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Keywords:

  • biogeography;
  • Hordeum (Poaceae;
  • Triticeae);
  • long-distance dispersal;
  • phylogeny;
  • vicariance

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information
  • • 
    The grass genus Hordeum (Poaceae, Triticeae), comprising 31 species distributed in temperate and dry regions of the world, was analysed to determine the relative contributions of vicariance and long-distance dispersal to the extant distribution pattern of the genus.
  • • 
    Sequences from three nuclear regions (DMC1, EF-G and ITS) were combined and analysed phylogenetically for all diploid (20 species) and two tetraploid Hordeum species and the outgroup Psathyrostachys. Ages of clades within Hordeum were estimated using a penalized likelihood analysis of sequence divergence.
  • • 
    The sequence data resulted in an almost fully resolved phylogenetic tree that allowed the reconstruction of intrageneric migration routes. Hordeum evolved c. 12 million years ago in South-west Asia and spread into Europe and Central Asia. The colonization of the New World and South Africa involved at least six intercontinental exchanges during the last 4 million years (twice Eurasia–North America, North America–South America, twice South America–North America and Europe–South Africa).
  • • 
    Repeated long-distance dispersal between the northern and southern hemisphere were important colonization mechanisms in Hordeum.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Long-distance dispersal of plant seeds or vegetative parts to remote islands, followed by speciation, is thought to be a major mechanism contributing to the generation of diverse and disharmonic island floras (Wagner & Funk, 1995). Composition of continental floras, however, seems to be influenced mainly by taxon vicariance following range fragmentation resulting from plate tectonic events (Raven & Axelrod, 1974) and climatic changes (Engler, 1879). Several disjunctively distributed taxa have therefore been interpreted as remnants of earlier geofloras that were distributed in, for example, Laurasia or Gondwana (Raven & Axelrod, 1974; Boufford & Spongberg, 1983; Tiffney, 1985; Riddle et al., 2001), and were subdivided when these continents drifted apart. The importance of long-distance dispersal for continental floras is not equally acknowledged, although examples of intercontinental floristic exchange exist (Liston & Kadereit, 1995; Wendel et al., 1995; Vargas et al., 1998; Vijverberg et al., 1999; Winkworth et al., 2002; Coleman et al., 2003; Givnish et al., 2004).

Hordeum L., including cultivated barley (Hordeum vulgare ssp. vulgare), is a monophyletic genus of Poaceae–Triticeae, most closely related to the Asian Psathyrostachys Nevski (Petersen & Seberg, 1997; Blattner, 2004). Cytological analyses defined four Triticeae genomes (I, H, Xa, Xu) in Hordeum (Linde-Laursen et al., 1992; von Bothmer et al., 1995), which form monophyletic groups in the genus (Blattner, 2004). The 31 Hordeum species occur disjunctively on the continents of the northern hemisphere, in southern South America, and in South Africa (von Bothmer et al., 1995). To determine the impact of (recent) long-distance dispersal within and between continents vs. fragmentation of more ancient and formerly continuous distribution ranges, DNA sequence data from three nuclear loci were analysed for all diploid Hordeum species: Translation elongation factor G intron (EF-G; Komatsuda et al. 1999, 2002), disrupted meiotic cDNA 1 (DMC1; Petersen & Seberg, 2003), and the nuclear rDNA internal transcribed spacer region (ITS; Blattner, 2004). Like many other grasses, Hordeum is characterized by containing diploid (2n = 14) and polyploid (2n = 28, 42) species or cytotypes. Allopolyploid taxa can provide additional biogeographic information about contact zones of the parental species and have an independent geographical history after their origin. Therefore, four allopolyploid Hordeum species with distribution areas different from their diploid progenitors (von Bothmer et al., 1995; Blattner, 2004) were also included in this analysis.

Materials and Methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Taxon sampling and molecular methods

Twenty-six diploid Hordeum taxa representing all 20 diploid Hordeum species were analysed. Most accessions belong to the Barley Core Collection and have been used in earlier molecular studies (Komatsuda et al., 1999, 2002; Petersen & Seberg, 2003; Blattner, 2004). The nuclear loci analysed in the present investigation occur on four different chromosomes in H. vulgare: DMC1 is a single-copy gene on chromosome 3H (Petersen & Seberg, 2003), EF-G is a single-copy gene on chromosome 2H (Komatsuda et al., 1999), and the ITS region is part of the rDNA clusters on chromosomes 5H and 6H (Taketa et al., 1999). Table 1 lists the taxa and the EMBL nucleotide database accession numbers of the sequences included in the combined (supermatrix) data analysis. The EF-G (Komatsuda et al., 1999) and DMC1 (Petersen & Seberg, 2003) sequences of Psathyrostachys stoloniformis have been combined with the ITS sequence from Psathyrostachys juncea (Blattner, 2004) into a single, artificial Psathyrostachys taxon that was used as the outgroup. Most polyploid taxa of Hordeum occur in single geographical regions together with their ancestors, and therefore do not influence the interpretation of biogeographical patterns. However, four allopolyploid species with distribution patterns distinct from at least one of their parents exist and have been included in this study. While for the polyploids Hordeum jubatum and Hordeum guatemalense the parental species are quite clear (Linde-Laursen et al., 1992; Nishikawa et al., 2002; Blattner, 2004), contradicting hypotheses about the progenitors of the geographically critical tetraploids Hordeum capense and Hordeum secalinum have been proposed based on the sequences of DMC1 (Petersen & Seberg, 2004) vs nuclear rDNA (Baum & Johnson, 2003; Blattner, 2004). For both species no EF-G sequences were available in the EMBL nucleotide database. Therefore, the intron of the EF-G locus was polymerase chain reaction (PCR)-amplified according to the protocol of Komatsuda et al. (1999). The PCR was conducted in four parallel reactions to avoid missing rare EF-G copies. The four amplicons were pooled, purified, cloned, and eight clones per species were sequenced as described in Blattner (2004). The DMC1 sequences from these species were obtained from Petersen & Seberg (2004).

