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(American Journal of Botany. 2009;96:507-518.) doi: 10.3732/ajb.0800216 © 2009 Botanical Society of America, Inc. |
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Systematics and Phytogeography |
2 Department of Molecular Biology and Biochemical Engineering, Pablo de Olavide University, ctra. de Utrera km 1 41013 Sevilla, Spain 3 Botanic Garden of Madrid, CSIC, Pza. Murillo n° 2 28014 Madrid, Spain
Received for publication 27 June 2008. Accepted for publication 2 October 2008.
ABSTRACT
Oligomeris linifolia constitutes one of the few examples of intercontinental disjunctions at the species level between the arid regions of the Old World and SW North America. The status of the American populations has been obscure, with some authors considering the populations to be introduced, whereas others believe them to be native. To clarify these conflicting opinions, we performed phylogeographic analyses using nuclear ribosomal ITS and plastid trnL-F and rps16 sequences to infer the origin of the disjunct American populations. Two independent molecular clock approaches based on ITS and cpDNA sequences (rbcL, matK, trnL-F) were used to estimate a divergence time of O. linifolia. Low levels of sequence divergence and estimates of relatively recent splits of Oligomeris lineages disagree with the vicariance hypotheses traditionally suggested to account for New–Old World disjunctions. In addition, significant genetic differentiation of American populations does not indicate a recent anthropogenic introduction. Morphological uniformity and the sharing of haplotypes between disjunct populations, together with the molecular clock results, suggest that a long-distance dispersal event from the Old Word to SW North America may have taken place during the Quaternary, in spite of limited dispersal mechanisms in Oligomeris.
Key Words: arid regions • biogeography • intercontinental disjunction • long-distance dispersal • molecular clock • Oligomeris • Resedaceae • vicariance
One of the most fascinating aspects of plant biogeography has been the study and interpretation of intercontinental disjunctions (e.g., Raven, 1972
; Thorne, 1972; Givnish and Renner, 2004). Many species occurring in arid regions of the world have broad disjunctions, which have been the subject of past and current researches (e.g., Goldblatt, 1978; Liston et al., 1989; Thulin, 1994; Liston and Kadereit, 1995; Fritsch, 2001; Coleman et al., 2003; Beier et al., 2004; Meyers and Liston, 2008). These studies have chiefly focused on determining whether these disjunctions are the result of ancient vicariance, long-distance dispersal, or anthropogenic introduction.
Some plant groups from arid areas have a disjunct distribution between the Old World and southwestern North America (e.g., Thulin, 1994; Fritsch, 2001; Beier et al., 2004; Hohmann et al., 2006). This pattern has repeatedly been found at the genus level (e.g., Thorne, 1972; Raven and Axelrod, 1978; Stebbins and Day, 1967; Thulin, 1994), although it is very rare at the species level. Three classical colonization hypotheses involving vicariance have been proposed to account for such disjunctions: (1) the existence of a Beringian bridge between Asia and North America during Miocene, ca. 20 million years ago (Ma) (Stebbins and Day, 1967; Tiffney, 1985a; Mummenhoff et al., 2001; Hohmann et al., 2006); (2) the so-called "Madrean-Tethyan" belt of Tertiary sclerophyllous vegetation from North America to Central Asia, from the late Eocene to the end of the Oligocene, ca. 40–25 Ma (Axelrod, 1975); and (3) the boreotropics theory, which postulates a land bridge in the North Atlantic between North America, Europe, and Africa during the Eocene thermal maxima, in which thermophilic vegetation reached latitudes up to 50°N, ca. 54–35 Ma (Tiffney, 1985b; Fritsch, 2001; Davis et al., 2002; Beier et al., 2004). Alternatively, long-distance dispersal has been proposed to explain this pattern of intercontinental disjunction, although to a lesser extent than vicariance, and has usually referred to disjunctions at the specific level (Raven, 1971; Thorne, 1972; Liston et al., 1989; Liston and Kadereit, 1995; Coleman et al., 2001, 2003; Shaw et al., 2003; Meyers and Liston, 2008). Lastly, population disjunction as the result of post-Columbian anthropogenic introductions has received attention by some researchers (Bassett and Baum, 1969; Raven, 1971; Raven and Axelrod, 1978). Most alien species in southwestern North America were introduced by Spanish settlers during the 18th and 19th centuries (Bossard et al., 2000), although new introduced species have continuously been reported since then (Rejmánek and Randall, 1994).
A few, but hardly numerous examples of species with an Old World–southwestern North America disjunction, as the result of nonanthropogenic introduction, have been documented. For example, the presence of Senecio mohavensis subsp. mohavensis in North America has been postulated to be the result of a fairly recent long-distance dispersal (c. 0.15 Ma) from southwestern Asia (Liston et al., 1989; Liston and Kadereit, 1995; Coleman et al., 2001, 2003). Likewise, the disjunction found in Plantago ovata has been explained by a relatively recent (0.2–0.65 Ma) long-distance dispersal from the Old World to North America (Meyers and Liston, 2008). In addition, Shaw et al. (2003) have proposed a Quaternary long-distance dispersal as the most plausible explanation for the Mediterranean–western North American disjunction found in three moss species (Claopodium whippleanum, Dicranoweisia cirrata, and Scleropodium touretti).
Species of the Resedaceae (6 genera, c. 85 species) are mainly distributed in temperate areas of the Old World and are mostly centered around the Mediterranean basin (see maps in Culham, 2007; Martín-Bravo et al., 2007). Oligomeris Cambess. is a monophyletic genus (Martín-Bravo et al., 2007) comprised of three species typically found in desert and arid areas of the Old and New World (Abdallah and de Wit, 1978). Two species [O. dipetala (Aiton) Turcz. and O. dregeana (Müll. Arg.) Müll. Arg.] are narrow endemics in southern Africa. Conversely, O. linifolia (Vahl) J. F. Macbr. is a widespread species found in arid regions of the Old World, from northern Africa to southwestern Asia, and in the deserts of southwestern North America (Fig. 1). Additionally, O. linifolia has recently been reported from southern China (Lianli and Turland, 2001), which may be an additional disjunction for the species.
