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Systematics |
Department of Biological Sciences, University of Wisconsin–Milwaukee, Milwaukee, Wisconsin 53201 USA
Received for publication April 1, 2003. Accepted for publication August 19, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: biogeography • Caltha • diplophylly • Gondwanaland • molecular systematics • phylogeny • Ranunculaceae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Hill, 1918
). In any case, diplophylly is a highly variable character within the genus and has been utilized in both species delimitation and intrageneric classification.
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).
The first comprehensive taxonomic treatment of the genus was that of de Candolle (1818)
, in which he recognized two sections. Section Psychrophila in the Southern Hemisphere was characterized as having a persistent calyx, leafless solitary inflorescences, and sagittate basal leaves with upturned auricles. Section Populago in the Northern Hemisphere was characterized as having a deciduous calyx, leafy stems, and cordate or reniform leaves lacking upturned auricles. Subsequent authors (Huth, 1892
; Smit, 1973
) maintained these two sections, but with considerable variation in composition. In the most recent revision of the genus, 10 species are recognized (Smit, 1973
): four in the Northern Hemisphere (section Caltha) and six in the Southern Hemisphere (section Psychrophila).
Caltha palustris, the most widespread species, has a circumboreal distribution across much of Europe, Asia, and North America. This species displays a considerable amount of morphological variation, prompting the recognition of many segregate taxa. However, most of this morphological diversity has been shown to be the result of environmental conditions, and there is little support for many of the previously recognized segregates (Smit, 1967
, 1968
, 1973
; Woodell and Kootin-Sanwu, 1971
). Caltha natans, unique because of its floating or creeping aquatic habit, also has a distribution on multiple continents (northwestern North America and northeastern Asia) but is relatively invariable morphologically and has not been divided into segregate taxa.
The two remaining northern species have relatively broad distributions, but on single continents: C. scaposa is distributed throughout the Himalayas and C. leptosepala is distributed in mountainous regions of western North America. The latter presents a unique problem. In the southern portion of the species range, two distinct taxa are clearly present: plants in California have leaves that are wider than long, two flowers per inflorescence, and pantoporate pollen grains whereas plants in Colorado have leaves that are longer than wide, solitary flowers, and tricolpate pollen grains. However, in the northern portion of the species range, the two forms are indistinguishable. In the past, these taxa have been recognized as distinct species, but are currently recognized as merely subspecies (Smit, 1973
) or not at all (Ford, 1997
).
Three species of Caltha are endemic to South America. Of these, C. sagittata has the broadest distribution (primarily in the southern Andes, but with several disjunct northern populations) and the most morphological variation. The two other South American endemics (C. appendiculata and C. dionaeifolia) have more restricted distributions in the southernmost regions of the continent. An additional two species are endemic to New Zealand: C. novae-zelandiae found on both the North and South Islands and C. obtusa found only on the South Island. A single species, C. introloba, is endemic to the alpine regions of Australia and Tasmania.
Aside from the division of the genus into two sections, the evolutionary relationships within Caltha have not been formally addressed. For this reason, past notions regarding the evolution of diplophylly or the events responsible for the current distribution of the genus have been somewhat speculative. This phylogenetic study has the following objectives: (1) determine the phylogenetic relationships among the 10 species, (2) test the monophyly of sections Psychrophila and Caltha, (3) provide limited insight into species delimitation within C. palustris, C. leptosepala, and C. sagittata, (4) determine the evolutionary history of diplophylly and other morphological characters within the genus, and (5) explore explanations for the current geographical distribution of the genus, in hopes that this information will provide insight into the biogeographical histories of other related and unrelated taxa.