Table 1.  Taxa and sequence accession numbers used in the combined data set of three nuclear loci for the analysis of all diploid and two tetraploid Hordeum species
TaxonDistributionEMBL nos. EF-G1DMC12ITS3
Hordeum bogdanii WilenskyCentral AsiaAF135001AY137412AJ607819
Hordeum brachyantherum Nevski ssp. californicum (Covas & Stebbins) Bothmer et al. Western North AmericaAF135004AF277260AJ607842
Hordeum brevisubulatum (Trin.) LinkCentral AsiaAF135003AY137396AJ607852
Hordeum bulbosum L.Western EurasiaAF134989AY137411AJ607863
Hordeum capense Thunb. (4x)South AfricaAJ606093/4*AY592985/86AJ607868
Hordeum chilense Roem. & Schult.ChileAF134996AY137408AJ607872
Hordeum comosum J. PreslSouthern Andes, PatagoniaAF135000AY137400AJ607878/9
Hordeum cordobense Bothmer et al. Central ArgentinaAF134997AY137415AJ607885
Hordeum erectifolium Bothmer et al.Central ArgentinaAF135005AF277259AJ607899/900
Hordeum euclaston Steud.Central ArgentinaAF134993AY137401AJ607906
Hordeum flexuosum Nees ex Steud.Central ArgentinaAF134994AY137399AJ607911
Hordeum intercedens NevskiSouth-western North AmericaAF134992AY137409AJ607923
Hordeum marinum Huds. ssp. gussoneanum (Parl.) Thell.Western EurasiaAF135012AY137397AJ607960
Hordeum marinum Huds. ssp. marinumWestern EurasiaAF135011AF277257AJ607977
Hordeum murinum L. ssp. glaucum (Steud.) TzvelevWestern EurasiaAF134990AF277258AJ607986
Hordeum muticum J. PreslCentral and northern AndesAF134995AY137398AJ608020
Hordeum patagonicum (Haumann) Covas ssp. magellanicum (Parodi & Nicora) Bothmer et al.Southern PatagoniaAF135009AY137414AJ608032
Hordeum patagonicum (Haumann) Covas ssp. mustersii (Nicora) Bothmer et al. Southern PatagoniaAF135010AY137405AJ608036/7
Hordeum patagonicum (Haumann) Covas ssp. patagonicumSouthern PatagoniaAF135006AY137444AJ608041
Hordeum patagonicum (Haumann) Covas ssp. santacrucense (Parodi & Nicora) Bothmer et al. Southern PatagoniaAF135008AY137406AJ608055/8
Hordeum patagonicum (Haumann) Covas ssp. setifolium (Parodi & Nicora) Bothmer et al. Southern PatagoniaAF135007AY137404AJ608052
Hordeum pubiflorum Hook. f.Southern Andes, PatagoniaAF134999AY137402AJ608082/4
Hordeum pusillum Nutt.Central and E North AmericaAF134991AY137410AJ608095
Hordeum roshevitzii BowdenCentral AsiaAF135002AY137416AJ608111
Hordeum secalinum Schreb. (4x)Western EuropeAJ606095/6*AY5929783/4AJ608118/9
Hordeum stenostachys Godr.Central ArgentinaAF134998AY137407AJ608125
Hordeum vulgare L. ssp. spontaneum (K. Koch) Thell.Western EurasiaAF134988AF277262AJ608145
Hordeum vulgare L. ssp. vulgareCrop speciesAF134987AY137413AJ608146
Psathyrostachys juncea (Fisch.) NevskiCentral and western EurasiaAJ608151
Psathyrostachys stoloniformis BadenCentral and western EurasiaAF135013AF277261

Data analyses

Alignment of the sequences from the three loci was straightforward and could be done manually. Phenetic and parsimony analyses were performed in paup* 4.0b10 (Swofford, 2003), and Bayesian analyses were performed with mrbayes v3.0b4 (Ronquist & Huelsenbeck, 2003). Different likelihood models of DNA evolution were tested in modeltest 3.06 (Posada & Crandall, 1998) and the TrN + Γ and HKY85 + Γ models were chosen by LRT and AIC, respectively. For these models maximum-likelihood distances were calculated and analyzed with the neighbor-joining (NJ) algorithm. Parsimony analysis (MP) was conducted with the branch-and-bound search algorithm. Branch support was tested with 1000 bootstrap resamples (NJ and MP). For Bayesian inference (BI), six chains were run for 1 million generations under the HKY85 + Γ model of DNA evolution, with ‘databreaks’ defining the sequences from the three loci as separate DNA parts, and sampling a tree every 100 generations. Posterior probabilities were calculated from 8000 trees, excluding the initial nonstationary trees (burn in = 2001).

