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Systematics |
Department of Ecology and Evolutionary Biology and The Natural History Museum and Biodiversity Research Center, University of Kansas, Lawrence, Kansas 66045 USA
Received for publication March 18, 2004. Accepted for publication October 7, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Asteraceae • character evolution • Coreopsis • molecular phylogeny
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Coreopsis was once considered present in Africa, but the African species are now placed in Bidens (Mesfin Tadesse, 1986
) and Coreopsis is now a strictly New World genus. Centers of diversity for Coreopsis are Mexico, the Andes, and eastern North America (Smith, 1975
; Mesfin Tadesse et al., 1995
). The two genera have long been recognized despite the acknowledged difficulty in distinguishing them (e.g., Mesfin Tadesse, 1984
, 1986
, 1993
; Mesfin Tadesse et al., 1995
, 1996
, 2001
). Sherff (1955)
commented that the two genera are "easily distinguishable," yet "cannot be separated definitely by any one character." Phylogenetic analyses of morphological characters in the Coreopsideae were not informative in resolving relationships between the two genera (Ryding and Bremer, 1992
; Karis and Ryding, 1994
; Mesfin Tadesse et al., 2001
), but these and other workers have commented that their results provide little or no support for the monophyly of either genus. Despite the aforementioned problems with delimitation of the genera, morphological characters were used to generate phylogenetic hypotheses for different groups of Coreopsis, using both inexplicit (Smith, 1975
, 1976
, 1982
, 1983
) and explicit methods (Jansen et al., 1987
). Kim et al. (1999)
included species of Coreopsis and Bidens as the ingroup in a phylogenetic study using sequences from the internal transcribed spacer regions of nuclear ribosomal DNA (ITS), and Crawford et al. (2001)
and Kimball and Crawford (2004)
expanded taxon sampling to include most genera of Coreopsideae in an ITS phylogeny. These studies provided strong evidence that neither Bidens nor Coreopsis is monophyletic, but did resolve a number of strongly supported clades within each "genus." One clade receiving strong support in the Kim et al. (1999)
study contained species of Bidens and Coreopsis from temperate North America. Studies with expanded taxon sampling (Crawford et al., 2001
; Kimball and Crawford, 2004
) produced a tree that included five species of the genus Thelesperma (as a strongly supported group) in this north temperate clade, together with Bidens and Coreopsis.
The five sects. (sections) of Coreopsis included in the aforementioned clade with certain Bidens and with Thelesperma include Calliopsis, Coreopsis, Eublepharis, and Gyrophyllum (incorrectly called section Palmatae in prior studies, J. L. Strother, University of California, personal communication). Sherff (1955)
recognized these five sections, and Smith (1975)
generally agreed with Sherff's treatment with the exception of the sectional placement of several species. Smith (1975)
summarized the results of his extensive biosystematic studies showing that species within a section usually exhibit some level of cross compatibility. In contrast, Smith (1975)
was able to obtain intersectional hybrids only between certain members of sects. Calliopsis and Eublepharis. The cladistic analysis of Jansen et al. (1987)
included sections of Coreopsis from California and Mexico in addition to the five eastern North American sections as the ingroup. It is now known that the ingroup is not monophyletic (Kimball and Crawford, 2004
). Jansen et al. (1987)
resolved the five eastern North American sections as a monophyletic group, with each of the sections monophyletic. A later analysis of the Jansen et al. (1987)
data by Kim et al. (1999)
showed low (or no) bootstrap support for most clades. Only sect. Eublepharis and its sister group relationship with sect. Calliopsis enjoyed higher than 70% bootstrap support.
The purposes of the present molecular phylogenetic study were to use expanded taxon sampling and sequences from additional regions compared to earlier studies to provide a more highly resolved and strongly supported phylogeny for the north temperate clade of Coreopsideae than had hitherto been achieved with either morphological or molecular data. Such a phylogeny will provide a refined understanding of relationships among eastern North American Coreopsis and show how these species are related to representatives of the genera Bidens and Thelesperma in this clade (Crawford et al., 2001
; Kimball and Crawford, 2004
). A more fully resolved phylogeny will facilitate an examination of character evolution within the clade in order to evaluate characters that have been employed in taxonomic and phylogenetic studies of Coreopsis and other Coreopsideae (Sherff, 1955
; Smith, 1975
, 1976
, 1982
, 1983
; Mesfin Tadesse, 1984
, 1986
, 1993
; Mesfin Tadesse et al., 1995
, 1996
; Jansen et al., 1987
; Ryding and Bremer, 1992
; Karis and Ryding, 1994
).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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and Kimball and Crawford (2004)
served as the basis for defining the ingroup. In particular, an ITS phylogeny of tribe Coreopsideae provided moderate support (over 70% bootstrap in both parsimony and neighbor-joining trees, and over 95% posterior probability in Bayesian trees) for the clade containing the taxa used as the ingroup. The two species of Bidens used as outgroups are sister to the ingroup in a strongly supported clade (Kimball and Crawford, 2004
). Voucher specimens of Ganders are deposited in the University of British Columbia Herbarium (UBC), specimens collected by Crawford, Crawford and Lewis, Roberts, and Smith are deposited in the Ohio State University Herbarium (OS), Crawford and Giannasi voucher specimens are in the University of Georgia Herbarium (GA), and the Nelson specimen is deposited in the Rocky Mountain Herbarium (RM) of the University of Wyoming (Table 1. See data supplement accompanying the online version of this article).