DNA sequence data from the chloroplast atpB-rbcL intergenic spacer (atpB-rbcL spacer), the chloroplast trnL intron/trnL-trnF intergenic spacer (trnL-F region), and the internal transcribed spacers of nuclear ribosomal DNA (ITS regions) were used to reconstruct the phylogeny of the genus. Each of these regions is either noncoding or includes a noncoding component and is thus more variable and more useful at lower taxonomic levels.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Three samples of C. palustris covering the geographical range of the species, two samples of C. sagittata, and both subspecies of C. leptosepala were included. Because of their putative affinities with Caltha (Hoot, 1995
; Johansson, 1995
), Trollius, Helleborus, and two species of Callianthemum were included as outgroups to root the tree. Species sampled, their geographical sources, voucher information, and GenBank accession numbers are listed in the Appendix (see Supplemental Data accompanying the online version of this article).
DNA extraction and amplification
Total DNA was extracted from either fresh, silica-dried, or herbarium leaf material for each sample. When sufficient amounts of material were present, the DNA was extracted using the procedure of Doyle and Doyle (1987)
. When limited amounts of leaf material were available, DNeasy columns (Qiagen, Valencia, California, USA) were utilized according to the manufacturer's protocol. If necessary, DNA was further purified using DNeasy columns. For each of the samples, the atpB-rbcL spacer, trnL-F region, and ITS regions were separately amplified using the polymerase chain reaction (PCR). Amplifications of the nuclear ITS regions were carried out using primers 1830F (located in the 18S gene) and 25R (located in the 26S gene), originally designed by Nickrent et al. (1994)
. The PCR protocol was as described in Schuettpelz et al. (2002)
. When amplifications using this program were not successful, the annealing temperature was lowered to 34°C.
Amplification protocols for the two chloroplast regions differed from one another only in the primers used. Amplifications for the trnL-F region were carried out using primers A50272 (located in the trnF gene) and B49317 (located in the trnL gene: 5' exon), originally designed by Taberlet et al. (1991)
. Amplifications for the atpB-rbcL spacer were carried out using primers S385R (located in the atpB gene) and RBCL1R (located in the rbcL gene), as in Hoot et al. (1995)
. Reaction mixtures and cycling parameters were as in Hoot et al. (1995)
, differing only in MgCl2 concentration (3.0 mmol/L), number of cycles (30), and annealing temperature (45°C). When amplifications using this program were not successful, the annealing temperature was lowered to 40°C.
All PCR products were purified using one of two methods: (1) the PCR products were separated from impurities on a low-melt agarose gel, excised from the gel as a plug, and separated from the agarose and concentrated using Wizard Columns (Promega, Madison, Wisconsin, USA) according to the manufacturer's protocol; or (2) the PCR products were separated from impurities and concentrated using QIAquick Spin Columns (Qiagen) according to the manufacturer's protocol.
DNA sequencing
Sequence reactions were carried out in both directions for each purified double-stranded PCR product using Dye Terminator Cycle Sequencing or Big Dye Terminator Cycle Sequencing reagent (Applied Biosystems, Foster City, California, USA) and primers identical to those utilized in PCR, according to the manufacturer's protocol. In the case of the atpB-rbcL spacer, one of two sequencing primers, S2R (Hoot et al., 1995
) or S85R (sequence available from S. Hoot), was often substituted for the amplification primer (S385R).
Alignment
The sequences obtained as chromatograms for each sample were aligned, providing complete or nearly complete sequence overlap. Ambiguous bases were corrected and consensus sequences created using the computer program Sequencher 4.1 (Gene Codes, Ann Arbor, Michigan, USA). All consensus sequences for a given region were aligned manually using MacClade 4.01 (Maddison and Maddison, 2001
). Alignment procedures were as described in Hoot and Douglas (1998)
, paying careful attention to repeated motifs (Type Ib indels) and runs of the same nucleotide (Type Ia indels). Because of the presence of many indels, homology was at times difficult to assess. In such instances, the regions of ambiguous alignment were excluded from the analyses, as were portions of the alignment containing large amounts of missing data. Indels were not scored for inclusion in the analyses, but were mapped on the resulting topologies (Table 3).
