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Systematics |
2National Institute for Basic Biology, Okazaki 444-8585, Japan; 3Department of Biological Sciences, Graduate School of Science, University of Tokyo, Tokyo 113-0033, Japan; 4Laboratory of Plant Chromosome and Gene Stock, Faculty of Science, Hiroshima University, Higashi-Hiroshima 739-8526, Japan; 5Department of Molecular Biomechanics, School of Life Science, The Graduate University for Advanced Studies, Okazaki 444-8585, Japan
Received for publication April 23, 2002. Accepted for publication July 19, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Aldrovanda • biogeography • carnivorous plants • Dionaea • Drosera • Droseraceae • rbcL • 18S rDNA
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The carnivorous plant family Droseraceae includes four genera historically: the sundews Drosera, Drosophyllum, Aldrovanda, and the Venus's flytrap Dionaea, the last three of which are monotypic (Cronquist, 1981
; Takhtajan, 1997
). A phylogenetic analysis based on the sequences of two plastid genes, rbcL and matK, indicated that Drosophyllum lusitanicum, a perennial subshrub native to the Iberian coastal fringe and northern Morocco (Juniper, Robins, and Joel, 1989
), does not form a clade with other members of the Droseraceae, but is sister to the Dioncophyllaceae-Ancistrocladaceae clade (Fay et al., 1997
; Meimberg et al., 2000
). The exclusion of Drosophyllum is also supported by some morphological characters (Takahashi and Sohma, 1982
; Juniper, Robins, and Joel, 1989
; Conran, Jaudzems, and Hallam, 1997
).
Aldrovanda vesiculosa and Dionaea muscipula share a similar trapping mechanism, called a snap trap, exclusive to these two taxa (Juniper, Robins, and Joel, 1989
). Aldrovanda vesiculosa is a floating aquatic species that is found throughout the Old World and northern and eastern Australia, while Dionaea muscipula is a terrestrial plant that is endemic to marshy habitats on the coastal plains of North and South Carolina, USA (Juniper, Robins, and Joel, 1989
). The genus Drosera includes nearly 150, mostly perennial, species (Juniper, Robins, and Joel, 1989
; Lowrie, 1998
). Although Drosera has a worldwide distribution, the vast majority of species are found in the Southern Hemisphere, especially in southwestern Australia. Drosera have active flypaper traps and capture their prey with mobile glandular hairs that are present on the adaxial leaf surface.
The evolution of leaves with trap systems from noncarnivorous ones is mysterious, and there are no widely accepted hypotheses. Active flypaper traps are believed to have evolved from a leaf only with adhesive glands after acquisition of nastic and tropic gland tentacles with touch receptors and mobility (Juniper, Robins, and Joel, 1989
). However, the correlations between active flypaper traps and snap traps are ambiguous, because there are no reports of morphologically intermediate leaves. Furthermore, the relationships among the three genera have not been solved with high statistical confidence in either rbcL or matK trees, although the monophyly of Drosera, Dionaea, and Aldrovanda is widely accepted, based on the morphological and molecular data (Williams, Albert, and Chase, 1994
; Fay et al., 1997
; Meimberg et al., 2000
).
Historically, the characters most used for the taxonomy of Drosera have been habit, leaf shape, style number and morphology, and the presence or absence of stipules and specialized organs, such as tubers and gemmae (Candolle, 1824
; Planchon, 1848
; Diels, 1906
, 1936
). In recent decades, new information, such as chromosome numbers (e.g., Kondo, 1976
), pollen morphology (Takahashi and Sohma, 1982
), secondary compounds (Culham and Gornall, 1994
), and seed germination types (Conran, Jaudzems, and Hallam, 1997
), has been added. Although new systems have been proposed recently (Marchant, Ashton, and George, 1982
; Seine and Barthlott, 1994
; Schlauer, 1996
), the delimitations of the subgenera and sections of Drosera are controversial. Williams, Albert, and Chase (1994)
inferred the phylogenetic relationship of 12 Drosera species covering most sections sensu Seine and Barthlott (1994)
, but the phylogenetic relationships within Drosera, which is morphologically divergent and includes more than 150 species, are still ambiguous, because the few species selected from each section have not been sufficient for an overview of the general phylogenetic relationships of Drosera.