DNA extraction, amplification, and sequencing
Total DNA was extracted from a small amount (
10 mg) of silica-gel-dried leaf material or from fresh leaves using a modified CTAB method (Mort et al., 2001
). Target DNA regions were amplified via PCR using the primer combinations N-nc18S10/ C26A for ITS (Wen and Zimmer, 1996
), 3914F/psbA-R for matK (Johnson and Soltis, 1994
, 1995
), and F71 (Jordan et al., 1996
) and REx2 (R. T. Kimball, University of Florida, personal communication) for rpl16. Amplicons were purified using QIAquick PCR purification columns (Qiagen, Valencia, California, USA). Automated sequencing was accomplished using a Beckman-Coulter CEQ 8000. We employed cycle sequencing using standard dye terminator cycle sequencing kits (Beckman-Coulter, Fullerton, California, USA) following the manufacturer-supplied protocol, with half-volume reactions. For rpl16, the same primers used for amplification were used for sequencing; sequences of ITS were generated using the primers ITS-1 and ITS-4 (White et al., 1990
). Cycle sequencing of matK employed the primers 1F, 2F, 3F, 1R, 2R, and 3R (Sang et al., 1997
). Cycle sequencing reactions were purified using CleanSEQ (Agencourt Bioscience, Beverly, Massachusetts, USA). All contigs were edited and assembled using Sequencher version 4.1 (GeneCodes, Ann Arbor, Michigan, USA).
Phylogenetic analyses
Alignment of the DNA data was easily accomplished by eye using Se-Al v.1.0 (Rambaut, 1996
); all gap characters ("-") were scored as missing data ("?") and were not included in any of the phylogenetic analyses. Parsimony analyses were conducted using PAUP* with all characters equally weighted (Swofford, 1998
). All data were combined a priori into a single data matrix for parsimony analyses. Initial searches were conducted using 500 replicates of random taxon addition and NNI (nearest neighbor interchange) branch swapping. Each set of shortest trees from these initial searches was used for subsequent analyses employing TBR (tree bisection reconnection) branch swapping. Relative support for the clades recovered was assessed using bootstrap analyses (Felsenstein, 1985
) with 500 replicates, TBR branch swapping, and saving a maximum of 500 trees per replicate.
Morphological character evolution
The selection of morphological characters and the coding of character states were based primarily on data given in Sherff (1955)
, Jansen et al. (1987)
, Ryding and Bremer (1992)
, Karis and Ryding (1994)
, and Mesfin Tadesse et al. (2001)
. Characters were selected from among those used taxonomically and phylogenetically in temperate North American Coreopsis (Smith, 1975
, 1976
; Jansen et al., 1987
). In particular, characters were selected from among those that defined groups or showed complex patterns of evolution in the phylogeny of Jansen et al. (1987)
. The evolution of these features was examined by coding the terminal taxa with each character state. These features were then traced onto the strict consensus topology using MacClade (Maddison and Maddison, 1992
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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A large majority of the ingroup species produce fruits that possess a thin wing; however, this condition is absent in the outgroup, in Bidens, and in several species of Coreopsis. Tracing this feature onto the phylogeny suggests two evolutionary scenarios. The first is that winged fruits have been derived three times (the C. pulchra–C. major clade, the C. floridana– C. gladiata clade, and the C. leavenworthii–C. wrightii clade) with two apparent reversals in C. basalis and C. wrightii. The second scenario is that winged fruits have been derived twice, once in the C. pulchra–C. major clade and once in the C. floridana–C. wrightii clade, with three reversals noted in C. rosea, C. basalis, and C. wrightii (Fig. 2).
