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Systematics |
2Universität Osnabrück, Fachbereich Biologie, Spezielle Botanik, Barbarastrasse 11, 49069 Osnabrück, Germany; and 3Section of Plant Biology, University of California Davis, Davis, California 95616 USA
Received for publication December 12, 2000. Accepted for publication June 12, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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3 bp (base pairs) provided reliable phylogenetic information whereas indels 
2 bp, probably originating from slipped-strand mispairing, are prone to parallelism in the context of our phylogenetic framework. For the first time, an hypothesis of the genus Lepidium is proposed based on molecular phylogeny, in contrast to previous classification schemes into sections and greges (the latter category represents groups of related species within a given geographic region), which are based mainly on fruit characters. Only a few of the taxa as delimited in the traditional systems represent monophyletic lineages. The proposed phylogeny would suggest three main lineages, corresponding to (1) sections Lepia and Cardaria, (2) grex Monoplocoidea from Australia, and (3) remaining taxa, representing the bulk of Lepidium species with more or less resolved sublineages that sometimes represent geographical correspondence. The fossil data, easily dispersible mucilaginous seeds, widespread autogamous breeding systems, and low levels of sequence divergence between species from different continents or islands suggest a rapid radiation of Lepidium by long-distance dispersal in the Pliocene/Pleistocene. As a consequence of climatic changes in this geological epoch, arid/semiarid areas were established, providing favorable conditions for the radiation of Lepidium by which the genus attained its worldwide distribution.
Key Words: biogeography • Brassicaceae • chloroplast DNA • Lepidium • phylogenetics • trnT-trnL spacer • trnL intron • trnL-trnF spacer
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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175 species. It is distributed wordwide, primarily in temperate and subtropical regions; the genus is poorly represented in Arctic climates, and in tropical areas it grows in the mountains. Lepidium is characterized by angustiseptate, dehiscent, usually notched fruits; a single pendulous, usually copiously mucilaginous seed in each locule; strongly keeled valves; and tooth-like nectar glands (Al-Shehbaz, 1986b
). Reduction in floral organ number is common within the genus Lepidium, and over half of the species have only two or four stamens, rather than the usual six. Petals are reportedly absent from about one quarter of the Lepidium species, and they are rudimentary in many others (Al-Shehbaz, 1986b
; Endress, 1992
; Bowman and Smyth, 1998
; Bowman et al., 1999
). Thus, in the majority of species, the flowers are reduced in size and scentless, promoting widespread autogamy in the genus (Al-Shehbaz, 1986b
). Chromosome numbers are known for 50 species, of which all except five have x = 8 and nearly half of which are polyploid (Al-Shehbaz, 1986b
; Brüggemann, 2000
). Polyploidy may be the outcome of hybridization, as was suggested by Hitchcock (1936, 1945a, b)
and Howell (1934)
, but has not been documented experimentally (Al-Shehbaz, 1986b
).
Lepidium is well known for its infrageneric difficulty (Marais, 1970
; Latowski, 1982
; Schultze-Motel, 1986
), and in the monograph of the genus, Thellung (1906)
found only a few diagnostic characters for infrageneric grouping. Thellung summarized earlier classifications and proposed a revised one for sections and subsections. The three minor sections, Lepia (Desv.) DC. (six species, one with a number of subspecies), Lepiocardamon Thell. (two species), and Cardamon DC. (one species) are native to Europe, the Mediterranean area, the Near East, and southwestern Asia (Thellung, 1906
; Al-Shehbaz, 1986b
). The position of Cardaria (Desv.) DC. is a matter of controversy; it was classified by Thellung (1906)
and Latowski (1982)
as a section of Lepidium, whereas others (Rollins, 1940
; Mulligan and Frankton, 1962
; Al-Shehbaz, 1986b
) treated Cardaria as a separate genus, based mainly on its indehiscent fruits. Remaining taxa represent a large critical species complex of >100 species, i.e., section Nasturtioides (Medik.) Thell. Apparently, Thellung (1906)
was in doubt as to the further subdivision of this assemblage because of a lack of reliable characters. Notwithstanding his doubt, Thellung subdivided species of section Nasturtioides, based on slight differences in fruit shape, into subsections Dileptium (Raf.) Thell., Monoploca (Bunge) Thell., and Lepidiastrum (DC.) Thell., which were later elevated to the rank of sections, i.e., Dileptium (Raf.) DC., Monoploca (Bunge) Prantl, and Lepidium L. (Hewson, 1981
). In detail, Thellung classified the species of section Nasturtioides within a priori defined geographic regions, i.e., (1) Eurasia and Africa, (2) North and South America, and (3) Australasia and the Pacific region, respectively, into subsections Dileptium, Monoploca, and Lepidiastrum. Furthermore, he proposed another classification system using a category called grex, which is outside the formal ranks of botanical nomenclature (Hewson, 1981
). Greges were regarded by Thellung as groups of related species within the geographic regions. Although greges should be subordinated to the sections, their spectrum of morphological variation does not coincide with that defined for the sections (Thellung, 1906
; Hewson, 1981
). It seems that subsection Dileptium contains grex Ruderalia, Virginica, Oxycarpa, Bipinnatifida, and parts of greges Pseudo-Ruderalia and Oleracea. Subsection Monoploca comprises grex Monoplocoidea, Alyssoidea, Gelida, and parts of grex Oleracea, whereas subsection Lepidiastrum are attributed some species of Pseudo-Ruderalia and Oleracea. Greges Papillosa and Neozelandica were not assigned to any section (Table 1). In addition, many of the species in the critical species complex (among them all species from Africa) were apparently not assignable to any of the greges (Thellung 1906
; Table 1).
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; Mummenhoff, Hurka, and Bandelt, 1992
; and below for the Australian species), the general concept may be criticized on the following bases. First, Thellung's system is based on a single character (fruit shape) and thus represents a largely artificial concept (Jonsell, 1975
). Second, the classification of the critical species complex into geographic elements of the respective subsections based on their distribution by continents is apparently an a priori procedure. Therefore, differences (if any) or conclusions on phylogenetic relationships between taxa from different geographic areas (continents) remain obscure (Ryves, 1977
). Third, classification of species of the critical species complex into greges is outside the formal ranks of botanical nomenclature and phylogenetic relationships of the greges are unsettled (Hewson, 1981
; Mummenhoff, Hurka, and Bandelt, 1992
).