The purposes of this study were (1) to investigate the delimitations and phylogenetic relationships of the subgenera and sections in Drosera, (2) to infer the origin and dispersal of Drosera, (3) to infer the evolution of chromosome number, and (4) to infer the phylogenetic relationships among Aldrovanda, Dionaea, and Drosera using rbcL and 18S rDNA sequences.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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except sect. Meristocaules (http://ajbsupp.botany.org/v90/). Total DNA extraction and sequencing generally followed Hasebe et al. (1994)
.
DNA isolation and sequencing
Three overlapping fragments, which cover most of the rbcL gene, were amplified by the polymerase chain reaction (PCR). The primers used for the amplification followed Hasebe et al. (1994)
. The amplified products were electrophoresed on 1% agarose gels and purified with GeneClean III (BIO 101, La Jolla, California, USA). The purified double-stranded DNA was sequenced in both directions using an ABI PRISM 377 DNA sequencer (Applied Biosystems, Foster City, California, USA) with a BigDye Terminator Cycle Sequencing Ready Reaction Kit (Applied Biosystems).
Based on the resulting rbcL tree, eight species of Drosera, Aldrovanda, and Dionaea were selected (http://ajbsupp.botany.org/v90/), and their 18S rDNA was sequenced to analyze the basal relationships of the Droseraceae. The PCR amplification of partial 18S rDNA using primer N-NS1, N-18G, N-18H, C-18G, C-18H, and C-18L (Bult, Källersjö, and Suh, 1992
) was performed. The DNA was purified and sequenced as for the rbcL gene.
Phylogenetic analyses
The rbcL and 18S rDNA nucleotide sequences were aligned using Clustal W version 1.8 (Thompson, Higgins, and Gibson, 1994
) and then revised manually. Phylogenetic analyses were conducted using the parsimony method. To search for the most-parsimonious (MP) tree, PAUP* version 4.0b4a (Swofford, 2000
) was used with the heuristic search option, saving all minimal length trees (MULPARS on) with tree bisection-reconstruction (TBR) branch-swapping, and 10 000 replicates of random taxon addition. Characters were equally weighted. Bootstrap (Felsenstein, 1985
) and decay (Bremer, 1988
; Donoghue et al., 1992
) analyses were used to obtain a measure of support for each branch. Ten thousand bootstrap replications were carried out using "Fast" stepwise addition. The decay indices for representative branches were calculated with PAUP* in conjunction with the program AutoDecay version 5.0 (provided by T. Eriksson, Stockholm University, Stockholm, Sweden). In the decay analyses, the MP trees were searched for under the reverse-constraint option of PAUP* with 100 replications of random sequence addition using TBR branch swapping. The computations were done on a SUN Enterprise 3000 or an SGI Origin 2000 in the Computer Laboratory of the National Institute for Basic Biology (NIBB).
Species of Ancistrocladaceae, Frankeniaceae, Nepenthaceae, Plumbaginaceae, Polygonaceae, Simmondsiaceae, Tamaricaceae, and Drosophyllum were selected as outgroup taxa of the rbcL tree based on previously published broadscale analyses (Williams, Albert, and Chase, 1994
; Meimberg et al., 2000
). Because 18S rDNA sequences are not available in the DNA database for most of these taxa, Simmondsia chinensis and Nepenthes alata were used as outgroup taxa.
We also conducted maximum likelihood (ML) analyses for both rbcL and the combined data sets with PAUP* version 4.0 using a heuristic search, TBR branch-swapping with 1000 random sequence additions, and the HKY85 model (Hasegawa, Kishino, and Yano, 1985
) with a transition/transversion ratio of 2.0, empirical base frequencies, and assuming an equal rate of evolution for all sites.