Most Hordeum species contain two nucleolus-organizing regions (NORs) in their genomes (Taketa et al., 1999, 2001). The rDNA clusters in the NORs evolve in a punctuated pattern (i.e. periods of independent evolution within the NORs are periodically interrupted by interlocus homogenization between the NORs; Blattner, 2004). Independent evolution of the rDNA clusters during the last two million years (MY) created two paralogous ITS sequence types in New World Hordeum species. Each of these types was lost from the genomes of some Hordeum species by bidirectional interlocus homogenization (Blattner, 2004). Thus, these species possess ITS sequences of either type-1, type-2, or of both ITS types. Because the analysis of ITS data resulted in a sister-group relationship of the two paralogs in the New World Hordeum species and some species lack one or the other type, it is not possible to deduce directly species phylogeny from the ITS gene tree. Therefore, for most species the type-2 ITS copy was included in the combined data matrix here, as this type occurs in a higher number of species. Three taxa which lack type-2 ITS (Hordeum cordobense, Hordeum muticum, and Hordeum patagonicum ssp. patagonicum) were included with their type-1 sequences. To determine the phylogenetic position of the New World taxa despite the occurrence of paralogs two approaches were used. (1) Two data matrices, combining DMC1 and EF-G sequences with either the type-1 or type-2 ITS sequences were analysed (MP) and either the resulting 16 and 20 most parsimonious trees or their strict consensus trees were recoded for a matrix representation with parsimony (MRP) supertree approach (Baum, 1992; Ragan, 1992; for reviews see Sanderson et al., 1998; Bininda-Emonds et al., 2002). The characters derived from both tree sets were weighted 1 : 0.8 to compensate for the differences in tree number, and analyzed with MP in paup*. (2) In a supermatrix approach DMC1 and EF-G sequences were combined with the ITS sequences including type-1 and type-2 ITS as two separate genes, and coding the sequences missing in some taxa as unknown character states (N). Maximum parsimony was used as before to analyse this data matrix.

As sequence assignment to the two parental genomes in the allotetraploid species H. capense and H. secalinum was unambiguously possible at all nuclear loci, the DMC1, EF-G, and ITS sequences from each of the tetraploid species were combined into two pseudotaxa. These were analysed together with the diploid Hordeum taxa to find the positions of putative parental species in the phylogenetic trees. In H. capense, where only the H-genome specific ITS sequence was found, the Xa sequence positions were coded as missing.

The age of the crown group of the genus of roughly 12 million years (MY) (Blattner, 2004) was calculated under the assumption of a split between wheat and barley c. 13 MY ago. A date of 13 MY (Gaut, 2002) was derived from two chloroplast genes (ndhF and rbcL) of representative Poaceae species, using the nonparametric rate smoothing method (Sanderson, 1997) and the phylogeny of Poaceae as presented by the Grass Phylogeny Working Group (2001). The age of 12 MY was used to calibrate the deepest split in Hordeum. As the sequence data failed a likelihood-ratio test of mutation rate constancy among lineages (χ2 test, P < 0.01), calculations of the divergence times of the clades within Hordeum were carried out with a penalized likelihood (PL) approach in r8s, version 1.5 (Sanderson, 2002) with the truncated newton method (TN). The smoothing parameter S was determined by the cross-validation procedure of r8s and was set to S = 10 in the final run. Standard deviations for the node dates were calculated in r8s with the bootstrap procedure involving 200 bootstrap resamples (Baldwin & Sanderson, 1998) on the data set with the root node of Hordeum fixed to an age of 12 MY. To account for possible uncertainties in this date caused by the use of a secondary calibration point, the fixed node was also constrained to ages in a range of 12.5–10 MY.

Biogeographic scenarios were reconstructed using dispersal–vicariance analysis in DIVA 1.1 (Ronquist, 1996, 1997) using initially five geographic regions: Western Eurasia, Central and East Asia, North America, southern South America, and South Africa. The occurrence of two monophyletic Hordeum groups in distinct areas of South America allowed further subdivision of this region into southern Argentina and central Argentina to Peru, particularly as these areas differ also pronouncedly with respect to climate conditions (S. S. Jakob & F. R. Blattner, unpublished). To define the initial distribution area of Hordeum, three additional outgroup species from Triticeae plus Bromus were added to the DIVA tree with phylogenetic positions according to Blattner (2004). Two analyses were conducted using either unconstrained ancient distribution areas or imposing a constraint for maximally two ancient distribution areas. The ages of Hordeum (12 MY) and the relevant subgroups (6–4 MY) allowed for the assumption that the continents were in their present-day positions and that the relevant landbridges (Beringia, Central America) were nearly or already in place at the time of origin of the taxa (Tiffney, 1985; Graham, 2003).

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

The alignment of sequences from three DNA loci from 26 diploid Hordeum taxa and the outgroup Psathyrostachys was 1980 base pairs in length and had 358 variable positions, of which 180 were parsimony-informative. Pairwise HKY85 + Γ maximum-likelihood distances ranged from 0.1 to 7.8%. All phylogenetic algorithms produced nearly identical tree topologies (Figs 1 and S1; figures and tables prefixed by ‘S’ are available as supplementary online material on the journal's homepage or directly from the author). Species relationships had to be derived from these (gene) trees by either a supertree or a supermatrix approach, because two ITS paralogs and bidirectional interlocus ITS homogenization occurred in two South American Hordeum groups (Blattner, 2004), resulting in a seemingly polyphyletic H. patagonicum and a close relationship of H. patagonicum ssp. patagonicum, H. cordobense, and H. muticum (Fig. 1). The MRP supertree analysis of the 36 most parsimonious trees resulted in 282 trees, which placed ssp. patagonicum with the other subspecies of H. patagonicum, included H. cordobense and H. muticum in a clade of mostly northern Argentinean species, and grouped Hordeum comosum together with H. patagonicum and Hordeum pubiflorum (Fig. 2). No unsupported clades (Bininda-Emonds, 2004) occurred in the resulting supertree. Analysing the ITS paralogs as two separate genes together with DMC1 and EF-G in a supermatrix resulted in 10 012 most parsimonious trees of 712 steps length. In the strict consensus tree Hordeum brachyantherum (2x) is sistergroup to all other New World taxa (data not shown). Although the resolution within this latter clade is generally low, two North American–South American species pairs were found within this group (see later).

image

Figure 1. Phylogenetic analysis of the combined data sets of the nuclear loci DMC1, EF-G and ITS from diploid Hordeum species with Bayesian inference. The numbers at the branching points give the posterior probabilities of the respective groups. Penalized likelihood (PL) age estimates (in million years, MY) plus standard deviations are given along the branches. Asterisks indicate taxa which possess exclusively the type-1 ITS paralog. For all other species type-2 ITS sequences were included in this analyses. For subspecies names see Table 1.