Recent morphological/anatomical studies were confined to selected geographical regions. Based upon differences in fruit and seed anatomy, Latowski (1982)
subdivided Lepidium into three subgenera: Cardaria, Lepia, and Lepidium. This study suffers from the poor taxon coverage because only 16 species (restricted to Europe and Asia) were analyzed. In a revision of the genus Lepidium in Australia (Hewson, 1981
) using fruit and flower structure, greges Monoplocoidea and Pseudo-Ruderalia were suggested to represent sections Monoploca and Dileptium, respectively, whereas greges Oleracea and Papillosa were elevated to sectional rank (Table 1).
Our recent molecular studies in Thlaspi clearly indicate convergence in fruit characters (fruit shape) previously used for subdivision in sections (Mummenhoff and Koch, 1994
; Mummenhoff, Franzke, and Koch, 1997b
). Fruit shape is also the key character in subgeneric classification of Lepidium, and the reliance on such characters can easily suggest misleading phylogenetic concepts. Therefore, we have started molecular work in Lepidium using isoelectric focusing analysis of RUBISCO, restriction site analysis of chloroplast DNA and ITS sequence analysis. In the initial studies, we focused on the minor sections from the Old World (Lepia, Lepiocardamon, Cardamon, Cardaria) and on selected issues (e.g., evolutionary changes in floral structure). These analyses indicate that (1) Cardaria draba and taxa of section Lepia seem to be closely related based on the same IEF polypeptide pattern (Mummenhoff, 1995
), (2) section Lepia should be recognized and section Lepiocardamon (one of two species studied) should be amalgamated with monotypic section Cardamon (Mummenhoff et al., 1995
), and (3) floral structure within Lepidium is relatively fluid and at least two independent reductions to the two stamen condition and at least one reversal to flowers with increased organ numbers are likely to have occurred (Bowman et al., 1999
).
As outlined above, phylogenetic relationships within Lepidium are still unsettled and continue to be disputed. Although our previous molecular work on selected taxa and issues has shed light on single aspects of evolution in Lepidium, the current study is the first comprehensive phylogenetic analysis on a worldwide basis. We are studying data from the nuclear (ITS regions) and chloroplast genomes. These data sets will be analyzed separately and in conjunction with each other. In the current study, we are reporting the results of our cpDNA study. We have analyzed three noncoding regions from the chloroplast (cp) genome of 73 species/subspecies of all seven sections and 11 out of the 12 greges of Thellung's fundamental monograph (Thellung, 1906
), to elucidate phylogenetic relationships and to improve our understanding of possible past dispersal patterns of this cosmopolitan genus.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Thus, our taxon sampling represents the full range of variation in Lepidium and the entire geographic distribution of the genus on all continents. Sources of plant material are given in the Appendix (provided at http://ajbsupp.botany.org/v88/mummenhoff.pdf).
Because Lepidium may not clearly be separated from the closely related genera Coronopus Zinn, Winklera Regel, and Stroganowia Karelin & Kirilow (Zunk, 1994
; Zunk, Mummenhoff, and Hurka, 1999
; Brüggemann, 2000
), we selected three taxa of tribe Lepidieae as more remote outgroup species, i.e., Pritzelago alpina (L.) Kuntze, Hymenolobus procumbens (L.) Nuttal, and Hornungia petraea (L.) Reichenbach. In a recent cpDNA restriction site analysis (Zunk, 1994
; Zunk, Mummenhoff, and Hurka, 1999
) these species are sister to the Lepidium/Coronopus clade. Voucher specimens are deposited in the herbarium of the Botany Department of the University of Osnabrück (OSBU).
DNA isolation, PCR amplification, and sequencing
Genomic DNAs were isolated from fresh material and herbarium specimens. Fresh leaves were harvested from plants grown from seeds in the greenhouse at Osnabrück University. The CTAB technique of Doyle and Doyle (1987)
was used with some modifications (Mummenhoff, Franzke, and Koch, 1997 a, b
). Primers a, b, c, d, e, and f of Taberlet et al. (1991)
were used for double stranded DNA amplification of the trnT/trnL spacer, the trnL intron, and the trnL/trnF spacer, hereafter referred to as T/L spacer, intron, and L/F spacer, respectively (Fig. 1). Successful PCR (polymerase chain reactions) resulted in a single band in a minigel. The PCR amplification and purification of the three PCR products was conducted as described by Mummenhoff, Franzke, and Koch (1997a)
. Purified PCR products were sequenced following the protocol given in Mummenhoff, Franzke, and Koch (1997a)
using the three forward (a, c, e) and reverse (b, d, f) primers of Taberlet et al. (1991)
.
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). In the core data matrix, insertion/deletion positions (indels) were treated as missing, but indels were recoded as additional binary characters, as suggested by Wojciechowski et al. (1993)
.
Previous analyses of these cpDNA regions clearly suggest that indels longer than 2 base pairs (bp) are not prone to parallelism and thus may provide important phylogenetic information whereas homoplasy in indel distribution is almost completely accounted for by indels of 1 or 2 bp (van Ham et al., 1994
; Bayer and Starr, 1998
). Therefore we recoded only indels of 3 bp and longer for phylogenetic analysis.
Sequence data were analyzed using PAUP 4.0b3 (Swofford, 2000
). Phylogenetic reconstruction was performed using heuristic searches with 20 random addition sequences and TBR (tree bisection reconnection) swapping to search for alternative islands of most parsimonious trees (Maddison, 1991
; all analyses found a single island). Strict consensus trees were constructed for multiple parsimonious trees. The consistency index (CI) and the retention index (RI) are presented to estimate the amount of homoplasy in the characters and clade robustness was analyzed using the bootstrap method (Felsenstein, 1985
) with heuristic search settings and 100 replicates.