Character evolution
The phylogenetic distribution of chromosome numbers and geographic distribution were investigated. Chromosome numbers were obtained from the references listed in http://ajbsupp.botany.org/v90/, and operational taxonomic units (OTUs) whose chromosome numbers were counted were included in this analysis. Using MacClade 3.05 (Maddison and Maddison, 1992
), we traced data onto the strict consensus of the shortest trees obtained in the rbcL analysis. Outgroup taxa were excluded, because information on chromosome number for these taxa is scarce. The phylogenetic positions of Aldrovanda and Dionaea were followed for the tree using the combined data set of rbcL and 18S rDNA (Fig. 2). Species with intraspecific polymorphisms of chromosome number were treated as a clade including polytomy OTUs with each chromosome number. Drosera trinervia "A" and "B" formed a sister group (Fig. 1) and merged into a single OTU. To gain insights into the geographic history of Drosera from a phylogenetic perspective, information on the geographic distribution of Drosera obtained from the Carnivorous Plant Database (http://www2.labs.agilent.com/bot/cp_home) was traced on the strict consensus tree of the shortest rbcL trees modified as mentioned above. Species distributed in different geographic areas were treated as a clade, including OTUs with different distributions.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), was used for the phylogenetic analyses. The nucleotide sequences were aligned without any insertions or deletions. The data matrix for the 75 taxa including 16 outgroup taxa contained 395 variable sites, of which 262 were phylogenetically informative. Parsimony analysis produced 4608 MP trees of 1087 steps in 12 islands (Maddison, 1991
). One of the islands included 4597 MP trees, while every other island contained a single tree. The MP trees had a consistency index of 0.501 (0.421 excluding uninformative sites), a retention index of 0.800, and a rescaled consistency index of 0.400. One of the 4620 MP trees is shown in Fig. 1 with decay indices and bootstrap values. The ML analysis yielded a single ML tree (–ln = 8789.030) in a single island that is concordant with the strict consensus tree of the MP analysis (data not shown).
As the relationships of Dionaea, Aldrovanda, Drosera regia, D. arcturi, and other Drosera species were not well-resolved, partial 18S rDNAs of the former four species and D. pygmaea, D. glanduligera, D. anglica, D. montana var. tomentosa, D. sessilifolia, and D. platypoda were sequenced (http://ajbsupp.botany.org/v90/). The nucleotide sequences of 18S rDNA between base pairs 49 and 1707, numbered from the first nucleotide of Glycine max 18S rDNA (Eckenrode, Arnold, and Meagher, 1985
), were aligned, and the 1648-bp region excluding insertions and deletions was combined with the 1227-bp rbcL nucleotide sequence. The 2875-bp data matrix for the 13 taxa, including two outgroup taxa, contained 357 variable sites, of which 181 were informative. Parsimony analysis produced a single MP tree of 589 steps in a single island with a consistency index of 0.727 (0.600 excluding uninformative sites), a retention index of 0.574, and a rescaled consistency index of 0.417 (Fig. 2). The ML analysis yielded a single ML tree (–ln = 7748.00) identical to the MP tree in a single island (data not shown).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Juniper, Robins, and Joel, 1989
). Both systems have sessile glands for absorbing digested prey, and the cellular anatomy of these glands is similar in the two systems. Comparative studies of cellular organization of the stalked glands of Drosera and the trigger hairs of Dionaea and Aldrovanda indicate that these multicellular hairs have a close relationship. The origin of these glandular hairs, trigger hairs, and sessile glands is likely traced to adhesive glands observed in the Plumbaginaceae and other families, which are outgroups of the Droseraceae clade (Drosera, Dionaea, and Aldrovanda) and the Dioncophyllaceae clade, which includes two flypaper carnivorous plants, Drosophyllum and Triphyophyllum (Meimberg et al., 2000
). Our result indicates that the flypaper system of Drosera and the snap trap system of Dionaea and Aldrovanda were established early in the evolution of these carnivorous plant taxa. As the rbcL tree does not show high bootstrap support for particular relationships to any of the outgroup taxa, it was not possible to elucidate which trap system the common ancestor of these two lineages had or whether these two systems evolved independently from noncarnivorous plants. The sister relationship of Dionaea and Aldrovanda indicates a single evolutionary origin of the elaborate snap trap system in plants, although terrestrial Dionaea and aquatic Aldrovanda have different habitats.