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image

Figure 2. Majority rule consensus tree of 282 most parsimonious trees derived from a matrix representation with parsimony (MRP) supertree analysis. Group frequencies are given along the branches. Taxa with the ITS paralogs are given in bold letters.

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All analyses revealed the four genome groups of Hordeum (H, I, Xa and Xu) as monophyletic (Fig. 3a), and resulted in a clear distinction of the three Asian species (Hordeum bogdanii, Hordeum brevisubulatum, and Hordeum roshevitzii) within the H-genome group from the remaining taxa, which are distributed in the New World (Fig. 3a). Hordeum murinum was sister to Hordeum bulbosum and H. vulgare, though with bootstrap support as low as 56%. Bootstrap support (bs) values, particularly those obtained in the MP analysis, were often lower than the respective posterior probabilities (pp) of BI (Figs 1 and S1). The monophyly of H. marinum and all H-genome taxa (100% bs and 1.0 pp) and the monophyly of the latter clade (= 97% bs, 1.0 pp) were strongly supported. The branches important for the inference of biogeographic patterns were also well-supported. Even among the closely related and genetically rather similar New World species, the combined data were able to resolve species relationships. All analyses identified the diploid Californian H. brachyantherum as sister (= 96% bs, 1.0 pp) to the mainly South American species of the H-genome group. Within this latter clade the data revealed two North American–South American disjunct species pairs, namely Hordeum pusillum/Hordeum erectifolium (= 51% bs, 0.94 pp) and Hordeum intercedens/Hordeum euclaston (= 90% bs, 1.0 pp).

image

Figure 3. Phylogenetic relationships and biogeographic scenario of Hordeum. (a) Phylogenetic tree of diploid Hordeum species based on a combined data matrix of sequences from three nuclear loci (DMC1, EF-G, ITS). The diploid Hordeum species are drawn directly on the branches of the phylogeny. Tetraploid taxa are mapped to the right, with lines connecting the taxon names with their respective parental species. Full subspecies names are listed in Table 1. Genome denominations are given in italic type below the branches. Numbers to the right of the branches show the estimated ages (in million years, MY) of the splits, calculated under the assumption of a separation of Triticum and Hordeum ancestors c. 13 MYA (Gaut, 2002). Roman numbers (I–XI) refer to the distribution routes in the map in (b). The colors in the tree depict the geographical distribution of the taxa: Blue, western Eurasia; green, Central and East Asia; orange, North and Central America; red, northern group in South America; brown, southern group in South America; pink, South Africa. Colored dots and squares on the tree mark arrivals in new geographic regions, where squares depict vicariance patterns and dots the intercontinental long-distance dispersals. (b) Biogeographic scenario of Hordeum species plotted on the distribution map of the genus. Shading of the areas reflect the species numbers of the respective regions. Black roman numbers refer to the diploid parts of the phylogenetic tree as shown in the insert, while the distribution events on the polyploid level were indicated by gray roman numbers.

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The analysis of the combined data sets in the allotetraploid species H. capense and H. secalinum resulted in two classes of parental sequences, similar to either sequences of H. marinum (Xa genome) or of the H-genome taxa (Fig. S3). The latter sequences grouped in the H-genome clade between the three species from Asia and the New World taxa. This supports the conclusion that H. marinum and a H-genome species were involved in the evolution of the tetraploids. The positions of two additional allotetraploid taxa of the H-genome group in the tree (Fig. 3a) were inferred from cytological studies (Linde-Laursen et al., 1992) and chloroplast (Nishikawa et al., 2002) and ITS (Blattner, 2004) sequence analyses of Hordeum. According to these data, H. jubatum is derived from the Asian H. roshevitzii and the Californian H. brachyantherum or a close extinct relative (Linde-Laursen et al., 1992; Nishikawa et al., 2002; Blattner, 2004). The Central American H. guatemalense originated from H. jubatum and southern Californian H. intercedens (Blattner, 2004).

The PL age estimates of the Hordeum clades are given in Table 2, Fig. 1, and for clades with high statistical support also in Fig. 3a. Changes in the basal calibration point between 12.5 and 10 MY changed the estimated ages of the internal nodes in the tree relatively uniformly by c. 18% (data not shown) and revealed no inconsistencies with the biogeographical scenario reported below. The dating of the split between H. capense and H. secalinum was calculated from ITS data (Blattner, 2004).

Table 2.  Estimated crown ages (in million years) for the major clades in the phylogeny of diploid Hordeum species
NodeMeanSDMinimumMaximum
Hordeum (fixed node)12.0
I plus Xu clade 9.7760.4758.79511.128
H plus Xa clade 6.3400.4124.914 7.661
I clade 5.8270.4584.631 7.150
Hordeum vulgare 0.6670.2220.135 1.182
Xa clade (H. marinum) 1.9270.4201.073 3.562
H clade 5.3080.8451.311 7.461
Old World H-clade taxa 3.9700.5492.607 5.458
New World H-clade taxa 3.7250.4962.531 5.248
South American clade 2.3370.4011.558 4.061
Hordeum comosum/chilense 2.0810.3631.072 3.824
Hordeum pusillum/stenostachys 1.5520.4400.811 3.672
Hordeum pusillum/erectifolium 1.2700.3780.402 3.067
Hordeum intercedens/flexuosum 1.8660.3640.923 3.309
Hordeum intercedens/euclaston 0.9970.2540.419 1.604
Hordeum patagonicum/pubiflorum 1.3520.3830.643 3.050
Hordeum muticum/patagonicum 2.1440.3471.567 4.102
Hordeum muticum/cordobense 1.0170.2320.421 1.705

Dispersal–vicariance analysis of distribution patterns for Hordeum and the outgroup taxa using DIVA (Ronquist, 1996, 1997) and restricting the ancient distribution to two geographical areas indicates a Eurasian origin of Hordeum and subsequent migration through Asia to North and South America (Figs 3b and S4). North America was reached again by two independent dispersals from South America (H. intercedens and H. pusillum). The analysis of the distribution patterns of the tetraploid species requires an additional Asian–North American colonization (by the Old World progenitor of the tetraploid H. jubatum), while both progenitors of the Central American H. guatemalense lived in North America. The paternal progenitors of the allotetraploid H. secalinum reached Europe where its maternal ancestor H. marinum occurs, either from Asia or from South America. South Africa was colonized from Europe either by H. secalinum or the common ancestor of H. capense and H. secalinum. Splitting South America in two regions (southern Argentina vs central Argentina to Peru) or not did not influence the outcome of intercontinental distribution patterns in the DIVA analyses.