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; Abdallah and de Wit, 1978; Martín-Bravo et al., in press). In contrast, the native status of O. linifolia in the New World has been controversial. Some authors have considered it a post-Columbian introduction (Bentham and Hooker, 1865; Watson, 1876; Raven and Axelrod, 1978; Wiggins, 1980), while others have regarded it as the only indigenous Resedaceae species in America (Torrey and Gray, 1838; Jepson, 1936; Stebbins and Major, 1965; Stebbins and Day, 1967; Thorne, 1972, 1986; Correll and Johnston, 1979; Halvorson, 1992; Daniel, 1993). Some authors have even considered North American populations a distinct species (North American O. linifolia vs. Old World O. subulata Delile ex Webb; Stebbins and Major, 1965; Stebbins and Day, 1967) or a distinct genus (Ellimia ruderalis Nuttal in Torrey and Gray, 1838). The view that O. linifolia is indigenous to North America is suggested by its restricted distribution, both geographically and ecologically, to arid regions of southwestern North America. There, it occupies undisturbed habitats similar to those where it is found in the Old World. Thus, O. linifolia does not match the expected pattern for most introduced species, which are usually generalist and become widespread in disturbed habitats (Liston et al., 1989), as observed for Reseda species introduced in North America. In the last years, there has been an increase in the governmental initiatives for the conservation of biodiversity. These usually include programs that aim to reduce the negative effects of alien invasive species on the native flora by means of their eradication or control. Therefore, it would be important to assess the origin of species such as O. linifolia whose indigenous status in a region is uncertain.
DNA sequences have been used to help determine explicit biogeographic hypotheses (e.g., Coleman et al., 2003; Shaw et al., 2003; Dick et al., 2007; Meyers and Liston, 2008). To determine whether the intercontinental disjunction found in O. linifolia is the result of a natural colonization event, we analyzed nuclear ribosomal ITS (internal transcribed spacer) and plastid rbcL, matK, trnL-trnF, and rps16 sequences. Specifically, we addressed the following objectives: (1) to determine the origin of the disjunct O. linifolia American populations (i.e., vicariance, long-distance dispersal, or anthropogenic introduction); (2) to estimate divergence times of Oligomeris by means of a molecular clock approach; (3) to relate the intercontinental disjunction to the biology of the species.
MATERIALS AND METHODS
Sampling, DNA extraction, amplification, and sequencing
A total of 24 populations of O. linifolia from the Old (14) and New (10) World, representing the species distribution, were included in the phylogeographic analyses, based on nuclear ITS and plastid trnL-F/rps16 sequences (Appendix 1). Because the majority of samples were obtained from herbarium material, only one individual per population was included. Five samples of O. dipetala and O. dregeana were also included. Two species of Reseda sect. Glaucoreseda (R. battandieri, R. complicata), the sister group of Oligomeris (Martín-Bravo et al., 2007), were included as outgroup taxa. Nine ITS and three trnL-F sequences were obtained from a previous molecular study (Martín-Bravo et al., 2007). Total genomic DNA was extracted from silica-dried material, fresh tissue from cultivated plants and herbarium specimens (BM, CAS, EA, HBG, HUJ, LD, RNG, RSA, UC, UCR, UPOS, UPS, WAG, WU, Z), using a Dneasy Plant Mini Kit (Qiagen, Valencia, California, USA).
The ITS and trnL-F regions were amplified and sequenced as detailed by Martín-Bravo et al. (2007). The rps16 intron was amplified using rpsF and rps2R primers as described by Oxelman et al. (1997), but with lower annealing temperatures (54–55°C).
Two data sets (plastid rbcL-matK-trnL-F, nuclear ITS; Appendix 1) were used to estimate divergence times of O. linifolia and related lineages (Oligomeris, Resedaceae). Specifically, 49 Resedaceae accessions were included for this analysis: 22 of Oligomeris taxa (five of O. linifolia from the Old World and eight from the New World; six of O. dipetala; and three of O. dregeana), 19 accessions of five Reseda species, and four accessions each of Caylusea and Sesamoides (Appendix 1). Sixty accessions from other Brassicales taxa (Caricaceae, Moringaceae, Bataceae, Koeberliniaceae, Tovariaceae, Pentadiplandraceae, Gyrostemonaceae, Capparaceae, Forchhammeria, Cleomaceae, Brassicaceae; Appendix 1) were primarily taken from the GenBank. These sequences were mainly obtained in previous systematic studies of Brassicales (e.g., Rodman et al., 1993; Hall et al., 2002, 2004; Martín-Bravo et al., 2007).
Standard primers were used for the amplification and sequencing of the matK (trnK-3914F, matK-1412R [ Johnson and Soltis, 1995 ]; trnK-710F [ Koch et al., 2001 ]; trnK-570F [ Samuel et al., 2005 ]; matK-8R [ Ooi et al., 1995 ]) and the rbcL (1F-724R, 636F-1460R [ Savolainen et al., 2000 ]) regions. Amplification of rbcL and matK used a 5-min pretreatment at 95°C; followed by 35 cycles of 1 min at 95°C, 0.5–1 min at 50–57°C, 1–2 min at 72°C; and a final extension of 7 min at 72°C.
Phylogenetic and haplotype data analyses
We manually aligned two matrices of 30 sequences each: nuclear (ITS) and plastid (trnL-F/rps16) data sets. For the plastid data set, gaps were treated as missing data as well as coded as additional characters, with the exception of mononucleotide repeat units (poli-T and poli-A), which are considered to be highly homoplasic (Kelchner, 2000). Maximum parsimony (MP) and Bayesian inference (BI) analyses were performed, as in Martín-Bravo et al. (2007). Congruence of the ITS and trnL-F/rps16 data sets was assessed using a Hompart test for matrices (100 replicates) and Kishino–Hasegawa (KH) and Shimodaira–Hasegawa (SH) tests for topology (1000 replicates each) as implemented in the program PAUP* version 4.0b10 (Swofford, 2002).
Statistical parsimony analyses of Oligomeris haplotypes were performed using the program TCS version 1.21 (Clement et al., 2000) with a 95% parsimony connection limit. We estimated completeness of the ribotype (ITS) and haplotype (trnL-F/rps16) sampling using a Stirling probability distribution as described by Dixon (2006).