Estimates of divergence time
To estimate divergence times among the Lepidium lineages we used information from Rorippa (Brassicaceae) fossil data as suggested by Koch, Haubold, and Mitchell-Olds (2000)
. In a recent study of nuclear ITS (Mitchell and Heenan, 2000
) and cpDNA L/F spacer and trnL intron sequence variation in Cardamine L. (Brassicaceae) and related genera, Rorippa Scop. was found to be a sister to the Cardamine/Nasturtium R. Br. clade (Franzke et al., 1998
). Assuming correct dating of Rorippa fruit fossils, i.e., 2.5–5 million years ago (mya) (Mai, 1995
), the roughly 5% divergence observed between Cardamine and Rorippa noncoding cpDNA (Franzke et al., 1998
) might then correspond to a maximum of 5 mya as a rough estimate for divergence time between Rorippa and Cardamine, contingent upon the assumption of rate constancy.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; van Ham et al., 1994
; Cros et al., 1998
; Franzke et al., 1998
). They are located in the large single copy region of the cp genome, i.e., the intergenic spacer between the trnT gene and trnL 5' exon, the trnL intron, and the intergenic spacer between the trnL 3' exon and the trnF gene (see Taberlet et al., 1991
; Fig. 1). The length of the T/L spacer, the L/F spacer, and the trnL intron in the species under study varies between 761 and 810 bp, 491 and 541 bp, and 268 and 1000 bp (e.g., in L. sativum), respectively (Table 2). For six species (L. campestre, L. flavum, L. perfoliatum, L. sativum, L. spinosum, and L. villarsii) overlapping sequencing of the L/F spacer could not be achieved due to extreme length of the spacer. In these cases, total spacer length was estimated by comparison of the PCR amplification products with a DNA length standard on agarose gels.
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270 and 250 bp from primer a and b, respectively, caused premature termination of sequencing reactions in most species under study. We have been able to overcome this sequencing problem in some species, and for these the T/L spacer length are reported. Because of the sequencing problem in poly A/T stretches in most of the species studied, the alignment contains only those regions sequenced for all taxa.
Sequences of the three noncoding regions were aligned easily by hand despite the introduction of 19 + 44 indels of 1–129 bp in length (Table 2). However, the 3' region of the L/F spacer could not be aligned unambiguously, apparently due to multiple insertion/deletion (indel) events, which probably caused the dramatic differences in spacer length (Table 2). Recently, it was shown that trnL/F regions of approximately the same size in widely divergent species (Sedum, Nicotiana, Zea; van Ham et al., 1994
) and even in individuals of the same species (Rorippa, Brassicaceae; Bleeker, 2000
) may exhibit underlying, nonhomologous patterns of indels at the sequence level. Furthermore, we detected three, one, and two regions of polynucleotide stretches in the intron and spacer regions, respectively (Table 2), which probably originated via replication slippage (Levinson and Gutman, 1987
), and these regions have also not been included in the alignment.
After eliminating regions with ambiguous alignment, 652, 519, and 350 positions from the T/L spacer, the intron, and the L/F spacer, respectively, were available for phylogenetic analysis. The alignment is available upon request. Overall, 1521 characters (nucleotides) were sampled, yielding 356 variable positions of which 170 (11.2%) were phylogenetically informative, and 186 sites (12.2%) were autapomorphic. The mean transition/transversion ratio (ts:tv) across the cpDNA sequences was 1 : 2.5, 1 : 1.4, and 1 : 2 for the T/L spacer, intron, and L/F spacer, respectively, and averaged over all regions was 1 : 2 (Table 2).
In the context of our phylogeny (Fig. 2), 20 out of the 22 parsimony informative indels >3 bp (Table 2) changed only once (i.e., had a CI of 1); 17 of these were in the two spacers and 5 were in the intron (Table 2). All of the 11 phylogenetically informative indels of 1or 2 bp in length required more than one step to explain their distribution over the phylogenetic tree. As we have outlined above, only indels of 3 bp and longer have been included in the phylogenetic analyses. Averaged over the three noncoding regions, mean Jukes-Cantor pairwise sequence distances (gaps treated as missing data; Small et al., 1998
) between Lepidium species are greater for the spacers than for the intron (Table 2).
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Phylogenetic reconstruction
Figure 2 presents the strict consensus of 50 000 most parsimonious trees of 550 steps each produced by the cpDNA data set. This tree divides Lepidium into three major clades, I through III. Bootstrap proportions of >75% (Hillis and Bull, 1993
) strongly support this grouping. Internal branching among the three main clades in the most parsimonious trees (data not shown) is weakly supported by synapomorphic character changes and the branching pattern is inconsistent, resulting in a basal trichotomy in the strict consensus tree. Thus, relationships between these groups remain unclear. Clade I corresponds to the Australian representatives of section Monoploca (grex Monoplocoidea sensu Thellung, 1906
), hereafter referred to as Monoploca sensu stricto (s.s.) (Fig. 2). The second clade (clade II) includes two well-supported monophyletic groups, sections Lepia and Cardaria, and will be referred hereafter as Lepia sensu lato (s.l.). Lepidium perfoliatum (subsection Lepidiastrum sensu Thellung) is sister to Lepia/Cardaria. Taxa of this clade are distributed in the Mediterranean area, Europe, and Asia. Clade III comprises, with some more or less resolved sublineages, the bulk of Lepidium species, representing all continents, nine out of the ten greges studied (Monoplocoidea excluded) and, with the exception of Lepia/Cardaria, all sections sensu Thellung (1906)
and Table 1. This lineage, therefore, largely corresponds to the critical species complex (Fig. 2). We refer to this clade hereafter as Lepidium s.s. Within this clade, some strong and moderately supported sublineages may be found, but most of the sublineages are weakly supported by the cpDNA data. However, section Cardamon may be recognized with the inclusion of L. spinosum from section Lepiocardamon. Lepidium aucheri, the second representative of section Lepiocardamon, originates from a basal polytomy and two Asian species, L. ruderale and L. pinnatifidum, are found as sister to remaining taxa of Lepidium s.s. Some sublineages correspond to geographical regions. For example, clades of species from Australia/New Zealand, South Africa, South America, and two clades of species from North America (one of which contains species from Hawaii along with species from western North America) are distinct monophyletic groups. Other species of Asian/European distribution originate either singly (L. aucheri, L. latifolium, L. apetalum) from the basal polytomy of clade III or as species pairs (L. alluaudii/L. armoracia; L. ferganense/L. lyratum) from polytomous node IV within clade III. With the exception of grex Oxycarpa (L. nitidum included), it appears that none of the greges, sections, and subsections as delimited by Thellung correspond to lineages found in our molecular tree.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Böhle, Hilgert, and Martin, 1996
; Gielly et al., 1996
; McDade and Moody, 1999
) in that the intron shows overall least variability among the regions investigated (Table 2). This observation suggests that the intron is under stronger selection than the spacers, possibly due to its catalytic properties (Gielly and Taberlet, 1994
). The observed transition/transversion ratio of 1 : 2 averaged across all three cpDNA regions in Lepidium (Table 2) is equivalent to those recently reported in Gossypium (Small et al., 1998
). However, there are also reports in which the substitution process is widely biased in favor of transition events in noncoding cpDNA (Zurawski and Clegg, 1987
; Cros et al., 1998
) and thus a general rule cannot be deduced. Recent observations that indels occur at a rate equal to that for nucleotide substitutions in noncoding cpDNA (Golenberg et al., 1993
; Gielly and Taberlet, 1994
) are not supported by our data (Table 2). As in comparable studies (Bayer and Starr, 1998
; Small et al., 1998
; McDade and Moody, 1999
) we detected a pronounced higher rate of substitutions than indels. It has already been outlined above that indels 2 bp should be eliminated from phylogenetic analysis because they are prone to parallelism (van Ham et al., 1994
; Bayer and Starr, 1998
).