Yellow ligules are widespread in the ingroup, but several species possess ligules that have red (sometimes brownish) spots or flecks at the base of the petals, or petals that are entirely rosaceous; the outgroup species, as well as T. megapotamicum, are variable for this trait and thus were coded as polymorphic for analyses in MacClade. These analyses indicate that entirely yellow ligules are basal in the Coreopsis + eastern North American Bidens clade. Furthermore, rosaceous or basally spotted ligules have arisen four separate times in Coreopsis: C. rosea, C. wrightii, C. tinctoria, and the ancestor of the C. nuecensis–C. nuecensoides clade (Fig. 2).
Our analyses indicate that the condition of four-lobed disk florets has either arisen twice (the C. floridana–C. rosea and C. leavenworthii–C. tinctoria clades) or once (C. floridana–C. wrightii clade) with a reversal to five-lobed disk florets in the C. intermedia–C. wrightii clade (Fig. 2).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) nor ITS sequences alone (Kim et al., 1999
) provided support for the monophyly of any section of Coreopsis except sect. Coreopsis. Because prior molecular studies (Crawford et al., 1991
, 2001
; Kim et al., 1999
; Kimball and Crawford, 2004
) focused on higher level relationships, taxon sampling within sections was often inadequate for providing a thorough picture of relationships within sections. Therefore, hypotheses of relationships at the intrasectional level have been formulated primarily from inexplicit methods in which the evolutionary advancement was determined for species based on whether they exhibited "primitive" or "advanced" states for 12–15 mostly morphological characters (Smith, 1982
, 1983
; E. B. Smith, personal communication) or from cladistic analyses of morphological characters (Jansen et al., 1987
). Discussion will be limited to comparing salient similarities and differences in relationships portrayed in the present vs. past studies.
Within the small sect. Calliopsis (three species), the two primarily eastern North American species, C. leavenworthii and C. tinctoria, have been viewed as sister to the northern Mexican species C. paludosa (Smith, 1983
; Jansen et al., 1987
). The monophyly of this section is well supported (84%) by our combined analyses. However, in contrast, the present study provides moderate support (73%) for C. leavenworthii and C. paludosa as sister species (Fig. 1).
Section Coreopsis is the largest in eastern North America with nine recognized species (Smith, 1976
). No prior studies have provided complete resolution of relationships within this section, and this investigation is no exception. Jansen et al. (1987)
showed a tritomy at the base with the four annual species forming one clade, four perennial species in another clade, and C. grandiflora sister to all other taxa. The one consistent difference between molecular and morphological phylogenies is the position of C. wrightii. This species always groups with the other three annual species (C. basalis, C. nuecensoides, and C. nuecensis) in morphological analyses, but in molecular phylogenies (Crawford et al., 1990
; Kim et al., 1999
) C. wrightii is sister to all other members of the section. The present study shows a similar pattern of relationships except there is now strong support (83%) for a clade of C. lanceolata and C. wrightii, which in turn is sister to a strongly supported grouping (92%) of the other species in this section (Fig. 1). No prior studies have suggested that the latter two species are sister taxa, and we have not found any morphological or biosystematic data in support of it. J. L. Strother (University of California, personal communication) is of the view that C. wrightii should be submerged in C. basalis; the present results from combined nuclear and plastid sequences as well as prior molecular data (Crawford et al., 1991
; Kim et al., 1999
) suggest rather that they are in distinct lineages in the section.
The discussion of sect. Eublepharis will include five of the seven species assigned to this section (Smith, 1976
); we were not able to amplify ITS from herbarium material of C. falcata and C. nudata. Smith's (1983)
drawing has C. rosea near the base and Jansen et al. (1987)
place C. rosea (together with C. nudata) as sister to the remaining species of the section. Our results are concordant with earlier studies in placing this distinctive species as a basal element in the section. It shares with C. nudata ligules that vary from orange-yellow to rose, which contrast with the typical yellow ligules found in other Coreopsis. Also, C. rosea, which occurs from Maryland to Nova Scotia, has a more northerly distribution than other species in sect. Eublepharis (Smith, 1976
). The tree of Jansen et al. (1987)
places C. integrifolia sister to the remaining taxa (C. falcata, C. floridana, C. gladiata, C. linifolia) of the section; Smith's (1983)
drawing has it as the most basal species in the section. The three species C. floridana, C. gladiata, and C. linifolia have been viewed as a closely related group (Smith, 1983
; Jansen et al., 1987
). The present results place C. gladiata as sister to a strongly supported clade (96%) containing C. integrifolia and the other two species (Fig. 1). Additional field and laboratory studies are needed to elucidate relationships in this species complex (Smith, 1975
, 1976
, 1983
).