Estimating divergence times
We used two independent approaches to infer divergence times of Oligomeris lineages. The first was a penalized likelihood approach using two data sets, one of nuclear (ITS) and one of plastid (rbcL-matK-trnL-F) sequences. For this analysis, we used the tree topology and branch lengths obtained from the BI phylogenetic analyses. Carica papaya (Caricaceae) and Moringa oleifera (Moringaceae) were used as the outgroup species for the analyses of both data sets (rbcL-matK-trnL-F, ITS). We evaluated rate heterogeneity among lineages by means of a Langley and Fitch (LF) test (Langley and Fitch, 1974). The null hypothesis of molecular clock (constant rate) was rejected for both the ITS and plastid data sets. As a result, divergence times were estimated by applying a penalized likelihood method (Sanderson, 2002) with the truncated Newton algorithm, as implemented in the rate smoothing program r8s version 1.71 (Sanderson, 2004). We obtained the smoothing parameter for this analysis by a cross-validation procedure, which involves pruning terminal branches and predicting the rate along that branch. We pruned the extra outgroup (Carica papaya in both data sets) as recommended in the r8s manual. Penalized likelihood search parameters included five initial and five perturbed restarts. The best smoothing parameter resulting from the cross-validation was 100 000 for rbcL-matK-trnL-F data set and 10 for the ITS data set. Standard errors of divergence time estimates were obtained using a nonparametric bootstrap procedure (Baldwin and Sanderson, 1998), which involves the generation of 1000 resampled data matrices with the SEQBOOT program implemented in the program PHYLIP version 3.67 (Felsenstein, 2005). Relative divergence times were converted into absolute time units using calibration points. Due to the lack of macrofossil record in Resedaceae, we used divergence ages of other families within the Brassicales, as proposed by Wikström et al. (2001). This constrained the corresponding nodes with a minimum and maximum age (Fig. 2). Due to the low level of sequence divergence, we only used a subset of O. linifolia populations in the penalized likelihood analyses, representing the species distribution (Old/New World) and sequence diversity found in our sampling (Fig. 2).
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, using nucleotide sequence divergences of ITS and trnL-F/rps16 sequences between O. linifolia populations. Because no estimates of mutation rates in Resedaceae are known, we used Brassicaceae (placed in the core of order Brassicales as does Resedaceae) ITS and noncoding cpDNA nucleotide substitution rates. These mutation rates, calibrated with fossil data, allowed us to perform an approximate molecular clock. Mummenhoff et al. (2004) estimated that 1% K2P sequence divergence in Lepidium corresponded to 0.6–1.1 Ma for the ITS region and to 1.3–2.8 Ma for cpDNA. Such values seem reasonable because they are similar to others published for different plant groups (Richardson et al., 2001; Mummenhoff et al., 2004; Kay et al., 2006). However, phylogenetic relatedness may not be an appropriate method for choosing mutation rates from the literature, due to the considerable molecular variation that can exist within a single family (Kay et al., 2006). As a result, we also performed a conservative approach by using the slowest published rates (0.076% divergence/Ma for ITS sequences [Wen and Shi, 1999] and 0.2% divergence/Ma for cpDNA sequences [ Wolfe et al., 1987 ]). This approach would overestimate divergence times and therefore would favor acceptance of vicariance hypotheses (Dick et al., 2007). PAUP* was used to calculate pairwise sequence divergences (K) between O. linifolia populations, both under Kimura’s two parameter model (K2P) and under the models selected by the program MrModeltest version 1.1b (Nylander, 2002): HKY85 for ITS and F81 for trnL-F/rps16. If observed divergences (Kobs) between Old and New World populations were below levels expected by the vicariance hypotheses (Kexp), corresponding to less than 20 Ma of genetic isolation, these were rejected in favor of a relatively recent long-distance dispersal or anthropogenic introduction. RESULTS
Sequence variation and haplotype analysis
In Oligomeris, the ITS region was 637 base pairs (bp). Plastid sequence lengths were 728–730 bp for trnL-F and 830–854 bp for rps16. Within the ITS matrix, 19 variable sites were detected within Oligomeris (three in O. linifolia), of which eight were parsimony-informative (one in O. linifolia). Visual inspection of O. linifolia ITS chromatograms revealed no nucleotide additivities. Four O. linifolia nuclear ribosomal types (ribotypes) were distinguished within the ITS matrix (Figs. 1, 3A; Table 1). One ITS ribotype is distributed across the entire species range and was present in most populations (R1; 19 Old and New World populations, 82% of all populations). Two ITS ribotypes were represented by single individuals from the Old World (R3, Yemen-Hadramaut; R4, Israel). A fourth (R2) was exclusive to the New World (North Baja California and San Nicolas Island populations).
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Within the plastid trnL-F/rps16 matrix, 11 sites were variable within Oligomeris (four in O. linifolia), seven of which were parsimony-informative (one in O. linifolia). Five trnL-F/rps16 haplotypes were found in O. linifolia (Figs. 1, 3B; Table 1), of which only one haplotype (H1) was found in both Old and New World populations (18; 78% of all populations). The other four haplotypes were exclusive to two American populations (H2: Arizona; H3: California-Imperial County) and three Old World populations (H4: Yemen-Hadramaut; H5: Argelia and China). The application of Dixon’s (2006) method revealed a probability of over 90% that all ribotypes and haplotypes have been sampled. As a result of coding indels (two within the trnL-F region and one within the rps16 intron; Table 1), three additional haplotypes from the New World were identified in four populations (H6: Coahuila and Texas-Starr County; H7: Guadalupe Island; H8: San Nicolas Island). In total, plastid DNA variation accounted for a total of five haplotypes exclusive to the New World when coding indels. No variable sites were found within the three rbcL-matK accessions of O. linifolia (one population from the Old World and two from the New World; Fig. 2A, Appendix 1).
The analysis of the plastid trnL-F/rps16 data set, without coding indels, reveals genealogical relationships between haplotypes, as depicted by TCS, that are remarkably similar to those retrieved from the ITS data set (Fig. 3B). The most frequent and widely distributed haplotype (H1; 18 populations) is placed in an internal position and shows five mutational connections, which link it to the two Oligomeris species from southern Africa and to the four other O. linifolia tip haplotypes (H2: Arizona; H3: California-Imperial County; H4: Yemen-Hadramaut; H5: Argelia and China). Coding indels (three) revealed three additional haplotypes (H6, H7, H8), in agreement with previous network topologies, with the exception of the Oligomeris species connections (Fig. 3C). Haplotype 6 (Coahuila and Texas-Starr County) has two connections, which link it to O. dipetala and to H1. Interestingly, the insular H7 haplotype (Guadalupe Island) is connected with H1 and with the tip H8 (San Nicolas Island). It should be noted, however, that the codification of two indels (indicated with asterisks in the network, Fig. 3C), is homoplasic in haplotypes H6 and H8. This means that the same mutational step had to be mapped onto the network more than once.