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Phylogenetic analyses

The analysis of three combined nuclear DNA sequence sets for all diploid Hordeum species resulted for the first time in a phylogenetic tree with strongly supported backbone structures and resolution within the New World taxa of the genus. In general, statistical support of the clades (posterior probabilities and bootstrap values) was higher than in earlier separate analyses of the same loci (Komatsuda et al., 1999; Blattner, 2004) or in the combination of EF-G, DMC1, and chloroplast data (Petersen & Seberg, 2003). The general topology of the tree is entirely compatible with the postulated genome relationships (Fig. 3a) and earlier cytological (for references see von Bothmer et al., 1995), amplified fragment length polymorphism (AFLP) (El-Rabey et al., 2002), EF-G (Komatsuda et al., 1999, 2002), and ITS analyses (Blattner, 2004). Differences between the topology observed in the present study and the results of a separate analysis of the DMC1 locus alone (data not shown) concern only H. brevisubulatum and H. marinum, which group together with the basal New World taxon H. brachyantherum ssp. californicum, although with low statistical support. As this DMC1 topology contradicts the relationships deduced from independent nuclear data sets (see earlier), these differences are probably caused by the persistence of ancient polymorphisms and incomplete lineage sorting among DMC1 alleles in the young H-genome group (Maddison, 1997; Ting et al., 2000; Petersen & Seberg, 2003). Chloroplast data produced pronouncedly different tree topologies (Doebley et al., 1992; Nishikawa et al., 2002; Petersen & Seberg, 2003) when compared with the nuclear data. These incompatibilities were the reason for omitting chloroplast sequences from the combined data analysis here. The inconsistencies can mostly be attributed to lateral chloroplast transfer among some Hordeum taxa (Nishikawa et al., 2002) and particularly incomplete ancient lineage sorting (S. S. Jakob & F. R. Blattner, unpublished).

The occurrence of two ITS paralogs in the New World Hordeum clade and the reciprocal loss of one or the other paralog in some species results in seemingly contradicting phylogenetic topologies in this species group (Blattner, 2004) when analysed in a single data set (Fig. 1). Combining both ITS paralogs as separate loci with DMC1 and EF-G in a data matrix and coding the missing sequences as unknown character states resulted in a consensus tree with low resolution within the South American taxon group (data not shown). These problems were overcome by a separate analysis of data matrices containing only single ITS types and an integration of the phylogenetic information with an MRP supertree analysis. Supertree approaches are often used to combine data sets with differing taxon samples (Bininda-Emonds et al., 2002). In the case of bidirectional homogenization resulting in the loss of paralogous gene copies from several species, no possibility exists to recover the lost alleles. Phylogenetic analysis thus needs to combine the information from the separate loci (gene or locus trees) to arrive at the species’ phylogenies (Baum, 1992). The use of the recoded strict consensus trees from both data sets in MRP resulted in c. 250 000 most parsimonious trees, separating H. brachyantherum from the South American taxa, but with low resolution in the latter clade (data not shown). As this might be the result of under-representation of the data matrix (i.e. small number of matrix elements), all single most parsimonious trees instead of the consensus trees were recoded in the MRP matrix (Baum, 1992; Bininda-Emonds & Bryant, 1998). The analysis of these data substantially improved the resolution of the internal structure of the South American species (Fig. 2). The involvement of identical sequences for the Old World taxa in both data subsets resulted in pseudoreplication of these data in the MRP analysis (Bininda-Emonds, 2004). However, as only the relative phylogenetic positions of derived taxa with a single ITS paralog were of interest here, pseudoreplication of primary data in all other basal taxa is irrelevant for the resulting tree.

Hordeum consists of two major clades: (1) the primarily western Asian and Mediterranean species of the I- and Xu-genome groups, and (2) a clade formed by Eurasian H. marinum (Xa genome) and the large group of H-genome taxa (Fig. 3a). The basal branches in Hordeum are statistically well-supported, with the exception of the position of H. murinum, which in some analyses received only low bootstrap support (Fig. S1). However, in contrast to the separate analysis of ITS sequences (Blattner, 2004) neither of the analyses done here resulted in a sister-group relationship of H. murinum with the Xa/H-genome clade. In the H-genome clade the clear separation of the exclusively Asian taxa from the remaining New World taxa was highly supported (= 97% bs, 1.0 pp).

Within the closely related New World clade of the H-genome taxa the combination of nuclear DMC1, EF-G, and ITS sequences (Fig. 1), together with the use of an MRP supertree approach (Fig. 2) for the first time resulted in a relatively clear phylogenetic pattern. The North American H. brachyantherum was sister to the primarily South American species. Within this latter group H. chilense is sister to two geographically circumscribed clades, consisting of three southern species (H. comosum, H. patagonicum, and H. pubiflorum) and a northern group, respectively. The four mostly northern Argentinean species (Fig. 3a) group together with two taxa from North America. This clade, however, received only low statistical support (0.7 pp), although the two South American–North American species pairs within this group were well-supported (= 0.94 pp). The MRP supertree analysis also grouped H. cordobense and H. muticum with this northern clade, further supporting the geographical partition of the South American Hordeum species, as both these species occur in northern Argentina and H. muticum even reaches the Andes of Ecuador. This northern species group overlaps with section Anisolepis of von Bothmer et al. (1995), albeit with two differences: It includes H. erectifolium (section Stenostachys sensu von Bothmer et al., 1995) but excludes the basal South American H. chilense, as this species is sister to both the northern and the southern species group.