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). Models of sequence evolution were selected using a top-down approach (i.e., starting with the most complex model and moving towards models of decreasing complexity) and a topology generated through equally weighted parsimony analysis (1000 random addition sequence replicates, TBR branch swapping, and MULTREES in effect). For each nested comparison, parameters were estimated using PAUP 4.0b10 (Swofford, 2002
), and the resulting likelihoods were compared using the likelihood ratio test. The B/MCMC analyses were conducted using the selected model of evolution (with flat priors) and four chains (one cool and three heated). Chains were allowed to run for 1 x 106 generations, and trees were sampled from the cool chain every 100 generations. Following completion, sampled trees were plotted against their likelihood in order to recognize the point where the likelihoods converged on a maximum value, and all trees prior to this convergence were discarded as the "burn-in" phase. The remaining trees were combined in a majority rule consensus. The consensus trees resulting from each of the three analyses (with posterior probabilities) were then compared visually for conflict supported by a posterior probability 
0.95.
The three data sets were then combined and analyzed in unison. Searches for optimal trees used three methods: equally weighted parsimony, unequally weighted parsimony, and maximum likelihood. For the unequally weighted parsimony analysis, a symmetrical step matrix was obtained using STMatrix (F. Lutzoni and S. Zoller, Duke University), which determines the frequency of possible character state changes a priori from the data and converts these frequencies to costs with the negative natural logarithm (Felsenstein, 1981
; Wheeler, 1990
; Miadlikowska et al., 2002
). The resulting step matrix was implemented across all sites. For the maximum likelihood analysis, the appropriate model of sequence evolution was selected using the top-down approach as described. All searches were implemented in PAUP* 4.0b10 with 1000 random addition sequence replicates, TBR branch swapping, MULTREES in effect, and gaps treated as missing data. Various outgroup combinations were tested for their effect on the ingroup topology.
Branch support was assessed using maximum likelihood bootstrapping (Felsenstein, 1985
) and B/MCMC analysis. The maximum likelihood bootstrap analysis, implemented in PAUP* 4.0b10 using the model selected for the original data set, consisted of 1000 replicates, each with 10 random addition sequence replicates, TBR branch swapping, and MULTREES in effect. The B/MCMC analysis of the combined data set was conducted using three models (one for each molecular marker, as determined above), flat priors, and four chains. Chains were allowed to run for 1 x 106 generations, and trees were sampled every 100 generations. Following completion, the burn-in trees were discarded and the remaining trees were combined in a majority rule consensus, to determine the posterior probability of each node.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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0.95). None of the remaining nodes received posterior probability support greater than 0.81. The analysis of the atpB-rbcL spacer provided significant support for only six nodes, with the remaining nodes receiving 
0.76 posterior probability (Fig. 1B). The analysis of the trnL-F region recovered nine nodes with significant support, and in this case, the remaining nodes all received posterior probability support 0.65 (Fig. 1C). No significant conflict was detected among the three resulting topologies, and the data sets were combined.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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0.95) for at most 10 nodes (ITS data). When these data were combined, 11 nodes received posterior probability support of 1.00 (Fig. 2). This is not surprising, as nonconflicting data sets often provide more support and resolution when combined (Bremer et al., 1999
; Hahn, 2002
; Matheny et al., 2002
). In the topology resulting from the combined analysis, only one trichotomy is present (species from Australia and New Zealand), and only two resolved nodes receive poor support (the node that resolves C. leptosepala as paraphyletic and the node at the base of two populations of C. palustris). These superior levels of resolution and support allow one to draw conclusions from the phylogeny with reasonable confidence.