In the context of our phylogenic tree (Fig. 2) only 2 out of the 22 potentially phylogenetically informative indels 3 bp required more than one step to explain their distribution on the tree, i.e., they had a CI of 1. In contrast, all of the 11 parsimony informative indels 2 bp were homoplasious. Highly homoplastic indels 2 bp appear as unreliable characters for construction of evolutionary relationships and probably originated by slipped-strand mispairing (Levinson and Gutman, 1987
; van Ham et al., 1994
).
Estimates of divergence times
Estimates of rate and time in molecular analyses are problematic, because they rely on the assumption of a molecular clock and on correct dating of fossil records (Sanderson, 1998
). Notwithstanding these inherent uncertainties, estimations of divergence times using the molecular clock hypothesis have been useful in the study of plant evolution and biogeography (e.g., Böhle, Hilger, and Martin, 1996
; Sang, Crawford, and Stuessy, 1997
). Using independent fossil dates and different genes from the nuclear, chloroplast, and mitochondrial genome, Yang et al. (1999)
and Koch, Haubold, and Mitchell-Olds (2000)
obtained similar estimates of evolutionary timescale in the Brassicaceae. These similar estimates from independent analyses suggest that our estimates of sequence divergence rates of roughly 1% per million years (my) for the noncoding cpDNA under study (relying on the fossil data also used by Koch, Haubold, and Mitchell-Olds, 2000
) are reasonable (see MATERIALS AND METHODS).
Monophyly of Lepidium s.l
Relative to the preliminary taxon coverage considered in our previous analyses, Lepidium formed a natural monophyletic assemblage, although few of the sections and greges sensu Thellung (1906)
and Hewson (1981)
represent monophyletic groups (Mummenhoff, Hurka, and Bandelt, 1992
; Mummenhoff et al., 1995
; Bowman et al., 1999
). A matter of controversy is the position of Cardaria, classified by Thellung (1906)
and Rich (1991)
as a section of Lepidium, whereas others (e.g., Schulz, 1936
; Rollins, 1940
; Al-Shehbaz, 1986b
; Ball, 1993
) treated it as a separate genus or as subgenus (Latowski, 1982
). Fruits of Cardaria are indehiscent, inflated, wingless, and entire at the apex, whereas those of Lepidium are dehiscent, not inflated, strongly compressed contrary to the septum (resulting in a small septum), always keeled, often winged, and usually emarginate at the apex (Al-Shehbaz, 1986b
). Schulz (1936)
even separated C. pubescens (C.A. Meyer) Jarmolenko from Cardaria as Hymenophysa pubescens C.A. Meyer, based on its subglobose fruits with a broad septum, relative to the small septum typical of Cardaria. Schulz (1936)
not only recognized both genera but also placed Cardaria in tribe Lepidieae (subtribe Lepidiinae) and Hymenophysa in tribe Euclidieae. The present study is in full agreement with our preliminary isoelectric focusing analysis of RUBISCO (Mummenhoff, 1995
), suggesting that Cardaria is closely related to Lepidium section Lepia.
There are numerous examples in the Brassicaceae where emphasis on single fruit characters in traditional analyses result in misleading phylogenies (Mummenhoff, Franzke, and Koch, 1997a, b
and references therein). Recent molecular analyses in Brassicaceae demonstrated that species of different genera with widely different fruit types are closely related (Price, Palmer, and Al-Shehbaz, 1994
; Zunk et al., 1996
; Galloway, Malmberg, and Price, 1998
; Zunk, Mummenhoff, and Hurka, 1999
; Koch, Haubold, and Mitchell-Olds, 2000
). On the other hand, our recent molecular studies suggested that the same fruit type in Thlaspi s.l. (e.g., fruits with prominent horns at apex) is distributed among different clades, thus indicating convergence in fruit characters (Mummenhoff, Franzke, and Koch, 1997b
). The present study supports this view. The primary differences in fruit type between Cardaria (fruit indehiscent) and Lepidium (fruit dehiscent) may result from the mutations of single major morphogenetic genes, leading to profound differences in morphology not accompanied by adequate change of the molecular marker (Kadereit, 1994
and references therein). Recent molecular work supports our conclusion. The change from dehiscent to indehiscent fruits in Arabidopsis mutants seems to be under control of solely two MADS-box genes, i.e., SHP1 and SHP2 (Liljegren et al., 2000
).
Interestingly, the indehiscent fruit type typical of Cardaria apparently also occurs in L. heterophyllum var. alatostylum (Thellung, 1906
). Therefore, the common ancestor of Cardaria and Lepia could have been characterized by indehiscent fruits and the species of section Lepia evolved dehiscence. Alternatively, indehiscent fruits evolved independently from dehiscent fruits in Cardaria and C. heterophyllum var. alatostylum. It comes as a surprise to see L. perfoliatum in clade II along with Lepia and Cardaria. This species is characterized by two unique traits: yellow flowers and leaves strongly dimorphic. The basal leaves are long-petiolate, 2- to 3-pinnatifid, and the upper cauline leaves are entire, with the broad lobes enclosing the stem (Ball, 1993
). Lepidium perfoliatum was tentatively included by Thellung in sect. Nasturtioides subsect. Lepidiastrum, although he described it as morphologically intermediate among subsections Monoploca, Dileptium, and Lepidiastrum. There are, however, some morphological characters that also support the common ancestry of L. perfoliatum, Cardaria, and Lepia. With the exception of C. draba, whose subspecies are polyploids with 2n = 32, 64 (subsp. draba) and 2n = 48, 64, 80 (subsp. chalepense), remaining taxa of this clade are diploids with 2n = 16 (Brüggemann, 2000
and references therein). All taxa are characterized by auriculate and amplexicaul cauline leaves (Ball, 1993
), the same seed coat type (Cernohorsky, 1947
), complete flowers with 2 + 4 stamens (indicating allogamy) (Thellung, 1906
; Al-Shehbaz, 1986b
), and all taxa are native in the Old World (the Mediterranean area, Europe, and southwest and central Asia). Low cpDNA sequence divergence among taxa of section Lepia (0.9% mean) correlated well with previous analyses and morphological data (Mummenhoff et al., 1995
) indicating that taxa of section Lepia are closely related and most likely have diversified recently.