Phylogenetic analyses
Phylogenetic reconstructions of MP analyses of the ITS matrix (aligned length 638 bp) retained two optimal trees with 30 steps (CI = 0.94, RI = 0.97, RC = 0.94; results not shown). The trnL-F/rps16 matrix (aligned length 1593 pb) produced a single tree of 27 steps (CI = 1, RI = 1, RC = 1; not shown). Phylogenetic analyses of plastid and nuclear matrices retrieved very similar topologies and Hompart and KH-SH tests showed that both data sets were congruent (p = 1.00, p > 0.07, respectively). Therefore, we also conducted the MP and BI analyses of a combined trnL-F/rps16-ITS matrix (30 sequences), which increased branch support for all clades. The MP analysis of the combined trnL-F/rps16-ITS matrix (aligned length 2231 bp) retained two optimal trees with 57 steps (CI = 0.98, RI = 0.99, RC = 0.97; not shown).
The hierarchical likelihood ratio test (hLRT) and the Akaike information criterion (AIC), as implemented in MrModeltest, retrieved different models of sequence evolution for the ITS-1 (K80 and SYM, respectively) and the ITS-2 (JC and HKY) spacers. Therefore, a character partition was implemented in the ITS matrix for the BI analyses. On the other hand, both hLRT and AIC retrieved F81 as the simplest model of sequence evolution for the trnL-F/rps16 matrix. Tree topology and clade support obtained with the two different approaches were identical.
BI majority rule consensus trees obtained from the analyses of the single (ITS, trnL-F/rps16; not shown) and combined matrices (Fig. 4) are consistent with the strict consensus trees of the MP analyses. Accessions of Oligomeris form a strongly supported monophyletic group irrespective of the data set used or analysis performed (100% PP; 100% BS). Oligomeris linifolia is also monophyletic with moderate to strong support in the plastid trnL-F/rps16 (76% PP; 64% BS) and ITS data set analyses (100% PP; 94% BS). Additionally, support increased in the combined analysis (100% PP; 98% BS; Fig. 4). Similar results were obtained when analyzing the combined rbcL-matK-trnL-F matrix used for the penalized likelihood approach (Oligomeris: 100% PP; 82% BS; O. linifolia: 100% PP; 69% BS; Fig. 2A). These results are in agreement with a previous molecular study (Martín-Bravo et al., 2007), which, however, did not include any O. linifolia sample from America. Within O. linifolia, most accessions are placed unresolved in the phylogenetic trees, due to the low level of sequence divergence (Fig. 4). Only two pairs of accessions (North Baja California and San Nicolas Island; Argelia and China) form clades in the combined analysis (Fig. 4).
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), the split of the Resedaceae may be dated to the Miocene (12.6 ± 0.85 Ma, rbcL-matK-trnL-F; 10.48 ± 1.82 Ma, ITS; Fig. 2, Table 2). Both chronograms placed the divergence of Oligomeris during the Lower Pleistocene (1.5 ± 0.47 Ma, cpDNA; 0.97 ± 0.37 Ma, ITS) and that of O. linifolia during the Upper Pleistocene (0.18 ± 0.13, cpDNA; 0.087 ± 0.063 Ma, ITS) (Fig. 2, Table 2).
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1.52 for ITS; Kexp 4 for trnL-F/rps16), as well as using rates from the Brassicaceae (Kexp 18.18 for ITS; Kexp 7.14 for trnL-F/rps16). The application of the latter mutation rates to the maximum levels of sequence divergence between O. linifolia lineages (Kobs = 0.29 for ITS; Kobs = 0.13 for trnL-F/rps16) results in an estimated maximum age of disjunction between 0.17–0.32 Ma (ITS) and 0.17–0.36 Ma (cpDNA).
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Origin and time estimates for the intercontinental disjunction
Our molecular results do not suggest vicariance as an explanation for the intercontinental disjunction of O. linifolia. Very low levels of genetic differentiation were observed between American and Old World conspecific populations. These values are far below those expected by any of the three vicariance hypotheses (Table 3). Likewise, this result is also supported by the penalized likelihood approach (Table 2), which suggests a relatively recent origin of O. linifolia (0.18 ± 0.13 Ma, cpDNA; 0.087 ± 0.063 Ma, ITS), the genus Oligomeris (1.5 ± 0.47 Ma, cpDNA; 0.97 ± 0.37 Ma, ITS), as well as the familiy Resedaceae (12.6 ± 0.85 Ma, cpDNA; 10.48 ± 1.82 Ma, ITS). At present, the only fossil record for family Resedaceae is pollen from Miocene (c. 5.3–1.8 Ma) sediments from the Sahara (Beucher, 1975), in agreement with our estimated divergence times.
Our results are not unexpected considering morphological differentiation and palaeogeological events. Land bridges between North America and the Old World postulated by different biogeographic theories (Beringian bridge, Madrean-Tethyan belt, boreotropical land bridge) date back at least to the Miocene (ca. 20 Ma). These high-latitude land bridges may have allowed an exchange of taxa between continents until the late Tertiary or even the Quaternary (e.g., Tiffney, 1985b; Mummenhoff et al., 2001; Gladenkov et al., 2002). However, at this time, plant exchange was likely limited to cool-tolerant and boreal taxa, unlike thermophilic lineages like Oligomeris (Tiffney and Manchester, 2001; Davis et al., 2002). Therefore, no palaeogeological/climatical evidence exists for a connection between the arid regions of the Old–New World during the Pleistocene (Liston et al., 1989; Coleman et al., 2003). In addition, morphological uniformity within O. linifolia (Jepson, 1936; Abdallah and de Wit, 1978; Daniel, 1993; Martín-Bravo et al., in press) and the sharing of the most frequent and widespread ITS (R1) and cpDNA (H1) sequences between populations of the Old World and North America (Fig. 1) do not suggest a disjunction caused by vicariance.