Interspecific relationships of Drosera
The basal relationships of Drosera were ambiguous in both the rbcL and combined trees, although D. regia and D. arcturi clustered more basally than the other Drosera species in both trees. Drosera regia, which occurs in a single mountain valley in South Africa (Obermeyer, 1970
), has traditionally been treated as a different group from the other Drosera, because it has several plesiomorphic characters, such as operculate pollen (Takahashi and Sohma, 1982
) and a lack of stipules (Williams, Albert, and Chase, 1994
), both of which are similar to characters found in Dionaea. Drosera regia also has some autapomorphic characters, which are not observed in other Drosera species, such as woody rhizome, the longest leaves and inflorescences in the genus, and somewhat zygomorphic flowers resulting from the odd position of the three exceptionally long and undivided styles except at the very apicies (Stephens, 1926
).
The basal clustering of D. arcturi is unexpected, because this species does not have plesiomorphic characters as observed in D. regia. Drosera arcturi is native to New Zealand and southeastern Australia, including Tasmania (Allan, 1961
; Lowrie, 1998
), and is thought to be closely related to D. stenopetala and D. uniflora because of their shared characters, such as solitary white flowers on relatively short scapes and reduced or absent stipules (Diels, 1906
, 1936
; Schlauer, 1996
; Lowrie, 1998
). On the rbcL tree, D. arcturi was not closely related to D. stenopetala and D. uniflora. Further analyses of morphological characters, such as pollen morphology, which is divergent among major groups of Drosera (Takahashi and Sohma, 1982
), may produce further evidence that supports the basal relationship of D. arcturi in Drosera.
Australian species
We will follow the system of Seine and Barthlott (1994)
in the following discussion (http://ajbsupp.botany.org/v90/, Fig. 1). The clade from D. stolonifera to D. glanduligera in Fig. 1 includes species distributed in Australia. Section Coelophylla is basal to sect. Bryastrum, sect. Lasiocephala, sect. Phycopsis, and subgen. Ergaleium including sect. Ergaleium, Erythrorhizae, and Stoloniferae. A clade composed of these sections was found in a smaller scale rbcL analysis (Albert et al., 1992; Williams, Albert, and Chase, 1994
) and was further confirmed in this study, which included several more species. Species in this clade are well adapted to dry environments and have tubers (subgen. Ergaleium), stout roots (sect. Phycopsis), or an annual habit (sect. Coelophylla) (Lowrie, 1987
, 1989
, 1998
), and species with each adaptive character form a different clade. Species with gemmae for vegetative propagation form a monophyletic group (sect. Bryastrum and Lasiocephala). The monophyly of sect. Phycopsis and subgen. Ergaleium proposed based on pollen morphology characterized by poorly developed radial plates (Takahashi and Sohma, 1982
) was supported with a high bootstrap probability (BP) (80%).
All species in sect. Bryastrum, except D. pygmaea, have pentamerous flowers and are restricted to southwestern Australia. Drosera pygmaea has tetramerous flowers and occurs in New Zealand (Allan, 1961
) and both eastern and western Australia (Lowrie, 1989
). Due to its tetramerous flowers and unique distribution, D. pygmaea has been placed in a different section from all other pygmy sundews (Planchon, 1848
; Diels, 1906
, 1936
; Marchant, Ashton, and George, 1982
; Schlauer, 1996
). The rbcL tree indicates that D. pygmaea forms a clade with other pygmy sundews and that tetramerous flowers are an autapomorphic character that evolved in this species from the pentamerous flowers shared by other pygmy sundews. This result supports the system of Seine and Barthlott (1994)
in which D. pygmaea is included in sect. Bryastrum with other pygmy sundews.
The three sections of subgen. Ergaleium are distinguished by their leaf shape and the presence or absence of erect stems (Marchant, Ashton, and George, 1982
). Section Ergaleium is characterized by erect or scrambling stems. Section Erythrorhizae includes species with non-erect short stems with leaves in rosettes. Section Stoloniferae comprises a few species that form two growth phases: a short stem with rosette leaves in early development and short erect stems at a later stage. The rbcL tree suggests that the species with an erect stem without rosette leaves in sect. Ergaleium are more basal than those with rosette leaves in sect. Erythrorhizae and Stoloniferae. The latter two sections are paraphyletic in the rbcL tree, although their bootstrap values are not so high. Further analyses using more taxa are necessary for systematic revision of these sections.