Species of clade I (Monoploca s.s.) correspond to grex Monoplocoidea sensu Thellung (1906)
. These species appear to be neither closely related to the other Lepidiums native to Australia/New Zealand nor are they closely related to North American representatives of subsection Monoploca (grex Alyssoidea), which are both found as separate sublineages in clade III (Lepidium s.s.). Therefore, subsection Monoploca as traditionally described by Thellung (silicula broadly winged, style long and exsert, not connate with the wing) is apparently not monophyletic. Species of Monoploca s.s. have the largest flowers (with 2 + 4 stamens) and fruits in the genus Lepidium; they evolved shrub growth habit in contrast to the herbaceous habit more typical of Lepidium. These shrubs demonstrate a range of apparent xeromorphic characters, well-adapted to the dry regions of Australia (Hewson, 1981
).
Seeds of Lepidium typically have incumbent arrangement of the cotyledons (notorrhizal). However, in three species of Monoploca (e.g., L. linifolium), Hewson (1981)
described the cotyledons as extended in length and folded in a diplecolobous manner (twice transversely folded). Based upon folding of cotyledons, Hewson (1981)
defined two subsections within Monoploca s.s., i.e., Diploploca (e.g., L. linifolium) and Monoploca. We do not find evidence for further subdividing Monoploca, as the species analyzed (L. linifolium of subsection Diploploca included) form an unresolved polytomy. This may indicate that mutation rates in the marker system used do not appear high enough to provide sufficient information (Small et al., 1998
). However, pairwise differences among species of Monoploca (1.2–2%) are relatively high in comparison to a maximum of 2.2% within Lepidium s.s., which suggests that informative characters should not be lacking. Inspection of a number of equally parsimonious trees clearly demonstrates the internal nodes within Monoploca s.s. are only weakly supported by a maximum of seven character changes, whereas most changes (63) occur in the terminal branches.
In view of both obvious differences in morphology (Hewson, 1981
) and high molecular divergence, we suggest early and rapid radiation followed by a long period of independent evolution of present-day species. Hewson (1981)
tentatively discussed possible recognition of this lineage as a separate genus, but she concluded that it is not sufficiently distinct. In a previous treatment, Bunge (1845)
advocated generic rank for Australian Lepidium species representing grex Monoplocoidea. Desveaux (1814)
circumscribed representatives of section Lepia (e.g., L. campestre), monotypic section Cardamon (L. sativum), and Australian taxa of grex Monoplocoida (e.g., L. linifolium) as genus Lepia, whereas remaining species of Lepidum were distributed among the genera Cardaria and Lepidium. The latter genus included present-day subsections Dileptium and Lepidiastrum sensu Thellung. Interestingly, representatives of Lepia and Monoploca as delimited in our tree are characterized by perennial habit and complete flowers, which represent the ancestral condition in floral ground plan in Lepidium (Bowman et al., 1999
) and probably indicate an allogamous breeding system (Thellung, 1906
). Our molecular data do not allow definite conclusions about phylogenetic relationships between Lepia s.l. and Monoploca s.s. because both lineages and Lepidium s.s. originate from a basal trichotomy.
Pairwise sequence divergence between these three main lineages range between 2.1 and 4.2% and are thus in an order of magnitude recently documented in intergeneric analyses of Brassicaceae, e.g., between Rorippa Scop. and Nasturtium R. Br. (Franzke et al., 1998
). However, any conclusion about the separate generic status of Lepia s.l. and Monoploca s.s. respectively, relative to Lepidium s.s., should await the inclusion of closely related genera in the analysis, e.g., Andrzeiowskia Reichenbach, Coronopus Zinn, Stroganowia Kar. et Kir., Stubendorffia Schrenk, and Winklera Regel. (Thellung, 1906
). Interestingly, the South African endemic genus Heliophila L. (73 species) is characterized by diplecolobous cotyledons, otherwise found in the Brassicaceae in only three species of Monoploca s.s. (see above) (Appel and Al-Shehbaz, 1997
). Preliminary sequence analysis of Heliophila coronopifolia and H. amplexicaulis spacer sequences indicates an unexpectedly close relationship between Australian Monoploca s.s. and South African Heliophila. This, however, has to be corroborated by further analysis of Heliophila species.
Intrageneric classification
Based upon the fundamental work of Thellung (1906)
, Hewson (1981)
discussed hypothetical evolutionary lines and subgeneric classification. Following her ideas, we suggest that the three minor sections (Lepia, Lepiocardamon, and Cardaria) represent an evolutionary lineage, separated from the other sections (the critical species complex sensu Thellung) on the basis of style fusion to the wing of the fruit. Fruits of subsection Lepidiastrum are not winged, whereas the remaining subsections, Monoploca and Dileptium, have winged fruits, but the wing is not connate with the style. The present study clearly demonstrates that Lepia, Lepiocardamon, and Cardamon apparently do not form a monophyletic group. Instead, Lepia (Cardaria included) represents a monophyletic assemblage, whereas section Cardamon (L. sativum, L. spinescens), along with L. spinosum (section Lepiocardamon), appears to be a monophyletic lineage (clade XII) within Lepidium s.s. (clade III), well separated from Lepia. Lepidium aucheri, the second member of sect. Lepiocardamon sensu Thellung (1906)
is not included in that group, but phylogenetic relationships of this species remain obscure.
Clade III (Lepidium s.s.) represents the critical species complex sensu Thellung (section Nasturtioides), excepting grex Monoplocoidea and L. perfoliatum. As already outlined above, species of section Cardamon and Lepiocardamon are also found here. Inspection of clade III indicates that none of the sections and greges as traditionally defined are monophyletic. However, one may recognize sublineages corresponding to geographic regions, irrespective of their classification to the traditionally defined sections, subsections, and greges (e.g., species from South Africa, Australia/New Zealand, South America, or western North America/Hawaii). These groups may be the basis for further taxonomic considerations and they will be discussed in the context of biogeography.