Two alternative hypotheses remain as the most likely explanations for the disjunction: intercontinental dispersal event or introduction by man. One ITS ribotype and several cpDNA haplotypes were exclusively found in the New World populations (Fig. 1). Therefore, based on the genetic differentiation of American populations, a post-Columbian anthropogenic introduction (Bentham and Hooker, 1865; Watson, 1876; Raven and Axelrod, 1978; Wiggins, 1980) appears unlikely. Taking into account the distribution of the other species of Oligomeris (O. dipetala, O. dregeana) and the family in the Old World (see maps in Culham, 2007; Martín-Bravo et al., 2007), all the evidence presented led us to suggest that a long-distance dispersal from the Old World to North America appears the most likely explanation for this intercontinental disjunction. The application of an approximate molecular clock based on Brassicaceae substitution rates (Mummenhoff et al., 2004) dated back the long-distance dispersal event to late Quaternary times, with a maximum of 0.17–0.36 Ma. This result is congruent with the Upper Pleistocene origin of O. linifolia estimated by the penalized likelihood approach (0.18 ± 0.13, cpDNA; 0.087 ± 0.063, ITS; Fig. 2, Table 2). The disjunction of O. linifolia is strikingly similar to other species showing the same biogeographic pattern, not only in the estimated age of the long-distance dispersal (Senecio mohavensis, c. 0.15 Ma [Coleman et al., 2003]; Plantago ovata, 0.2–0.65 Ma [Meyers and Liston, 2008]), but also in the direction of dispersal (from the Old to the New World). While vicariance has been frequently suggested as an explanation for most North America–Old World disjunctions (e.g., Tiffney, 1985b; Fritsch, 2001; Hohmann et al., 2006), molecular dating of lineage divergence has conversely favored oceanic dispersal over vicariance, as in O. linifolia, in a wide variety of animal and plant taxa showing intercontinental disjunct distributions (see reviews in Givnish and Renner, 2004; de Queiroz, 2005; Renner, 2005).
In a recent review, Mummenhoff and Franzke (2007) provide several examples of intercontinental disjunctions originating in the late Tertiary/Quaternary by long-distance dispersal. The Pleistocene was characterized by climatic oscillations that affected most parts of the world and could have created new habitats that provided new niches for colonization of dispersed plants (Hewitt, 2003). Indeed, deserts of southwestern North America, where O. linifolia is found, are of recent geological origin, dating back to the Late Pliocene or Pleistocene (e.g., Raven and Axelrod, 1978; Thorne, 1986; Moore and Jansen, 2006).
Dispersal and colonization of Oligomeris
Our results imply that O. linifolia is the only Resedaceae species whose presence in the New World is probably not related to an anthropogenic introduction. Furthermore, the case of O. linifolia, together with those of Senecio mohavensis (Liston et al., 1989; Liston and Kadereit, 1995; Coleman et al., 2001, 2003) and Plantago ovata (Meyers and Liston, 2008) may be examples of natural disjunctions at the species level between Old World deserts (northern Africa–southwestern Asia) and the arid region of southwestern North America. It should be noted, however, that morphological differentiation between the disjunct populations of Senecio mohavensis and Plantago ovata was enough to justify segregation into different subspecies (Coleman et al., 2001, 2003) or varieties (Meyers and Liston, 2008), respectively, whereas no infraspecific distinction has been recognized within O. linifolia (Jepson, 1936; Abdallah and de Wit, 1978; Daniel, 1993; Martín-Bravo et al., in press).
An epizoochoric dispersal event has been suggested in Senecio mohavensis (Coleman et al., 2003) and Plantago ovata (Meyers and Liston, 2008), while Oligomeris lacks obvious specific mechanisms for long-distance dispersal ("unassisted dispersal," according to Ridley [1930] and van der Pijl [1979]). A possible explanation could be that migrating birds have carried seeds across the Atlantic Ocean. Although no extant bird species currently have a migration route matching the disjunction of O. linifolia (Lincoln, 1979), vagrant birds (migrants widely deviating from their normal route) have been reported worldwide covering such distances and are cited as potential intercontinental long-distance dispersal vectors (Thorup, 1998; Coleman et al., 2003; Mummenhoff and Franzke, 2007). Additionally, Wilkinson (1997) has suggested that seeds dispersed over long distances during the Quaternary postglacial colonization of North America, were mainly carried by birds. Alternatively, the seeds of O. linifolia are very small (c. 0.5 mm) and light, and as a result wind currents could have been involved in a long-distance dispersal event. However, plants without specific wind-dispersal mechanisms have rarely been reported to have been dispersed long distances (Wilkinson, 1997; Cain et al., 2000). In addition, no evidence is reported of prevailing wind currents connecting the Old World and southwestern North America during the Quaternary.
Despite the unassisted dispersal syndrome in O. linifolia, it seems to have great dispersal and colonization ability, as suggested by its large and disjunct range (Fig. 1). The species has been reported from many islands or archipelagos throughout its range, including most islands off the Californian coast (Watson, 1876; Halvorson, 1992), the eastern Canary Islands (Hansen and Sunding, 1993) and islands in the Persian Gulf (Kunkel, 1977). Many of these islands are of oceanic origin, and their indigenous floras are a consequence of dispersal from the continent. Moreover, some of them are situated a considerable distance from the mainland, such as the Canary Islands (c. 100 km), the Channel Islands (20–100 km) and Guadalupe Island (260 km). In this respect, O. linifolia shares a similar pattern of oceanic dispersal with other organisms of apparent low dispersal ability (see review in de Queiroz, 2005).
Our data from cpDNA indels (Fig. 3C) indicate a possible colonization of Guadalupe Island (H7), followed by colonization of San Nicolas Island (H8). However, because H8 haplotype was generated from the codification of a homoplasic indel, a cautious interpretation of this genealogical relationship is made.
The considerable trnL-F/rps16 haplotype diversity in the New World contrasts with the relatively poor genetic differentiation in the Old World, where O. linifolia is distributed across a comparatively larger territory (Fig. 1). This may be the result of an active process of genetic differentiation within American populations, which may have started soon after the long-distance dispersal event. Alternatively, the poor genetic differentiation in the Old World populations may be the result of a higher extinction rate due to climatic oscillations during the Quaternary.
Interestingly, the other Oligomeris species (O. dipetala and O. dregeana) are southern African endemics and therefore represent another remarkable disjunction within the family Resedaceae (Martín-Bravo et al., 2007), providing further evidence of dispersal and colonization success within the genus Oligomeris.