Low resolution and the lack of one species (C. verticillata) in our analyses limit the insights obtained into relationships in sect. Gyrophyllum. One result not seen in prior investigations was the strong sister group relationship (92%) between the rare northern Alabama endemic C. pulchra and the prairie species C. palmata (Fig. 1).
Relationships among sections and genera
The hypothesis of intersectional relationships generated in the present study can only be contrasted with trees or diagrams based on morphology (Smith, 1975
; Jansen et al., 1987
) because prior trees based on cpDNA restriction sites (Crawford et al., 1991
) and ITS sequences (Kim et al., 1999
) were deficient in taxon sampling and were poorly resolved. The relationship of the monospecific sect. Silphidium (C. latifolia) has been problematic. Smith (1975)
considered sect. Silphidium closely related to Coreopsis sect. Electra from Mexico and Central America, rather than a member of the eastern North American group. In contrast, Jansen et al. (1987)
place it basal to the four other eastern North American sections in a strongly supported clade. Both cpDNA (Crawford et al., 1991
) and ITS sequences (Kim et al., 1999
; Kimball and Crawford, 2004
) put C. latifolia in a strongly supported clade with the other eastern North American Coreopsis sections, but do not resolve its relationships within these other sections. The present study provides strong support for sect. Silphidium as sister to a weakly supported sect. Gyrophyllum (<50%; Fig. 1). No synapomorphic morphological or anatomical characters have been identified for these two sections (Jansen et al., 1987
).
This study is the first to document two large strongly supported clades in temperate North America. One of these clades (85%) consists of the aforementioned sects. Silphidium and Gyrophyllum, and representative species of north temperate Bidens sect. Bidens (Fig. 1). Prior phylogenies from ITS sequences (Kim et al., 1999
; Crawford et al., 2001
; Kimball and Crawford, 2004
) included these three sections of the two genera as elements in a strongly supported clade. However, Kim et al. (1999)
failed to resolve relationships among the sections, and the tree produced in the other investigation (Crawford et al., 2001
; Kimball and Crawford, 2004
) place the five representatives of the genus Thelesperma (a strong monophyletic group) sister to Coreopsis in a strongly supported clade. This clade is in turn sister to two species of Bidens sect. Bidens. Thus, the combined data sets employed in the present study provide the most refined hypothesis yet available for relationships between Bidens and Coreopsis in temperate North America. In doing so, our results contrast with prior hypotheses by indicating that the sections of Coreopsis within this clade do not form a monophyletic group (Fig. 1). Our results also suggest that the genus Thelesperma is not sister to a monophyletic Coreopsis, with Bidens then sister to these two genera. Rather, Thelesperma is instead sister to a clade containing Bidens and Coreopsis (Fig. 1). Despite the strong molecular support for a sister group relationship between two sections of Coreopsis and representatives of temperate North American Bidens, neither we nor others (Sherff, 1955
; Mesfin Tadesse et al., 2001
) have yet identified anatomical-morphological characters uniting them.
The other major clade consisting of Coreopsis sects. Calliopsis, Coreopsis, and Eublepharis receives very strong support (100%), with complete resolution of relationships among the sections (Fig. 1). The grouping of sect. Calliopsis with sect. Coreopsis (with weak to moderate support [61%], but present in all shortest trees) rather than with sect. Eublepharis (Fig. 1) contrasts with all prior hypotheses where sects. Calliopsis and Eublepharis are considered more closely related to each other than either is to any other section (Smith, 1975
, 1983
; Jansen et al., 1987
; Kim et al., 1999
). Smith (1983)
discussed the characters, arguing for and against uniting the two sections; the one character that has been used to unite these two sections will be discussed in the next section.
Character evolution
The well-resolved phylogeny obtained in this study provides an opportunity for an analysis of character evolution and for investigating characters that have been used to define groups at various taxonomic levels. Jansen et al. (1987)
suggested two origins for the annual habit in eastern North American Coreopsis, one in the common ancestor of C. basalis, C. nuecensis, C. nuecensoides, and C. wrightii in sect. Coreopsis and another in C. tinctoria of sect. Calliopsis. Crawford et al. (1990
, 1992
), based on cpDNA restriction site data, discussed the possibility that there have been two rather than a single origin of the annual habit in sect. Coreopsis because C. wrightii did not occur in the same lineage as the other three annual species. There was, however, less than compelling evidence for these relationships because of the few mutations supporting the grouping of the annual species. The present study provides strong support for two origins of the annual habit in sect. Coreopsis (Fig. 2).