Caltha natans was resolved as the earliest branching species. This is surprising based on its presumably derived aquatic habit but is supported by its relatively low chromosome number (n = 16; Hoffmann, 1999
). Among the remaining species, C. scaposa is resolved as sister to the widespread C. palustris. Although the scapose habit of C. scaposa suggests an affinity to the Southern Hemisphere species, the presence of broadly obovate sepals suggests affinities with either C. natans or C. palustris (Fig. 3). Indel data (Table 3) further support the sister-group relationship of C. scaposa and C. palustris. Caltha leptosepala (although potentially paraphyletic) is resolved as sister to the Southern Hemisphere species. This relationship is supported by a common chromosome number (n = 24; Hoffmann, 1999
), the presence of oblong sepals, and indel data (Fig. 3; Table 3).
The Southern Hemisphere species have always been recognized as a natural group based on the presence of diplophyllous leaves, and the results of this study strongly support (PP = 1.00; BS = 92) this relationship (Fig. 2). Caltha sagittata, with the broadest distribution in the Southern Hemisphere and relatively simple diplophylly (Fig. 3), is resolved as basal. Caltha dionaeifolia and C. appendiculata, both from South America, are resolved as sister species. They both have highly modified and divergent leaf morphologies (Fig. 3). The species from Australia and New Zealand also form a well-supported, and geographically consistent, clade (PP = 1.00; BS = 97).
Sectional classification
Of the two sections of Caltha previously recognized, only section Psychrophila is monophyletic. The species of section Caltha form a paraphyletic grade (Fig. 2). For this reason, it is necessary to revise the previous classifications of the genus. Three phylogenetically sound, informal groupings are suggested (Fig. 2). The Natans group (C. natans) has an aquatic creeping habit and small (
1 cm diameter) flowers with obovate white sepals; the Caltha group (C. palustris and C. scaposa) has a generally upright habit and larger (>2 cm diameter) flowers with obovate sepals; and the Psychrophila group (C. leptosepala, C. sagittata, C. dionaeifolia, C. appendiculata, C. introloba, C. obtusa, and C. novae-zelandiae) has a generally scapose habit, oblong sepals (more than twice as long as wide), and mostly diplophyllous leaves (Fig. 3).
Subspecific taxa
The three geographically disparate samples of C. palustris included in this study are, on a molecular level, quite distinct from other species and are united by several substitutions and a three base-pair indel (Fig. 2; Table 3). However, within this extremely polymorphic and widespread species, there is relatively little variation, supporting Smit's (1973)
recognition of one species (rather than the numerous segregates that had been proposed previously).
On the other hand, the two populations of C. sagittata included in this study are relatively divergent from each other on a molecular level, despite their geographical proximity. Such differentiation could indicate the presence of additional species as Hill (1918)
suggested, but further study at a more detailed level is required.
The results based on the inclusion of both subspecies of C. leptosepala are inconclusive but intriguing. The two populations sampled here (from Colorado and Oregon) are quite distinct on a molecular level and are actually resolved as paraphyletic. This result, although poorly supported (PP = 0.65; BS = 52), is contradictory to the three indels that support the monophyly of the species (Table 3). These results illustrate the problematic nature of these taxa, which are morphologically distinct in the southern portion of their geographical range, but indistinguishable in the northern portion. A more detailed molecular study examining many individuals across western North America is needed.
Evolution of diplophylly and other morphological features
Because the diplophyllous species are resolved as monophyletic, it is quite reasonable to believe that this trait evolved only once within the genus (Fig. 3). However, it is interesting and important to note that the basal lobes of the other species of Caltha often show tendencies toward an upturned morphology, especially in their younger leaves (Troll, 1932
; E. Schuettpelz and S. B. Hoot, personal observations). In any case, it is clear that the earliest form of this character is represented by inflexed lobes and that appendages that cover the entire lamina or that rise from the lamina itself are more derived (Fig. 3).
Most other morphological features of the genus appear to be homoplastic, including some that were previously used for intrageneric and intraspecific classification. A scapose habit has evolved three times (Fig. 3), pantoporate pollen twice (Fig. 3), and sepal color has toggled between white and yellow numerous times. Aside from strongly diplophyllous leaves, the only character that appears to be uniquely derived and not subsequently lost is the presence of oblong (greater than twice as long as wide) sepals (Fig. 3).