Conclusions
In this research, two independent molecular clock approaches reject the vicariance hypotheses traditionally proposed to explain the intercontinental disjunction found in O. linifolia. Once vicariance was rejected, genetic differentiation of American populations, characterized by the presence of exclusive ITS ribotypes and plastid haplotypes, does not suggest an anthropogenic introduction. Finally, the distribution of the remaining species of the genus and the family in the Old World suggests a long-distance dispersal from the Old to the New World as the most plausible explanation for the presence of O. linifolia in North America. Therefore, our molecular data support the indigenous status of this species in the New World, providing one of the few documented examples of a natural intercontinental disjunction at the specific level between the arid regions of the Old World and southwestern North America. Morphological uniformity and haplotype sharing across the disjunct populations suggest that the dispersal event may have occurred in relatively recent times. Likewise, estimates of divergence times obtained from the molecular clock analyses indicate that the dispersal could have taken place during the Quaternary. This successful colonization might have been favored by the formation of North American deserts and subsequent creation of new arid habitats suitable for the colonization of O. linifolia.
Appendix 1. List of studied material including taxon, GenBank accession number (ITS, rbcL, matK, trnL-F, rps16) and voucher information with Index Herbariorum abbreviation in brackets. Numbers of Oligomeris linifolia populations as depicted on map (Fig. 1) are included in brackets after the locality.
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FOOTNOTES
1 The authors thank M. Míguez and F. J. Fernández for technical support; B. Guzmán and M. Escudero for helpful advice with molecular clock analyses; the curators of BM, CAS, EA, HBG, HUJ, LD, RNG, RSA, UC, UCR, UPOS, UPS, WAG, WU, and Z herbaria for the loan of specimens and granting permissions for DNA extractions; and S. C. Meyers, G. C. Tucker, and two anonymous reviewers for their critical reading and commenting of the manuscript. This research was supported by the Spanish Ministry of Science and Technology and the Andalusian Government through projects CGL2005-06017-C02-02/BOS and P06-RMM-4128, respectively. 
4 Author for correspondence (e-mail: smarbra{at}upo.es); present address: Department of Molecular Biology and Biochemical Engineering, Pablo de Olavide University, ctra. de Utrera km 1, 41013, Sevilla, Spain; fax: + 34-954349813
LITERATURE CITED
Abdallah, M. S., AND H. C. D. de Wit. 1978. The Resedaceae: A taxonomical revision of the family (final installment). Mededelingen Landbouwhoogeschool Wageningen 78.
Axelrod, D. I. 1975. Evolution and biogeography of the Madrean-Tethyan sclerophyll vegetation. Annals of the Missouri Botanical Garden 62: 280–334.[CrossRef][Web of Science]
Baldwin, B. G., AND M. J. Sanderson. 1998. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proceedings of the National Academy of Sciences, USA 95: 9402–9406.
Bassett, I. J., AND B. R. Baum. 1969. Conspecifity of Plantago fastigiata of North America with P. ovata of the Old World. Canadian Journal of Botany 47: 1865–1868.[CrossRef]
Beier, B. A., J. A. A. Nylander, M. W. Chase, AND M. Thulin. 2004. Phylogenetic relationships and biogeography of the desert plant genus Fagonia (Zygophyllaceae), inferred by parsimony and Bayesian model averaging. Molecular Phylogenetics and Evolution 33: 91–108.[CrossRef][Web of Science][Medline]
Bentham, G., AND J. D. Hooker. 1865. Genera plantarum, vol. 1. Lovell Reeve & Co., Williams & Norgate, London, UK.
Beucher, F. 1975. Étude palynologique de formations néogènes et quaternaires du Sahara Nord-Occidental. Centre National de la Recherche Scientifique, série géologique 20, Université de Paris, Paris, France.
Bossard, C. C., J. M. Randall, AND M. C. Hoshovsky. 2000. Invasive plants of California’s wildlands, 14–15. University of California Press, Berkeley, California, USA.
Cain, M. L., B. G. Milligan, AND A. E. Strand. 2000. Long-distance seed dispersal in plant populations. American Journal of Botany 87: 1217–1227.
Clement, M., D. Posada, AND K. A. Crandall. 2000. TCS: A computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1659.[CrossRef][Medline]
Coleman, M., D. G. Forbes, AND R. J. Abbott. 2001. A new subspecies of Senecio mohavensis (Compositae) reveals Old–New World species disjunction. Edinburgh Journal of Botany 58: 389–403.
Coleman, M., A. Liston, J. W. Kadereit, AND R. J. Abbott. 2003. Repeat intercontinental dispersal and Pleistocene speciation in disjunct Mediterranean and desert Senecio (Asteraceae). American Journal of Botany 90: 1446–1454.
Correll, D. S., AND M. C. Johnston. 1979. Manual of the vascular plants of Texas. University of Texas, Dallas, Texas, USA.
Culham, A. 2007. Resedaceae. In V. H. Heywod, R. K. Brummit, A. Culham, and O. Seberg [eds.], Flowering plant families of the world. Royal Botanic Gardens, Kew, UK.
Daniel, T. F. 1993. Resedaceae. In J. C. Hickman [ed.], The Jepson manual: Higher plants of California, 930–931. University of California Press, Berkeley, California, USA.
Davis, C. C., C. D. Bell, S. Mathews, AND M. J. Donoghue. 2002. Laurasian migration explains Gondwanan disjunctions: Evidence from Malpighiaceae. Proceedings of the National Academy of Sciences, USA 99: 6833–6837.
Dick, C. W., E. Bermingham, M. R. Lemes, AND R. Gribel. 2007. Extreme long-distance dispersal of the lowland tropical rainforest tree Ceiba pentandra L. (Malvaceae) in Africa and the Neotropics. Molecular Ecology 16: 3039–3049.[CrossRef][Medline]
Dixon, C. J. 2006. A means of estimating the completeness of haplotype sampling using the Stirling probability distribution. Molecular Ecology Notes 6: 650–652.[CrossRef][Web of Science]
Felsenstein, J. 2005. PHYLIP (Phylogeny Inference Package), version 3.67. Computer program distributed by the author, Department of Genome Sciences, University of Washington, Seattle, Washington, USA, website http://evolution.genetics.washington.edu/phylip.html.