Biogeography: general considerations
Previous authors (Thellung, 1906
; Bush, 1939
) speculated that Lepidium is an ancient genus that then may have reached its worldwide distribution with the fragmentation of Laurasia and Gondwana in Late Cretaceous/mid-Tertiary. The fossil pollen record (Muller, 1981
), the easy dispersability of seeds (intercontinental dispersal of mucilaginous seeds adhering to birds; Carlquist, 1983
; Mummenhoff, Hurka, and Bandelt, 1992
), and the easy naturalization of recent Lepidium taxa (Al-Shehbaz, 1986a, b
) do not support this view. Furthermore, the maximum observed cpDNA sequence divergence among the primary Lepidium lineages ranged between 2.1 and 4.2% thus estimating the time of divergence of the main lineages roughly at 2.1–4.2 my. These levels of divergence are not consistent with Cretaceous/Tertiary vicariance. Instead, all these considerations argue in favor of long-distance dispersal in a more recent geological epoch (Pliocene, Pleistocene) by which Lepidium attained its worldwide distribution (Meusel, Jäger, and Weinert, 1965
).
Following the basic ideas of Hedge (1976)
, the origin of Lepidium and of the Brassicaceae as a whole occurred in a region encompassing the Mediterranean to the Irano-Turanian territory (Thellung, 1906
). This region is extremely diverse ecologically, altitudinally, and geologically. Most of the variability attributed to Lepidium taxa (except Monoploca sensu Thellung) is found in this region along with closely related genera, e.g., Andrzeiowskia, Stroganowia, Stubendorffia, and Winklera (Thellung, 1906
). Primarily, Lepidium is a genus of arid areas and of the mountains (Thellung, 1906
). Some species have left their typical habitats and colonized human-influenced habitats, and they have been dispersed as weeds by human activities throughout the world, e.g., L. ruderale, L. virginicum, L. africanum, and Cardaria draba (Thellung, 1906
). Mostly diploid Lepia s.l. seems to represent a basal lineage in Lepidium s.l., and the species are restricted to the presumed area of origin, whereas species from the critical species complex (clade III) with a high incidence of polyploidy have far wider ranges of geographic distribution.
Strictly Australian species of Monoploca s.s. are neither related to any other Australian Lepidium species nor are they related to North American members of subsection Monoploca as defined by Thellung (grex Alyssoidea) (Fig. 2). Certainly Monoploca s.s. represents an independent (earlier) introduction to Australia, in comparison to remaining Australian species (H. Hewson, Centre for Plant Biodiversity Research, Canberra, personal communication). Related genera of Monoploca s.s. are not known, although our preliminary data would suggest closer relationships with South African endemic Heliophila. Southwestern Australia has a Mediterranean-like climate similar to that of the Cape Region and may have provided the right environment for the evolution of the diversity in Monoploca s.s. (H. Hewson, personal communication). Interestingly, Heliophila pusilla L. is naturalized in southwestern Australia (Hewson, 1981
). To further explore the nearest relatives of Monoploca and the origin of this taxon in Australia, our current analyses include related genera of Lepidium (e.g., Coronopus, Stroganowia) and representatives of Heliophila and will be reported elsewhere.
Lepidium s.s. comprises species of all continents. Most of the extant species with reduced floral structures are characterized by an autogamous breeding system and are often polyploid, both of which are typical features of colonizing plants (Al-Shehbaz, 1986b
; Mummenhoff, Hurka, and Bandelt, 1992
; Bowman et al., 1999
). Species of this type are typically found among Lepidium s.s. (Thellung, 1906
; Al-Shehbaz, 1986b
). Assuming the area of origin to be in Eurasia, one might speculate that ancestors of such plants started to colonize new areas. In our phylogeny, Eurasian species are found as sister to the remaining Lepidium s.s. species (e.g., L. ruderale, L. pinnatifidum), originate from the basal polytomy (e.g., L. aucheri, L. apetalum), or are found basal to external nodes (e.g., L. ferganense/L. lyratum). Eurasian species are never found in derived positions of the clades. One might therefore suggest that ancestors of such Eurasian species represent the genetic stock from which the different sublineages may then have evolved.
The lack of resolution within Lepidium s.s. might reflect a rapid radiation into the lineages of the different continents. The 0–2.2% divergence observed between species of Lepidium s.s. might correspond to about a maximum of 2.2 my as a rough estimate for divergence time between these species. The corresponding geological period (Pliocene/Pleistocene) provided favorable conditions for the dispersal of species of Lepidium. As a consequence of climatic change, closed forests started to open up and arid/semiarid areas were established in western North and South America, South Africa, and Australia (Mummenhoff, Hurka, and Bandelt, 1992
; Cox and Moore, 1993
and references therein). Therefore, it is not surprising to find in these regions centers of diversification of Lepidium (Thellung, 1906
; Jonsell, 1975
; Hewson, 1981
; Rollins, 1993
) and the preadaptation to these arid/semiarid regions may have taken place in Eurasia.
Wolfson (1948)
suggested that the origin of migration of birds correlated with the dramatic climate change in Pliocene/Pleistocene. Since intercontinental dispersal of Lepidium is likely attributable to transport of mucilaginous seeds by birds (see above), one might speculate that the rapid radiation of Lepidium to different continents correlates with the migration patterns of birds.
Africa
Jonsell (1975)
suggested that central and South African Lepidium species (L. capense, L. schinzii, etc., clade VI) are closely related; this is corroborated by our cpDNA data. Although L. armoracia is distributed in the Yemen, Ethiopia, and, disjunct from these localities, in upland Kenya, Jonsell (1975)
argued that this species is closely related to chiefly Mediterranean L. graminifolium (not studied here). He finally concluded that L. armoracia belongs to a Mediterranean element, probably closely related to L. lyratum/L. ferganense (clade VII) from southwestern and central Asia (Jonsell, 1975
). Lepidium alluaudii is endemic to the Great Atlas mountains in Morocco, its nearest relative, L. myriophyllum, is from South Africa. Although not fully resolved, our tree is generally consistent with this view.
We would tentatively conclude that the ancestors of L. ferganense/L. lyratum from southwest Asia have entered the African continent. Lepidium alluaudii and L. armoracia might then represent North or northwestern African derivations of this colonization event, whereas South Africa was reached by the well-known East African route (Hedge, 1976
). Central African endemic upland Lepidium species described by Jonsell (1975; species not available) may represent relics of the migration to South Africa. Levels of divergence between L. lyratum/L. ferganense (Asia) and the African species range from 0.8 to 1.6%. Using the 1% nucleotide divergence per million years (see above), the disjunction between the two Asian and the most divergent African species would not exceed 1.6 my. This estimate dates the disjunction after the late Pliocene (2.5 mya) when the Sahara desert was well established (Potts and Behrensmeyer, 1992
). Our estimate of this divergence time thus suggests that this disjunction is probably due to long-distance dispersal.