Opposite leaves are found in the vast majority of Coreopsis species (Sherff, 1936
) and the species of temperate North America are no exception (Sherff, 1955
; Smith, 1976
). Alternate leaves are clearly the derived condition, and they occur in only two sections of the eastern clade: C. floridana, C. linifolia, and C. gladiata of sect. Eublepharis, and C. paludosa of sect. Calliopsis. There are two equally parsimonious reconstructions for the evolution of alterntate leaves. Either alternate leaves have evolved twice with a reversal in C. integrifolia, or there have been three separate origins of this condition (Fig. 2). It is notable that leaf arrangement is so variable among closely related species in sect. Eublepharis, yet it is nearly constant throughout much of temperate North American Coreopsis and, indeed, in the entire genus.
One of the characters used by Sherff (1955)
in separating Bidens and Coreopsis in his generic key was winged fruits in the latter genus as opposed to non-winged in the former, although there was the qualification that "most species" of Coreopsis have winged fruits. Jansen et al. (1987)
mentioned winged fruits as one of the characters showing repeated parallelisms and reversals. The present results show the complexity of winged fruit evolution in the temperate North American clade with two equally parsimonious scenarios. First, there could have been three derivations (C. pulchra–C. major clade, C. floridana–C. gladiata clade, and C. leavenworthii–C. wrightii clade) with two reversals, one in C. basalis, and another in C. wrightii (Fig. 2). A second equally parsimonious reconstruction hypothesizes two origins for winged fruits (C. pulchra–C. major clade and the C. floridana–C. wrightii clade), with reversals in the three species C. rosea, C. basalis and C. wrightii. Particularly interesting is that both scenarios indicate reversals in C. basalis, and C. wrightii because the loss of wings has been used as a diagnostic character uniting the two species as sister taxa (Jansen et al., 1987
). Despite the taxonomic importance that has been assigned to the winged fruit condition, it is not unexpected that the character is somewhat labile given that it has been demonstrated to be under very simple genetic control in Coreopsis tinctoria (Smith and Parker, 1971
).
In optimizing the evolution of ligule color, we have followed the coding of Jansen et al. (1987)
with yellow as one state, and under the other character state were lumped ligules that are not totally yellow. Species coded as having the latter character state include four taxa with red flecks or spots at the base (C. basalis, C. nuecensis, C. nuecensoides, C. tinctoria, and C. wrightii and one species (C. rosea) with ligules that are entirely rosaceous. If all "non-yellow" ligules are treated as the same state, then there have been four separate origins of the "non-yellow" condition in Coreopsis (Fig. 2). It may be more realistic, however, to treat the basal red flecking or spotting as a different character state than totally rosaceous ligules. If this were done, there would be a single origin of the latter condition in C. rosea (the other species of this section with rosaceous ligules, C. nudata, was not included in this study so it remains an open question as to whether the condition originated once or twice in sect. Eublepharis) (Fig. 2). The condition of basal flecks or spots has originated three times, and especially noteworthy is its parallel origin in the common ancestor of the C. basalis-C. nuecensis-C. nuecensoides clade and in C. wrightii (Fig. 2). The red flecks or spots have been used as diagnostic characters (together with the annual habit) for a clade consisting of C. basalis, C. nuecensis, C. nuecensoides, and C. wrightii (Smith, 1982
; Jansen et al., 1987
), but our results are not congruent with this interpretation and suggest that the character is more labile than previously thought (Fig. 2). The lability of the spotting or flecking character is not surprising because it has been shown to be variable within species, and segregation of the character in the F2 generation of C. nuecensis hybrids indicates that it is controlled by a single locus (with some variation in penetrance) with lack of spotting the recessive condition (Smith, 1974
, 1976
).
The character that has been used to diagnose sects. Calliopsis and Eublepharis is the four-lobed disk corolla, a feature otherwise unknown in Coreopsis (Smith, 1972
). The phylogeny generated in this study suggests that, rather than the four-lobed condition having arisen once in the common ancestor of the two sections, either there have been independent origins of the four-lobed condition in the two sections, or there has been one origin with reversal to five lobes in sect. Coreopsis (Fig. 2).
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Crawford D. J. J. D. Palmer M. Kobayashi 1990 Chloroplast DNA restriction site variation and the phylogeny of Coreospsis section Coreopsis (Asteraceae). American Journal of Botany 77: 552-558[CrossRef][ISI]
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Mort M. E. D. E. Soltis P. S. Soltis J. Francisco Ortega A. Santos Guerra 2001 Phylogenetic relationships and evolution of Crassulaceae inferred from matK sequence data. American Journal of Botany 88: 76-91
Rambaut A. 1996 Sequence alignment editor (Se-Al 1.0 a1). University of Oxford, Oxford, UK
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