Fritsch, P. W. 2001. Phylogeny and biogeography of the flowering plant genus Styrax (Styracaceae) based on chloroplast DNA restriction sites and DNA sequences of the internal transcribed spacer region. Molecular Phylogenetics and Evolution 19: 387–408.[CrossRef][Web of Science][Medline]
Givnish, T. J., AND S. S. Renner. 2004. Tropical intercontinental disjunctions: Gondwana breakup, immigration from the boreotropics, and transoceanic dispersal. International Journal of Plant Sciences 165 (Supplement_4): S1–S6.[CrossRef][Web of Science]
Gladenkov, A. Y., A. E. Oleinik, L. Marincovich, AND K. B. Barinov. 2002. A refined age for the earliest opening of Bering Strait. Palaeogeography, Palaeoclimatology, Palaeoecology 183: 321–328.[CrossRef]
Goldblatt, P. 1978. An analysis of the flora of southern Africa: Its characteristics, relationships, and origins. Annals of the Missouri Botanical Garden 65: 369–436.[CrossRef][Web of Science]
Hall, J. C., H. H. Iltis, AND K. J. Sytsma. 2004. Molecular phylogenetics of core Brassicales, placement of orphan genera Emblingia Forchhammeria Tirania and character evolution. Systematic Botany 29: 654–669.[CrossRef][Web of Science]
Hall, J. C., K. J. Sytsma, AND H. H. Iltis. 2002. Phylogeny of Capparaceae and Brassicaceae based on chloroplast sequence data. American Journal of Botany 89: 1826–1842.
Halvorson, W. L. 1992. Alien plants at Channel Islands National Park. In C. P. Stone, C. W. Smith, and J. T. Tunison [eds.], Alien plant invasions in native ecosystems of Hawaii, 64–96. Cooperative National Park Resources Studies Unit, Honolulu, Hawaii, USA.
Hansen, A., AND P. Sunding. 1993. Flora of Macaronesia. Checklist of vascular plants. Sommerfeltia 17.
Hewitt, G. 2003. Ice ages, species distributions, and evolution. In L. J. Rothschild, and A. M. Lister [eds.], Evolution on planet Earth—The impact of the physical environment, 339–361. Academic Press, Amsterdam, Netherlands.
Hohmann, S., J. W. Kadereit, AND G. Kadereit. 2006. Understanding Mediterranean–Californian disjunctions: Molecular evidence from Chenopodiaceae-Betoideae. Taxon 55: 67–78.[Web of Science]
Jepson, W. L. 1936. A flora of California, vol. 2. University of California, Berkeley, California, USA.
Johnson, L. A., AND D. E. Soltis. 1995. Phylogenetic inference in Saxifragaceae sensu stricto and Gilia (Polemoniaceae) using matK sequences. Annals of the Missouri Botanical Garden 82: 149–175.[CrossRef][Web of Science]
Kay, K. M., J. B. Whittall, AND S. A. Hodges. 2006. A survey of nuclear ribosomal internal transcribed spacer substitution rates across angiosperms: An approximate molecular clock with life history effects. BMC Evolutionary Biology 6: 36.[CrossRef][Medline]
Kelchner, S. A. 2000. The evolution of non-coding chloroplast DNA and its application in plant systematics. Annals of the Missouri Botanical Garden 87: 482–498.[CrossRef][Web of Science]
Koch, M., B. Haubold, AND T. Mitchell-Olds. 2001. Molecular systematics of the Brassicaceae: evidence from plastidic matK and nuclear Chs sequences. American Journal of Botany 88: 534–544.
Kunkel, G. 1977. The vegetation of Hormoz, Qeshm and neighbouring islands (southern Persian Gulf area). J. Cramer, Vaduz, Liechtenstein.
Langley, C. L., AND W. M. Fitch. 1974. An examination of the constancy of the rate of molecular evolution. Journal of Molecular Evolution 3: 161–177.[CrossRef][Web of Science][Medline]
Lianli, L., AND N. J. Turland. 2001. Resedaceae. In P. H. Raven, I. Al-Shehbaz, and G. Zhu [eds.], Flora of China, vol. 8, 194–195. Missouri Botanical Garden Press, St. Louis, Missouri, USA.
Lincoln, F. C. 1979. Migration of birds. Fish and Wildlife Service, circular 16. U. S. Department of the Interior, Washington, D.C., USA.
Liston, A., AND J. W. Kadereit. 1995. Chloroplast DNA evidence for introgression and long distance dispersal in the desert annual Senecio flavus (Asteraceae). Plant Systematics and Evolution 197: 33–41.[CrossRef][Web of Science]
Liston, A., L. H. Rieseberg, AND T. S. Elias. 1989. Genetic similarity is high between intercontinental disjunct species of Senecio (Asteraceae). American Journal of Botany 76: 383–388.[CrossRef][Web of Science]
Martín-Bravo, S., H. Meimberg, M. Luceño, W. Märkl, V. Valcárcel, C. Bräuchler, P. Vargas, AND G. Heubl. 2007. Molecular systematics and biogeography of Resedaceae based on ITS and trnL-F sequences. Molecular Phylogenetics and Evolution 44: 1105–1120.[CrossRef][Web of Science][Medline]
Martín-Bravo, S., G. C. Tucker, AND T. F. Daniel. In press. Resedaceae. In Flora of North America Editorial Committee [eds.], Flora of North America, vol. 7. Oxford University Press, New York, New York, USA.
Meyers, S. C., AND A. Liston. 2008. The biogeography of Plantago ovata Forssk. (Plantaginaceae). International Journal of Plant Sciences 169: 954–962.[CrossRef][Web of Science]
Moore, M. J., AND R. K. Jansen. 2006. Molecular evidence for the age, origin, and evolutionary history of the American desert plant genus Tiquilia (Boraginaceae). Molecular Phylogenetics and Evolution 39: 668–687.[CrossRef][Web of Science][Medline]
Mummenhoff, K., H. Brüggemann, AND J. L. Bowman. 2001. Chloroplast DNA phylogeny and biogeography of Lepidium (Brassicaceae). American Journal of Botany 88: 2051–2063.
Mummenhoff, K., AND A. Franzke. 2007. Gone with the bird: Late Tertiary and Quaternary intercontinental long-distance dispersal and allopolyploidization in plants. Systematics and Biodiversity 5: 255–260.[CrossRef][Web of Science]
Mummenhoff, K., P. Linder, N. Friesen, J. L. Bowman, J. Y. Lee, AND A. Franzke. 2004. Molecular evidence for bicontinental hybridogenous genomic constitution in Lepidium sensu stricto (Brassicaceae) species from Australia and New Zealand. American Journal of Botany 91: 254–261.
Nylander, J. A. A. 2002. MrModeltest version 1.1b. Computer program distributed by the author, Department of Systematic Zoology, Uppsala University, Uppsala, Sweden.
Ooi, K., Y. Endo, J. Yokoyama, AND N. Murakami. 1995. Useful primers to amplify DNA fragments of the plastid gene matK from angiosperm plants. Journal of Japanese Botany 70: 328–331.