North and South America
With the exception of L. virginicum (widely distributed in North America and central America, adventive in other continents), most other North American Lepidium species under study are native to the western states, particularly California (Thellung, 1906
; Rollins, 1993
). This region is suggested to represent a center of diversification in North America of Lepidium and the Brassicaceae as a whole (Thellung, 1906
; Rollins, 1993
). Some species are also native to Mexico, e.g., L. oblongum, L. lasiocarpum (Rollins, 1993
). Based on the cpDNA tree, North American Lepidium species exhibit relationships to Asian species. Clade VIII comprises Lepidium species from Hawaii and species from western North America (e.g., L. montanum, L. fremontii, clade XI) and these taxa seem to have their closest relatives outside North America in L. ferganense/L. lyratum from Asia.
Species of the other North American clade (L. dictyotum, L. latipes, L. nitidum, L. oxycarpum) are also native to the Pacific states of the United States, particularly California, and in Mexico. Except L. nitidum, this lineage corresponds to grex Oxycarpa, but these taxa are apparently not closely related to the other North American clade and may thus represent an independent immigration event. Closest relatives of these North American species may not easily be recognized, since the cpDNA tree is not fully resolved. The nearest relatives of the Californian species are not found in North America; instead Asian species (e.g., L. apetalum, L. latifolium) are found at the basal polytomy, suggesting that Asia is the cradle of the genus from where the other continents have been colonized. An immigration via the former Bering land bridge might be speculated as was suggested by Rollins (1982)
for a number of western North American Brassicaceae genera, among them Stroganowia, a genus closely related to Lepidium (Rollins, 1982
), which may be congeneric with Lepidium (Thellung, 1906
). Mean sequence divergence between Asian L. lyratum/L. ferganense and North American species of Lepidium of clade VIII (1.1%) and between the other Asian Lepidium species (e.g., L. apetalum) and the Californian clade XI (1%) might roughly correspond to a maximum of 1.1 my of divergence time between these taxa, respectively.
The Beringian land bridge allowed exchange of temperate plants between East Asia and western North America until late Tertiary or Quaternary (Wolfe, 1980
; Tiffney, 1985
; Colinvaux, 1996
). Thus, immigration of Lepidium species in Quaternary times is compatible with our estimates of divergence times, perhaps via long-distance dispersal by birds migrating along this corridor to North America. Lepidium is not found in high latitudes either in northeastern Asia near the former land bridge or in northwest North America. Rather, Lepidium species of southwest and central Asian origin as well as western North American species are typical of arid areas (Thellung, 1906
; Rollins, 1993
). Thus, it is not surprising that ancestral Lepidium taxa have not persisted in the intervening area, i.e., in the high northern latitudes.
Four out of the 34 Lepidium species native to South America have been studied. Based on this limited sample, these species form a monophyletic group (clade X). Since our molecular tree is not sufficiently resolved, phylogenetic relationships of South American species and implications about their origin cannot be inferred without the danger of ambiguity. However, biogeographical evidence at hand supports a western North American origin, probably from ancestors of clade XI (e.g., L. nitidum, L. latipes). Thellung (1906)
reported close relationships between species from California (e.g., L. nitidum, L. pubescens) and Chile (L. chilense, L. subvaginatum). Carlquist (1967, 1983)
and Vargas, Baldwin, and Constance (1998)
suggested these amphitropical disjunctions in Lepidium and many other temperate herbs to be the outcome of long-distance dispersal from western North America by birds, probably in the Pleistocene. The observed mean sequence divergence between South American species and relevant species from western North America is 1.0%, thus estimating the time of divergence at roughly 1 mya, which agrees with Carlquist's (1983)
and Vargas, Baldwin, and Constance's (1998)
data analyses.
The dispersal of Lepidium throughout the Americas must have been very rapid because we have estimated roughly the same time of divergence between Asian and western North American species on the one hand and between the latter species and South American taxa (see above) on the other. Alternatively, South American species may not be the consequence of immigration from California by long-distance dispersal but might represent an independent dispersal event, a scenario not supported by any data.
Hawaiian archipelago
Lepidium species of Hawaii and the Pacific Islands have been classified by Thellung into grex Oleracea, along with four species from New Zealand (Table 1; Fig. 2). The latter species grouped within a clade consisting exclusively of Australian and New Zealand species, whereas the three Hawaiian species are well nested as a monophyletic group within a lineage of species that are confined to western North America (Fig. 2, clade VIII; varieties of L. lasiocarpum and L. oblongum are restricted to Baja California and to the islands off the Californian coast [Rollins, 1993
]).
Weedy annual and herbaceous Lepidium species (e.g., L. virginicum, L. oblongum, L. bonariense) recently introduced into Hawaii are markedly different from the species native to the Hawaiian Islands (L. bidentatum, L. serra, L. arbuscula), which are shrubs or subshrubs (Rollins, 1986
). Based on comparative floristics, Fosberg (1948)
hypothesized that most natural introductions of Hawaiian angiosperms arrived from southeastern Asian source regions and only a minority (18%) of ancestral Hawaiian plant colonizers came from North and South America. This has been attributed to prevailing air currents, presence of stepping stone islands, and climatic similarities between Hawaii and southeastern Asia (Vargas, Baldwin, and Constance, 1998
). The volcanic history and extreme geographic isolation demonstrate that plant life in the islands must have arrived by long-distance dispersal (Wagner and Funk, 1995
). It was hypothesized that native Hawaiian Lepidium species all derived from the indigenous L. bidentatum, i.e., they are monophyletic (Rollins, 1986
; Wagner, Herbst, and Sohmer, 1990
), but where the ancestors of this species came from was not discussed. Carlquist (1967)
suggested a minimum of two successful introductions are needed to account for the native Lepidium species now resident, and he hypothesized colonization from the Americas. Members of the genus Lepidium typically have mucilaginous seeds, which upon becoming wet are dispersed for long distances by adhering to birds (Carlquist, 1967, 1983
; Mummenhoff, Hurka, and Bandelt, 1992
; and references therein).