Drosera burmannii and D. sessilifolia of sect. Thelocalyx have plesiomorphic pollen with simple cohesion, like that observed in Aldrovanda and Dionaea, instead of cross wall cohesion as observed in other Drosera species, except D. glanduligera. Their pentamerous gynoecium is also observed in the outgroup taxa, but not in other Drosera species (Diels, 1906
, 1936
). A sister relationship of both species was strongly supported with 100% BP in the rbcL tree, although these species are distributed in disjunct areas: Australia, India, China, Japan throughout Southeastern Asia for D. burmannii and endemic in South America for D. sessilifolia (Lowrie, 1998
; de Stefano and Culham, 1998
).
Polyphyly of section Drosera
Section Drosera is not monophyletic (Fig. 1). The most basal clade includes D. hamiltonii, which is native to southwestern Australia (Lowrie, 1989
) and has a fused style, a characteristic not observed in any other Droseraceae, except Dionaea (Diels, 1906
, 1936
; Lowrie, 1989
). Although D. hamiltonii has been classified in a section separate from other species of sect. Drosera (Diels, 1906
, 1936
; Marchant, Ashton, and George, 1982
; Schlauer, 1996
), it formed a clade with two species of sect. Drosera: D. adelae and D. indica. Although the close relationship between D. adelae and D. indica has been suggested by previous studies (Planchon, 1848
; Diels, 1906
, 1936
; Marchant, Ashton, and George, 1982
), neither of these species has ever been closely associated with D. hamiltonii. One character supporting the monophyly of this clade is the chromosome number of these species, 2n = 28 or 30, which is rare in other Drosera species (Fig. 3A; Venkatasubban, 1950
; Kondo, 1976
; Kondo and Olivier, 1979
; Kondo and Lavarack, 1984
).
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).
The clade from D. graminifolia to D. montana var. schwackei in Fig. 1 is distributed in South America, mainly in central and eastern Brazil. Drosera montana is one of the most taxonomically confusing species in the genus Drosera. Saint-Hilaire (1824)
described D. tomentosa, D. hirtella, and D. montana, but Diels (1906
, 1936
) eliminated the former two taxa as varieties of D. montana and further described D. montana var. schwackei. In the rbcL tree, D. hirtella belongs to a different clade from other varieties of D. montana, supporting the designation of Saint-Hilaire (1824)
. The three varieties of D. montana examined in this study did not form a clade, which suggests that these varieties should be treated as different species rather than as varieties of D. montana.
The clade from D. hilaris to D. aliciae is composed of African species. The species in sect. Ptycnostigma are characterized by their thickened roots. Some authors (Diels, 1906
, 1936
; Seine and Barthlott, 1994
) placed these species in an independent section, while Marchant, Ashton, and George (1982)
merged this section with sect. Drosera. The rbcL tree supports the classification treating sect. Ptycnostigma as different from other sections.
The rbcL tree is not concordant with any intrageneric classification of Drosera, although some clades characterized by morphological characters, chromosome number, and geographic distribution were detected in the rbcL tree. It is necessary to revise the classification of Drosera by incorporating the rbcL tree data and further analyses of morphological characters.
Evolution of chromosome number
Our analysis showed that conspicuous chromosome diversity caused by both aneuploidization and polyploidization is observed extensively in the clade from D. stolonifera to D. glanduligera, which is almost exclusively Australian, while chromosome number is moderately conserved in the other clades (Fig. 3A). Aneuploidy in Drosera is likely caused by the diffused centromeres, which should be stably transmitted after cell division, even if some chromosomes are fragmented (Kondo, Segawa, and Nehira, 1976
). Distinct primary constrictions or centromeres and clear gaps between sister chromatids have not been observed in Drosera (Kondo, Segawa, and Nehira, 1976
; Kondo and Segawa, 1988
), which supports this hypothesis. It has been shown that chromosomes artificially fragmented by gamma radiation are mitotically functional, which also supports this hypothesis (Sheikh, Kondo, and Hoshi, 1995
). The reason why aneuploidy is more popular in Australia than in other areas is unknown, and further studies on polymorphisms of chromosome numbers and karyotypes in Australian Drosera species are necessary.