Internal transcribed spacer (Blattner, 2004), chloroplast (Nishikawa et al., 2002) and cytological analyses (Linde-Laursen et al., 1992) defined Asian H. roshevitzii and North American H. brachyantherum (or a close extinct relative) as progenitors of tetraploid H. jubatum. These data also support the close relationship of H. guatemalense and H. jubatum, with ITS data further indicating H. intercedens as a parental taxon involved in the formation of H. guatemalense (Blattner, 2004). The close relationship of H. capense and H. secalinum was long recognized. Some authors even treated these species as conspecific (von Bothmer et al., 1995; Baum & Johnson, 2003). The contribution of H. marinum as one parental taxon has been shown in several analyses (Doebley et al., 1992; Nishikawa et al., 2002; Baum & Johnson, 2003; Blattner, 2004; Petersen & Seberg, 2004), but contradictory hypotheses about the second parent were proposed based on chloroplast data (H. brachyantherum; Doebley et al., 1992), DMC1 (H. brevisubulatum; Petersen & Seberg, 2004), and ITS sequences (a basal taxon from the South American H-genome group; Blattner, 2004). A South American origin (close to H. muticum) of one parent of H. capense was postulated from the analysis of 5S rDNA loci (Baum & Johnson, 2003). However, these authors interpreted the absence of a specific 5S rDNA unit from H. secalinum as indication of only a distant relationship to H. capense, despite high sequence similarity at shared 5S rDNA loci. Owing to the dynamic nature of 5S rDNA loci (Schubert & Wobus, 1985; De Bustos et al., 1996; Taketa et al., 1999, 2001), the absence of a locus does not necessarily contradict a close relationship of the two species, as number of loci is variable even within narrow species groups. The combined data matrix for all species here supported the close relationship between H. capense and H. secalinum and suggested H. marinum and an H-genome species (Fig. S3) as progenitors. However, no decision about an Old or New World origin is possible based on the data presented here. The combination of ITS and EF-G data clearly supports a South American species as one progenitor of these taxa, but DMC1 data are inconsistent with a New World origin of the H-genome parent of both species (data not shown). As the DMC1 sequences of the tetraploids fall into the already contradictory marinum/brevisubulatum-clade (see above), no safe conclusion about the phylogenetic position of the H-genome parent is possible from this locus and the combined data. In the phylogenetic tree in Fig. 3a the ambiguity over the origin of the H genome is depicted by dashed lines.

Estimations of the clade ages

The calibration for all age estimates within Hordeum was based on the split between barley and wheat 13 MYA (Gaut, 2002). This age estimate is similar to a previous estimate of 10 MY by Wolfe et al. (1989). Using the 13 MY calibration point, PL resulted in an age of 12 MY for the basal node (crown age) in Hordeum (Blattner, 2004). This relatively old age of Hordeum is consistent with its position in the phylogeny of Triticeae, indicating an early split of the lineage leading to Hordeum from the remaining genera in Triticeae (Petersen & Seberg, 1997). The use of a secondary calibration point was chosen because no EF-G and DMC1 sequences were available for most Poaceae and their sister taxon Joinvillea. High ITS sequence divergence among these taxa would further impair model-based rate calculations (for an extended discussion of secondary calibration points see Hedges and Kumar, 2004). To account for possible uncertainties in the age of the basal node in Hordeum (Wolfe et al. 1998; Gaut, 2002) it was constrained for ages between 12.5 MY and 10 MY. These differences resulted in relatively uniform changes in the ages of nodes within Hordeum (c. 18%) and produced no inconsistencies with the biogeographical scenario below. The lack of Triticeae fossils, however, shifts all hard calibration points far back in time (Hsiao et al., 1999 and references therein), thus possibly introducing an unknown magnitude of systematic error. The ages calculated should therefore be regarded as rough minimum age estimations which help to relate biogeographical events in Hordeum to major geological events, climate changes or recent human impact. Moreover, the use of single-copy nuclear genes in molecular clock approaches can result in apparently too old ages for very young nodes in a phylogenetic tree because the coalescence of such alleles can reach deep down into the species history. For example, the age of the node within H. vulgare was calculated as 0.67 MY (Fig. 1). This age surely does not reflect the split of barley from its wild progenitor but most probably the split between two ancient DMC1 allele lineages, as EF-G and ITS sequences were identical in the two subspecies of H. vulgare and archaeological records date barley domestication to c. 10 000 years before present (Zohary & Hopf, 2000).

Biogeographical scenario

The congruence among trees based on different nuclear data sets and phylogenetic methods and the statistical support of the diploid backbone phylogeny of Hordeum provides a sound phylogenetic framework for biogeographic analysis. The different tree topologies resulting from bidirectional homogenization of two ITS paralogs (Blattner, 2004) concern exclusively South American lineages and thus do not influence the interpretation of the general biogeographical pattern of the genus. Dispersal–vicariance analysis (Ronquist, 1996, 1997) was used to estimate ancient distribution areas for the nodes in the Hordeum phylogeny (Fig. S4 and Table S1). One characteristic of DIVA is that it adds no costs for the loss of character states (i.e. the extinction of taxa in specific areas). Thus, it results in an increasing number of possible distribution areas towards the basal nodes in a tree when no constraints for the maximum number of distribution areas are imposed. Moreover, DIVA does not take into account the relative or absolute nodal ages in the tree and the relative geographical positions of the specified distribution areas. This, too, adds to the loss of meaningful information for the deeper nodes in a tree. DIVA provides, for example, an optimization of the basal nodes to the occurrence of Hordeum in all distribution areas, colonized by the genus today (Table S1). This is a very unlikely scenario with regard to continental positions 12 MYA. As DIVA provides the technically possible character optimizations for the nodes in a tree, the consideration of all additional information helps to exclude the unlikely character states. The biogeographic scenario for Hordeum developed below is thus only one of several possibilities provided by DIVA. It is, however, parsimonious as it prefers easily crossable landbridges over intercontinental long-distance dispersals, and includes information on age estimates to reconstruct the sequence of migration and intercontinental colonization.