The low resolution of our cpDNA marker does not permit us to conclude whether L. bidentatum provided the genetic stock from which the other native Hawaiian species, i.e., L. serra and L. arbuscula, may have originated. But our molecular data clearly demonstrate support for the common descent of the three native Hawaiian Lepidium species from western North American (probably Californian) herbaceous ancestors. Our data are in agreement with recent molecular analyses in the Asteraceae (Baldwin et al., 1991
) and Apiaceae (Vargas, Baldwin, and Constance, 1998
) which also provide unequivocal examples of dispersals from western North America to Hawaii. Mean cpDNA sequence divergence between endemic species of Hawaii and closest relatives from western North America (e.g., L. oblongum, L. lasiocarpum) is 0.35%, yielding an age of 350 000 yr for the Hawaiian clade. Our estimate is in agreement with the ITS analysis of Vargas, Baldwin, and Constance (1998)
, who indicate a Pleistocene origin of Sanicula in Hawaii. Further insights into the evolution of Hawaiian Lepidium species, e.g., phylogeny of the endemic species (see above) and the causes of insular woodiness (Böhle, Hilger, and Martin, 1996
) must be based on a comprehensive sampling and the analysis of more variable marker systems, such as RAPD markers.
Australia/New Zealand
Australian and New Zealand endemic species within Lepidium s.s. represent a monophyletic lineage (Fig. 2, clade IX), although this clade is weakly supported by a bootstrap value of 44%. Two sublineages may be recognized irrespective of the traditional classification of relevant species into greges and sections (Thellung, 1906
; Hewson, 1981
). One sublineage classifies New Zealand coastal species (e.g., L. banksii, L. flexicaule, L. naufragorum) along with Australian species predominantly distributed in South and southeast Australia. The lack of resolution within this clade is due to low levels of sequence divergence (0.51% mean) among the species and may indicate rapid radiation. The other clade comprises L. sisymbrioides, with three subspecies that occur in inland New Zealand in dry areas. This taxon is the only one in the Brassicaceae known to be dioecious, and Lloyd (1985)
suggested an autochthonous origin of this feature in New Zealand. Lepidium muelleri-ferdinandi is sister to both sublineages. Apparently, this species of central Australian distribution does not seem to have any close relationships, as has already been suggested by Hewson (1981)
.
Some species are common between New Zealand and Australia, e.g., L. desvauxii, L. flexicaule, L. pseudo-tasmanicum, and L. pseudo-hyssopifolium. Lepidium desvauxii is native to Southeast Australia, Tasmania, and probably New Zealand (Hewson, 1981
; Webb, Sykes, and Garnock-Jones, 1988
). Lepidium flexicaule is native to New Zealand and Tasmania, whereas some other Australian species, e.g., L. pseudo-tasmanicum, L. pseudo-hyssopifolium, are naturalized in New Zealand. There is insufficient resolution on the tree to conclude unambiguously whether the influence is that of the Australian taxa on New Zealand, vice versa, or both. Nevertheless, common species between New Zealand and Australia would indicate intensive dispersal between these regions. The presence of New Zealand endemic taxa in both clades would suggest that there have been at least two dispersals and colonizations of Lepidium to New Zealand, corroborating the view of Mitchell and Heenan (2000)
, based on ITS sequence analysis.
Monophyly of these Australasian Lepidium species would suggest that they all have evolved from a single immigration event. Long-distance dispersal into the southern hemisphere in the Pliocene/Pleistocene is strongly indicated for numerous plant taxa (Raven and Axelrod, 1972
; Raven, 1973
; Barlow, 1994
; Pole, 1994
). Consistent with this hypothesis are the low levels of cpDNA sequence divergence between the species from Australasia and those from South America (1.2% mean), Asia (1.0% mean) and California (clade XI; 0.6% mean). Three migration routes appear feasible. (1) With respect to the Brassicaceae, Raven (1973)
and Gibbs et al. (1986)
suggested that Lepidium and Cardamine entered the southern hemisphere from Asia using the mountain systems of Malaya and New Guinea as stepping stones for crossing the tropics. (2) Lepidium may have also used the Andean Cordillera as an interhemispheric corridor and from there via bird dispersal to Australasia, as was suggested by Smith (1986)
and Barlow (1994)
for many bihemispheric taxa. (3) The third possibility is direct dispersal from the northern hemisphere, e.g., North America (Wardle, 1978
; van Houten, Scarlett, and Bachmann, 1993
). In fact, some birds are known to be regular migrants between Australia/New Zealand and North America (see Wardle, 1978
) and between Australia/New Zealand and East Asia (Rowley, 1982
).
Our phylogenetic tree does not allow firm conclusions on the origin of Australasian Lepidium species, although cpDNA mean sequence divergence indicate closest affinities between species from western North America and Australasia (see above). The inclusion of species from East Asia (e.g., L. chinense) and the high altitude New Guinean species in the study and the analysis of the more variable nuclear-encoded ITS region will perhaps help us understand the evolution of the Australasian Lepidium species.
Relative phylogenetic utility of the three noncoding cpDNA regions analyzed
Recent analyses suggested that these noncoding cpDNA regions are more useful in studying phylogenetic relationships among but not within genera due to lack of informative sequence variation (Sang, Crawford, and Stuessy, 1997
; Cros et al., 1998
; Small et al., 1998
; McDade and Moody, 1999
). The three main lineages in our phylogeny (clades I through III, Fig. 2) are well supported, and these lineages may represent different genera (see above). However, relationships among these basal nodes remain ambiguous due to lack of synapomorphic characters. This may indicate ancient and rapid radiation into the three main lineages. Alternatively, low resolution may be due to an inappropriate DNA marker system employed. Furthermore, relationships within the major clades are often less resolved (Fig. 2, clade III, Lepidium s.s.), apparently due to low numbers of characters. As a general rule, bootstrap values of <60% correspond to 1–2 nucleotide changes (data not shown). A low number of characters and the low rate of homoplasy as revealed by the parsimony analysis (CI = 0.68 excluding uninformative characters; RI = 0.89) may suggest rapid radiation of Lepidium s.s. taxa, as has been discussed in the context of biogeography of this group. In order to provide sufficient phylogenetic information to resolve relationships among the basal nodes and among Lepidium s.s. species, sequencing of a more rapidly evolving locus, i.e., nuclear ITS regions, is currently being performed.
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FOOTNOTES |
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4 Author for reprint requests (Mummenhoff{at}biologie.Uni-Osnabrueck.DE
).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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