnica originated in far western, temperate North America is in accord with a center of diversity for diploids of Arnica in the Klamath region of northern California and southern Oregon (Wolf, 1980, 1987
; Wolf and Denford, 1984
), but contrasts with Maguire's (1943)
hypothesis of an arctic or subarctic origin of the genus. Based on our ITS results, we conclude that the annual habit and other common characteristics of tarweeds that allow occupancy of the extreme summer-dry habitats of lowland, cismontane California (where most taxa of Madiinae occur) arose following divergence from a common ancestor with the Arnica lineage.
Ancient dysploidy
Chromosomally, the paraphyletic ITS group encompassing Arnica, Eatonella, Hulsea, and Venegasia is uniformly characterized by a base chromosome number of x = 19 (i.e., n = 19 or multiples thereof, with no dysploidy reported), as is Constancea (Eriophyllum) nevinii (see Mooring, 1997
). As noted above, the chromosome number of one member of the group, Arnica mallotopus, has been reported as 2n = 18, but a new count revealed 2n = 19 II (Baldwin, unpublished data). Because the tarweed–silversword lineage is nested in a paraphyletic group of taxa with x = 19, we conclude that the modal chromosome numbers of n = 7 and n = 8 in Madiinae are the results of extensive chromosomal reorganization, i.e., dysploidy. Based on the new perspective provided here, dysploidy has been more pervasive in Madiinae than is already well documented (see Kyhos, Carr, and Baldwin, 1990
). Absence of dysploidy in the closely related x = 19 "arnicoid" taxa is correlated with lack of annuals (except in the monotypic genus Eatonella). The annual habit is widely associated with dysploidy in plants, possibly as a result of selection for reduced recombination (Stebbins, 1950
). Additional studies of gene duplications in Madiinae (Gottlieb, 1987
) are needed to test the hypothesis that extant tarweeds are descendants of a polyploid ancestor, i.e., that the x = 19 condition is the result of paleopolyploidy.
Raillardella and ancestral tarweeds
Raillardella s.s. comes closest, among existing tarweeds, to embodying the set of morphological, ecological, and chromosomal characteristics that we believe may be ancestral to Madiinae on the basis of outgroup comparison. All three species of Raillardella s.s. are perennial, montane herbs with a pappus of well-developed, flattened, plumose bristles (the pappus elements present even on ray cypselae, unlike most other members of Madiinae but like Arnica), and a base chromosome number of x = 17, the highest base number among tarweed–silversword genera. Similarities between Raillardella s.s. and Arnica are sufficiently great that the two genera were closely associated taxonomically, as members of Senecioneae with opposite leaves, in systems of Compositae classification from the time of Bentham (1873)
until Carlquist (1959)
determined that Raillardella s.l. (including Anisocarpus scabridus and Carlquistia muirii) belongs in Madiinae. Members of the two genera have even been confused taxonomically; Raillardella paniculata is a synonym of Arnica viscosa. We are seeking finer level resolution of relationships in Madiinae in hope of determining whether Raillardella is truly a window on the past for understanding the earliest evolutionary history of the spectacular tarweed–silversword radiation.
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FOOTNOTES |
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2 Author for reprint requests ( bbaldwin{at}uclink4.berkeley.edu
).
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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 D. L. Remington and M. D. Purugganan GAI Homologues in the Hawaiian Silversword Alliance (Asteraceae-Madiinae): Molecular Evolution of Growth Regulators in a Rapidly Diversifying Plant Lineage Mol. Biol. Evol., September 1, 2002; 19(9): 1563 - 1574. [Abstract] [Full Text] [PDF]
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R. Chan, B. G. Baldwin, and R. Ornduff Cryptic goldfields: a molecular phylogenetic reinvestigation of Lasthenia californica sensu lato and close relatives (Compositae: Heliantheae sensu lato) Am. J. Botany, July 1, 2002; 89(7): 1103 - 1112. [Abstract] [Full Text] [PDF]
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W. S. Armbruster, C. P. H. Mulder, B. G. Baldwin, S. Kalisz, B. Wessa, and H. Nute Comparative analysis of late floral development and mating-system evolution in tribe Collinsieae (Scrophulariaceae s.l.) Am. J. Botany, January 1, 2002; 89(1): 37 - 49. [Abstract] [Full Text] [PDF]
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J. Lee, B. G. Baldwin, and L. D. Gottlieb Phylogeny of Stephanomeria and related genera (compositae-lactuceae) based on analysis of 18S-26S nuclear rDNA ITS and ETS sequences Am. J. Botany, January 1, 2002; 89(1): 160 - 168. [Abstract] [Full Text] [PDF]
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) indicate clades that collapse in the strict consensus tree. Note: The evident taxonomic problems in Eriophyllum are subjects of the authors' ongoing phylogenetic investigation of Baeriinae, in cooperation with Dale Johnson and John Mooring