Biogeography
The results of this study reveal that the Northern Hemisphere species of Caltha are paraphyletic to a strongly supported Southern Hemisphere clade, indicating that the origin and early differentiation of the genus most likely occurred in the Northern Hemisphere. Because the North American species, C. leptosepala, is sister to the Southern Hemisphere clade and the first-branching member of the Southern Hemisphere clade is a South American species (C. sagittata; Fig. 2), it is most probable that dispersal from the Northern to Southern Hemisphere occurred between North and South America. Based on our results, this was followed by later movement from South America to Australia and New Zealand. The primary biogeographical questions within the genus center on the timing of and the mechanisms involved in these two events: the movement of Caltha from the Northern Hemisphere to the Southern Hemisphere and the spread of Caltha throughout the Southern Hemisphere. It is interesting to note that another genus in the Ranunculaceae (Anemone) poses similar biogeographical questions (Schuettpelz et al., 2002
).
In addressing these questions, it is necessary to consider the dispersal strategies of the genus as well as its probable age. The fruits of Caltha are small, unspecialized follicles, making long-distance wind or animal dispersal unlikely. Therefore, scenarios involving repeated short-distance dispersals should be favored. There is no reliable fossil record for the Ranunculaceae. However, Ranunculales is one of the earliest branching eudicot clades (Hoot et al., 1999
; Soltis et al., 2000
). Given that eudicot pollen has been documented from around the Barremian-Aptian boundary of the Lower Cretaceous (approximately 125 mya; Crane et al., 1995
) and that angiosperms underwent a rapid diversification by the mid-Cretaceous (Crane et al., 1995
; Magallon et al., 1999
), an origin of Caltha by the mid-Cretaceous is possible.
The relative positions of North and South America have not changed substantially since the Cretaceous (Scotese, 2001
). However, the geology of the Caribbean region and Central America during this time is complicated and not well understood. It seems likely that a separate small tectonic plate, the Caribbean plate, formed between North and South America, producing chains of volcanic islands at its eastern and western margins (Cox and Moore, 2000
). This, together with a climactic cooling trend and lower sea levels during the late Cretaceous/early Paleocene, may have produced a land link similar to (if not identical with) the present day Panama Isthmus (Hallam, 1992
; Briggs, 1994
; Cox and Moore, 2000
). This scenario is consistent with the distributions of many terrestrial fossil vertebrates, the separation of marine bivalves, and the relatively old age of the Central American biota (Briggs, 1994
) and is also congruent with the movement of Caltha from North to South America indicated by our phylogeny (Fig. 2).
The Southern Hemisphere distribution of Caltha can be best explained by invoking a vicariance model. Under such a model, the ancestor of the Southern Hemisphere species (excluding C. sagittata) would have moved across Gondwanaland when the various austral landmasses were relatively contiguous (as late as the Middle Eocene; Scotese, 2001
) and diverged following the breakup. This model is supported by similar links found within other ranuculacean genera (e.g., Anemone; Schuettpelz et al., 2002
) and within other lower eudicot families (e.g., Proteaceae; Hoot and Douglas, 1998
).
In summary, based on our phylogeny, it seems most probable that Caltha originated in the Northern Hemisphere, moved from North to South America along a land bridge during the late Cretaceous or early Paleocene (ca. 65 mya), and moved from South America to New Zealand and Australia via Antarctica by the middle Eocene (ca. 49 mya). These movements, and their timing, will be further evaluated in future biogeographical studies of ranunculacean genera.
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FOOTNOTES |
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2 Present address: Department of Biology, Duke University, Durham, North Carolina 27708 USA (ejs7{at}duke.edu
)
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LITERATURE CITED |
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