The oldest diploid Hordeum groups occur in South-west Asia, thus pointing to this region as the probable center of origin of the genus (I; roman numbers refer to the dispersals depicted in Fig. 3), although range shifts of the taxa due to climate changes during the last 12 MY are possible. This area assignment is in accord with the proposed Eurasian origin of Triticeae (Hsiao et al., 1999). From South-west Asia migration took place into the western Mediterranean and north-western Europe (H. marinum). A route to the east (H-genome clade) resulted in the colonization of Central and East Asia (II, III) and, via Beringia, of North America (IV). Diploid H. brachyantherum today occurs only in California. The autotetraploid cytotype of this species, however, is disjunctively distributed from California northward along the Pacific rim of North America to coastal Kamtchatka and in a small area in Newfoundland (von Bothmer et al., 1995), possibly indicating a formerly wider distribution of the species. From North America Hordeum reached South America (V), where H. chilense is sister to all other taxa. The phylogenetic data indicate two independent dispersals back to the northern hemisphere, resulting in the colonization of North America by the South American progenitors of H. pusillum (VI) and H. intercedens (VII). Surprisingly, the sister of the widespread North American H. pusillum is the ecologically narrow endemic H. erectifolium (von Bothmer et al., 1995). This provides another example for a major shift in ecology in plants after colonization of a new continent (Morrell et al., 2000).

The allotetraploid H. jubatum combines a North American brachyantherum-like genome with an Asian genome most similar to H. roshevitzii (Linde-Laursen et al., 1992; Blattner, 2004). The occurrence of this Asian genome in the mainly North American H. jubatum necessitates a second traverse of Beringia (VIII). The close relationship of H. guatemalense with the widespread North American H. jubatum and the southern Californian H. intercedens (Doebley et al., 1992; Nishikawa et al., 2002; Blattner, 2004) indicates a colonization of Central America from the north (IX). The formation of H. secalinum in Europe, which involved either a Central Asian or a South American taxon (X) together with H. marinum, could not be unambiguously clarified by the molecular data. Although rDNA (Baum & Johnson, 2003; Blattner, 2004) and combined EF-G/ITS data strongly support a South American origin of one of the H. secalinum/H. capense progenitors, EF-G does not provide sufficient resolution in this part of the tree, and DMC1 contradicts this hypothesis (Petersen & Seberg, 2004). Furthermore, a transatlantic dispersal from the Southern to the Northern Hemisphere is unusual and, to my knowledge, has not been documented for other plant species. Unfortunately, chloroplast data cannot contribute to the solution of this question, as H. marinum is the maternal parent (Nishikawa et al., 2002) of the allopolyploid. The close relationship of H. secalinum and H. capense indicates the colonization of the Cape Province from Europe after the formation of H. secalinum or by the common ancestor of both these species (XI).

The geographical expansion of Hordeum is mostly restricted to the H-genome clade and started c. 6 MYA, long after Gondwana and Laurasia broke up, and clearly before the spread of humans across the world. Thus, the intercontinental distribution discussed here is neither connected with the occurrence of ancient Hordeum lineages in Gondwana, as speculated by Baum & Johnson (2003), nor with recent human influences on potential habitats or direct diaspore dispersal by humans. Plant migration between Asia and North America via Beringia is not unlikely for temperate and temporarily also for subtropical taxa (Tiffney, 1985). The present distribution of H. jubatum and H. brachyantherum in Alaska and adjacent Siberia supports the existence of this migration route and, furthermore, an occasionally continuous distribution of Hordeum species across Beringia. Dating of the split between New and Old World taxa (6–5 MYA) places this event before the start of the Quaternary climatic cycles (c. 2.5 MYA), which periodically closed Beringia for temperate plants and thus probably isolated Asian from New World Hordeum populations. The split between Old World and New World taxa is therefore interpreted as a vicariance event (Fig. 3a) caused by climatic changes that separated populations and prevented gene flow across Beringia by forcing the species into more southerly habitats. Vicariance also seems possible for the separation of Central American H. guatemalense from its North American progenitors, as during the ice ages temperate to dry climatic conditions reached far more south into Central America than today.

The next step in the range expansion of Hordeum involved the colonization of southern South America, and dates back c. 4 MY. The Central American landbridge was already in place (Graham, 2003) when the genus had to cross this area on its way to the south. Thus, two scenarios can be proposed. One involves southward migration of an H. brachyantherum-like species along the western American mountain ridges, the other long-distance dispersal between California and southern Chile. Disjunctive distributions between California and Chile are not uncommon (Raven, 1963; van Heusden & Bachmann, 1992; Morrell et al., 2000; von Hagen & Kadereit, 2001) and are thought to be mostly mediated by birds migrating along the west coast of the Americas. The basal taxon in the South American clade is H. chilense, sharing its distribution in summer-dry Chilean areas with several other taxa of North American origin. The ecology and distribution areas of extant Hordeum species together with the phylogenetic data presented here support the long-distance dispersal alternative in Hordeum. In case of stepwise southward migration the basal South American taxa would be expected to occur somewhere along the way in Central America or the Andes. However, the only South American high-altitude taxon occurring as far north as Ecuador is H. muticum. This taxon belongs to the northern clade of the South American taxa and possesses only one of the two ITS types occurring in South America (Blattner, 2004). This loss of type-2 ITS is a derived character state in South American Hordeum species, making a basal position of H. muticum highly unlikely. By contrast, H. chilense possesses both ITS types, which further supports the basal position of this species in the South American clade.