The chromosome number of D. regia is 2n = 34, which is unique among Drosera species. This number is similar to those of Dionaea (2n = 30 or 32) and Aldrovanda (2n = 38), which is concordant with the basal position of D. regia in the Drosera rbcL tree. On the other hand, the chromosome number of the other basal species, D. arcturi, is 2n = 20, which is also found in other Drosera species (Fig. 3A). This suggests that D. regia is more basal than D. arcturi.
Most of the species in the terminal clades from D. hilaris to D. montana var. schwackei have a chromosome number of 2n = 40, which is probably related to 2n = 20. A decrease in chromosome number from 40 to 20 occurred in D. burkeana.
Phytogeography of Drosera
Drosera is widely distributed in both hemispheres (Juniper, Robins, and Joel, 1989
; Schlauer, 1996
), and the center of diversity of Drosera appears to be Australia, where over 80 species are found (Lowrie, 1987
, 1989
, 1998
). Africa contains over 30 species, although species distributed in northern Africa are limited and half of the species are distributed in South Africa. South America also has about 30 species, some of which have expanded their range into North America. Less than ten species occur in Eurasia and North America, although some of these species are recorded over a wide range. Our analysis showed that the species endemic to Africa are divided into three groups: D. regia, D. indica, and the other African species (Fig. 3B). Drosera regia is basal, while the clade including all the other African species except D. indica clustered at the terminal position. Drosera arcturi, which is native to Australia and New Zealand, is also basal, and all the other Australian species clustered next to D. regia and D. arcturi, indicating that the origin of Drosera was in Africa or Australia. Aldrovanda is widely distributed in both hemispheres, including Australia and Africa, while Dionaea is endemic to North America. The distributions of the other outgroup species used in this study (http://www.ajbsupp.botany.org/v90/) varied, and it was impossible to specify whether Drosera originated in Africa or Australia.
The rbcL tree shows that the South American species arose by dispersal from Australia and that the African species other than D. regia and D. indica arose from South America. This pattern of distribution recalls the continental drift of Gondwanaland. This hypothesis is not plausible, because the Droseraceae are located close to the tip of the angiosperm phylogenetic tree, while this family would have to have split from the other angiosperm families at a very distant time for the Gondwanaland break-up to explain the divergence of Drosera species. Although some extinct angiosperm taxa related to extant families were reported (reviewed in Crepet, 2000
), it is hard to extrapolate that ancestors of extant species in an extant genus were diverged at the age of Gondwana breakage. The hypothesized Gondwana origins of the Coriariaceae and Melastomataceae were rejected by the molecular clock (Yokoyama et al., 2000
; Renner, Clausing, and Meyer, 2001
), and this is also the case for the Drosera, whose disjunct distribution likely resulted from long-distance dispersal. Even though a molecular clock of rbcL is episodic, divergence of extant genera does not ascend to the Cretaceous (Sanderson and Doyle, 2001
).
Dispersal from Australia to South America also likely occurred in the clade that includes D. burmannii and D. sessilifolia. Two closely related species, D. uniflora and D. stenopetala, have disjunct distributions in South America and New Zealand. Similar close relationships between New Zealand and South American species have been reported in Coriaria (Yokoyama et al., 2000
), and there might be some unknown mechanism for long-distance dispersal between these two continents. The species endemic to New Caledonia, D. neocaledonica, likely originated from a South American ancestor via long-distance dispersal.
Dispersal from Australia to Asia via Southeast Asia occurred in D. burmannii, D. indica, and D. peltata, although it is not known why these species were the only members of their respective clades to expand their distributions in such a manner. Smaller numbers of Drosera species are distributed in the Northern Hemisphere than in the Southern Hemisphere, as mentioned above. Our analysis suggests that all the Northern Hemisphere species examined (D. rotundifolia, D. anglica, D. filiformis, D. capillaris, D. brevifolia, D. indica, D. burmannii, and D. peltata) expanded their distributions from the Southern Hemisphere, although further analyses with more taxa will be necessary to confirm this inference. Drosera anglica and D. rotundifolia are distributed in both Eurasia and North America, and it is likely that these species expanded their range by dispersal from South America to Eurasia via North America.
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FOOTNOTES |
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6 Author for reprint requests (FAX: +81-564-55-7546; mhasebe{at}nibb.ac.jp
)
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LITERATURE CITED |
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