Oxelman, B., M. Lidén, AND D. Berglund. 1997. Chloroplast rps16 intron phylogeny of the tribe Sileneae (Caryophyllaceae). Plant Systematics and Evolution 206: 393–410.[CrossRef][Web of Science]
de Queiroz, A. 2005. The resurrection of oceanic dispersal in historical biogeography. Trends in Ecology & Evolution 20: 68–73.[CrossRef][Web of Science][Medline]
Raven, P. H. 1971. The relationships between ‘Mediterranean’ floras. In P. H. Davis, P. C. Harper, and I. C. Hedge [eds.], Plant life of south-west Asia, 119–134. Botanical Society of Edinburgh, Aberdeen, UK.
Raven, P. H. 1972. Plant species disjunctions: A summary. Annals of the Missouri Botanical Garden 59: 234–246.[CrossRef][Web of Science]
Raven, P. H., AND D. I. Axelrod. 1978. Origin and relationships of the California flora. University of California Publications in Botany 72: 7–134.
Rejmánek, M., AND J. M. Randall. 1994. Invasive alien plants in California: 1993 Summary and comparison with other areas in North America. Madroño 41: 161–177.
Renner, S. S. 2005. Relaxed molecular clocks for dating historical plant dispersal events. Trends in Plant Science 10: 550–558.[CrossRef][Web of Science][Medline]
Richardson, J. E., R. T. Pennington, T. D. Pennington, AND P. M. Hollingsworth. 2001. Rapid diversification of a species-rich genus of neotropical rain forest trees. Science 293: 2242–2245.
Ridley, H. N. 1930. The dispersal of plants throughout the world. Reeve & Co., Kent, UK.
Rodman, J. E., R. A. Price, K. Karol, K. J. Sytsma, AND J. D. Palmer. 1993. Nucleotide sequences of the rbcL gene indicate monophyly of mustard oil plants. Annals of the Missouri Botanical Garden 80: 686–699.[CrossRef][Web of Science]
Samuel, R., H. Kathriarachi, P. Hoffman, M. H. J. Barfuss, K. J. Wurdack, C. C. Davis, AND M. W. Chase. 2005. Molecular phylogenetics of Phyllanthaceae: Evidence from plastid matK and nuclear PHYC sequences. American Journal of Botany 92: 132–141.
Sanderson, M. J. 2002. Estimating absolute rates of molecular evolution and divergence times: A penalized likelihood approach. Molecular Biology and Evolution 19: 101–109.
Sanderson, M. J. 2004. r8s, version 1.71 user’s manual. Website http://loco.biosci.arizona.edu/r8s.
Savolainen, V., M. W. Chase, S. B. Hoot, C. M. Morton, D. E. Soltis, C. Bayer, M. F. Fay et al.. 2000. Phylogenetics of flowering plants based on combined analysis of plastid atpB and rbcL gene sequences. Systematic Biology 49: 306–362.
Shaw, A. J., O. Werner, AND R. M. Ros. 2003. Intercontinental Mediterranean disjunct mosses: Morphological and molecular patterns. American Journal of Botany 90: 540–550.
Stebbins, G. L., AND A. Day. 1967. Cytogenetic evidence for long continued stability in the genus Plantago. Evolution 21: 409–428.[CrossRef][Web of Science]
Stebbins, G. L., AND J. Major. 1965. Endemism and speciation in the California flora. Ecological Monographs 35: 1–35.[CrossRef][Web of Science]
Swofford, D. L. 2002. PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer, Sunderland, Massachusetts, USA.
Thorne, R. F. 1972. Major disjunctions in the geographic ranges of seed plants. Quarterly Review of Biology 47: 365–411.[CrossRef]
Thorne, R. F. 1986. A historical sketch of the vegetation of the Mojave and Colorado deserts of the American southwest. Annals of the Missouri Botanical Garden 73: 642–651.[CrossRef][Web of Science]
Thorup, K. 1998. Vagrancy of yellow-browed Phylloscopus inornatus and Pallas’ warbler Ph. proregulus in north-west Europe: misorientation on great circles? Ringing and Migration 19: 7–12.
Thulin, M. 1994. Aspects of disjunct distributions and endemism in the arid parts of the horn of Africa, particularly Somalia. In J. H. Seyani, and A. C. Chikuni [eds.], Proceedings of the XIIIth Plenary Meeting, Association pur l'Etude Taxonomique de la Flore d'Afrique Tropicale, 2: 1105–1119. National Herbarium and Botanic Gardens of Malawi, Zomba, Malawi.
Tiffney, B. H. 1985a. Perspectives on the origin of the floristic similarity between eastern Asia and eastern North America. Journal of the Arnold Arboretum 66: 73–94.[Web of Science]
Tiffney, B. H. 1985b. The Eocene North Atlantic land bridge: Its importance in Tertiary and modern phytogeography of the Northern Hemisphere. Journal of Arnold Arboretum 66: 243–273.
Tiffney, B. H., AND S. R. Manchester. 2001. The use of geological and paleontological evidence in evaluating plant phylogeographic hypotheses in the Northern Hemisphere tertiary. International Journal of Plant Sciences 162 (Supplement 6): S3–S17.[CrossRef][Web of Science]
Torrey, J., AND A. Gray. 1838. Flora of North America. Wiley & Putman, New York, New York, USA.
van der Pijl, L. 1979. Principles of dispersal in higher plants. Springer Verlag, New York, New York, USA.
Watson, S. 1876. The flora of the Guadalupe Island, Lower California. American Naturalist 10: 221–228.[CrossRef]
Wen, J., AND S. Shi. 1999. A phylogenetic and biogeographic study of Hamamelis (Hamamelidaceae), an eastern Asian and eastern North American disjunct genus. Biochemical Systematics and Ecology 27: 55–66.[CrossRef][Web of Science]
Wiggins, I. L. 1980. Flora of Baja California. Stanford University Press, Stanford, California, USA.
Wikström, N., V. Savolainen, AND M. W. Chase. 2001. Evolution of the angiosperms: Calibrating the family tree. Proceedings of the Royal Society of London, B, Biological Sciences 268: 2211–2220.
Wilkinson, D. M. 1997. Plant colonization: Are wind dispersed seeds really dispersed by birds at larger spatial and temporal scales. Journal of Biogeography 24: 61–65.[CrossRef][Web of Science]
Wolfe, K. H., W. H. Li, AND P. M. Sharp. 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proceedings of the National Academy of Sciences, USA 84: 9054–9058.
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