The biogeographic scenario for the South American species thus would involve initial long-distance dispersal from California to Chile and an expansion of the distribution area to the east of the Andes. From there, two migration routes could be inferred by the phylogenetic data. One group spread to the south and today occurs mainly in southern Patagonia, Tierra del Fuego and the southern Andes (H. comosum, H. patagonicum and H. pubiflorum), while a second lineage reached northern Argentina and Uruguay, and colonized the northern Andes. This intracontinental migration pattern of Hordeum, starting after long-distance dispersal from Chile and reaching secondarily northern Andean habitats in Peru is paralleled by the migration route of South American Microseris pygmaea (Asteraceae), for which a similar distribution pattern was found (Lohwasser et al., 2004). In the course of range expansion and the colonization of diverse South American habitats rapid speciation in Hordeum started c. 2 MYA. This radiation possibly is related to the Quarternary climatic oscillations (Blattner, 2004).

Two independent and relatively young reintroductions (c. 1 MYA) of South American Hordeum species to North America might also have been mediated by migrating birds. Species such as the buff-breasted sandpiper (Tryngites subruficollis) or the American golden plover (Pluvialis dominica) winter in Argentina and Uruguay and traverse Californian coastal habitats and the Great Plains of North America on their way to the breeding grounds in the high Arctic (del Hoyo et al., 1996; Global Register of Migratory Species, http://www.groms.de). Although this mechanism is speculative, the preferential occurrence of the disjunctive South–North American Hordeum species pairs in temporary wet habitats along ditches, riverbanks, and at lake shores certainly promotes epizoochory, where spikelets scattered in mud become attached to the legs of feeding waterbirds (pers. obs.). These habitats are the only sources of open water and feeding grounds for these birds in an otherwise semiarid to arid landscape of the Patagonian steppe. Repeated long-distance dispersal between North and South America is not unusual, as it was also found in the Gentianaceae genus Halenia (von Hagen & Kadereit, 2003), although in the case of Halenia, migration via stepping-stone habitats was proposed.

An explanation for long-distance dispersal from South America to Europe is much harder to find, if one H. secalinum progenitor should indeed belong to the New World clade. Even here bird dispersal seems to be the best explanation. During spring in the northern hemisphere, birds wintering in Patagonia can regularly be found on European coasts, carried away by storms on their way from South to North America (del Hoyo et al., 1996). They might, thus, provide a one-way connection between South America and Europe.

The Mediterranean basin and the Cape Province share similar climatic conditions and several plant families and genera (Raven, 1963). In the light of the dispersal ability of plants (Wagner & Funk, 1995; Vijverberg et al., 1999; Wright et al., 2000; Davis et al., 2002; Fuertes-Aguilar et al., 2002; Coleman et al., 2003; this study), long-distance dispersal is the most parsimonious explanation for the occurrence of Hordeum species at the northern and southern rim of the African continent. These regions are connected by migrating birds such as red knot (Calidris canutus) and corncrake (Crex crex), which both occur in H. secalinum habitats in Europe and the Mediterranean and winter in the Cape Province's habitats of H. capense.

Conclusions

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Hordeum provides an example for unusually pronounced dispersal dynamics of plants influencing the composition of continental biotas. The genus initially evolved in Eurasia and reached its present distribution area by at least six intercontinental exchanges, involving vicariance (twice Eurasia–North America) and long-distance dispersal (North America–South America, twice South America–North America, Europe–South Africa and possibly New World–Europe). Intercontinental long-distance dispersal is a very important factor, shaping the extant distribution pattern of Hordeum, although establishing populations upon arrival is probably harder within long-term coevolving plant communities on continents (Naeem et al., 2000) than in young and less stable island floras. On the global scale, invasive weeds show that under suitable climatic and ecological conditions, a small proportion of newly arriving taxa are able to establish a bridgehead and start the colonization of new areas (Sakai et al., 2001). Even if several successful intercontinental long-distance colonizations within one genus are highly unlikely, continuous diaspore input eventually will result in dispersal of plants to, presumably, all areas on earth. One should bear in mind that all biogeographical analyses are severely biased towards surviving species. All others, titanicking in the oceans, remain undetected.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

I thank R. von Bothmer, J. Kadereit, A. Schwarzbach, and I. Stehlik for valuable discussion or comments on an earlier version of the manuscript, and G. Petersen and O. Seberg for sharing sequence data before publication. This study was funded by grant Bl 462/3 from the Deutsche Forschungsgemeinschaft (DFG) within SPP 1127 ‘Biological Radiations’.

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  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information
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Supporting Information

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Fig. S2 Maximum parsimony trees resulting from the inclusion of either type-1 or type-2 ITS paralogs in the combined DMC1/EF-G/ITS data matrix from diploid Hordeum species.

Fig. S3 Parsimony and neighbor-joining trees derived from the analyses of the combined data matrices of DMC1, EF-G, and ITS, including sequences from the tetraploid species Hordeum capense and H. secalinum together with diploid Hordeum species.

Fig. S4 and Table S1 Dispersal–vicariance analysis reconstruction of ancient distribution areas of Hordeum species and their progenitor taxa based on the phylogeny of extant diploid Hordeum species and outgroups from Triticeae and Bromeae.

FilenameFormatSizeDescription
nph1610figS1.pdf15KSupporting info item
nph1610figS2.pdf13KSupporting info item
nph1610figS3.pdf18KSupporting info item
nph1610figS4.pdf14KSupporting info item
nph1610tableS1.pdf23KSupporting info item