Is Oligomeris (Resedaceae) indigenous to North America? Molecular evidence for a natural colonization from the Old World.
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.
- SourceAvailable from: linum.cofc.edu[show abstract] [hide abstract]
ABSTRACT: Long-distance seed dispersal influences many key aspects of the biology of plants, including spread of invasive species, metapopulation dynamics, and diversity and dynamics in plant communities. However, because long-distance seed dispersal is inherently hard to measure, there are few data sets that characterize the tails of seed dispersal curves. This paper is structured around two lines of argument. First, we argue that long-distance seed dispersal is of critical importance and, hence, that we must collect better data from the tails of seed dispersal curves. To make the case for the importance of long-distance seed dispersal, we review existing data and models of long-distance seed dispersal, focusing on situations in which seeds that travel long distances have a critical impact (colonization of islands, Holocene migrations, response to global change, metapopulation biology). Second, we argue that genetic methods provide a broadly applicable way to monitor long-distance seed dispersal; to place this argument in context, we review genetic estimates of plant migration rates. At present, several promising genetic approaches for estimating long-distance seed dispersal are under active development, including assignment methods, likelihood methods, genealogical methods, and genealogical/demographic methods. We close the paper by discussing important but as yet largely unexplored areas for future research.American Journal of Botany 10/2000; 87(9):1217-27. · 2.59 Impact Factor
- [show abstract] [hide abstract]
ABSTRACT: Following (1) the large-scale molecular phylogeny of seed plants based on plastid rbcL gene sequences (published in 1993 by Chase et al., Ann. Missouri Bot. Gard. 80:528-580) and (2) the 18S nuclear phylogeny of flowering plants (published in 1997 by Soltis et al., Ann. Missouri Bot. Gard. 84:1-49), we present a phylogenetic analysis of flowering plants based on a second plastid gene, atpB, analyzed separately and in combination with rbcL sequences for 357 taxa. Despite some discrepancies, the atpB-based phylogenetic trees were highly congruent with those derived from the analysis of rbcL and 18S rDNA, and the combination of atpB and rbcL DNA sequences (comprising approximately 3000 base pairs) produced increased bootstrap support for many major sets of taxa. The angiosperms are divided into two major groups: noneudicots with inaperturate or uniaperturate pollen (monocots plus Laurales, Magnoliales, Piperales, Ceratophyllales, and Amborellaceae-Nymphaeaceae-Illiciaceae) and the eudicots with triaperturate pollen (particularly asterids and rosids). Based on rbcL alone and atpB/rbcL combined, the noneudicots (excluding Ceratophyllum) are monophyletic, whereas in the atpB trees they form a grade. Ceratophyllum is sister to the rest of angiosperms with rbcL alone and in the combined atpB/rbcL analysis, whereas with atpB alone, Amborellaceae, Nymphaeaceae, and Illiciaceae/Schisandraceae form a grade at the base of the angiosperms. The phylogenetic information at each codon position and the different types of substitutions (observed transitions and transversions in the trees vs. pairwise comparisons) were examined; taking into account their respective consistency and retention indices, we demonstrate that third-codon positions and transitions are the most useful characters in these phylogenetic reconstructions. This study further demonstrates that phylogenetic analysis of large matrices is feasible.Systematic Biology 07/2000; 49(2):306-62. · 12.17 Impact Factor
- [show abstract] [hide abstract]
ABSTRACT: Capparaceae and Brassicaceae have long been known to be closely related families, with the monophyly of Capparaceae more recently questioned. To elucidate the relationship between Brassicaceae and Capparaceae as well as to address infrafamilial relationships within Capparaceae, we analyzed sequence variation for a large sampling, especially of Capparaceae, of these two families using two chloroplast regions, trnL-trnF and ndhF. Results of parsimony and likelihood analyses strongly support the monophyly of Brassicaceae plus Capparaceae, excluding Forchhammeria, which is clearly placed outside the Brassicaceae and Capparaceae clade and suggest the recognition of three primary clades-Capparaceae subfamily (subf.) Capparoideae, subf. Cleomoideae, and Brassicaceae. Capparaceae monophyly is strongly contradicted with Cleomoideae appearing as sister to Brassicaceae. Two traditionally recognized subfamilies of Capparaceae, Dipterygioideae and Podandrogynoideae, are embedded within Cleomoideae. Whereas habit and some fruit characteristics demarcate the three major clades, floral symmetry, stamen number, leaf type, and fruit type all show homoplasy. Clades within Capparoideae show a biogeographical pattern based on this sampling. These results are consistent with several alternative classification schemes.American Journal of Botany 11/2002; 89(11):1826-42. · 2.59 Impact Factor
American Journal of Botany 96(2): 507–518. 2009.
One of the most fascinating aspects of plant biogeography
has been the study and interpretation of intercontinental dis-
junctions (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 chiefl y 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 distribu-
tion 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 in-
volving vicariance have been proposed to account for such dis-
junctions: (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 boreotro-
pics 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 lati-
tudes up to 50 ° N, ca. 54 – 35 Ma ( Tiffney, 1985b ; Fritsch, 2001 ;
Davis et al., 2002 ; Beier et al., 2004 ). Alternatively, long-dis-
tance dispersal has been proposed to explain this pattern of in-
tercontinental disjunction, although to a lesser extent than
vicariance, and has usually referred to disjunctions at the spe-
cifi c 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 dis-
junction as the result of post-Columbian anthropogenic intro-
ductions 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 continu-
ously been reported since then ( Rejm á nek 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 . mohaven-
sis in North America has been postulated to be the result of a
fairly recent long-distance dispersal (c. 0.15 Ma) from south-
western 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.
1 Manuscript received 27 June 2008; revision accepted 2 October 2008.
The authors thank M. M í guez and F. J. Fern á ndez for technical support;
B. Guzm á n 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,
4 Author for correspondence (e-mail: firstname.lastname@example.org); present
address: Department of Molecular Biology and Biochemical Engineering,
Pablo de Olavide University, ctra. de Utrera km 1, 41013, Sevilla, Spain;
fax: + 34-954349813
IS OLIGOMERIS (RESEDACEAE) INDIGENOUS TO NORTH
AMERICA? MOLECULAR EVIDENCE FOR A NATURAL
COLONIZATION FROM THE OLD WORLD 1
SANTIAGO MART Í N-BRAVO, 2,4 PABLO VARGAS, 3 AND MODESTO LUCE Ñ O 2
2 Department of Molecular Biology and Biochemical Engineering, Pablo de Olavide University, ctra. de Utrera km 1 41013
Sevilla, Spain; and 3 Botanic Garden of Madrid, CSIC, Pza. Murillo n ° 2 28014 Madrid, Spain
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 confl icting 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 re-
cent splits of Oligomeris lineages disagree with the vicariance hypotheses traditionally suggested to account for New – Old World
disjunctions. In addition, signifi cant genetic differentiation of American populations does not indicate a recent anthropogenic in-
troduction. 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 ;
AMERICAN JOURNAL OF BOTANY
widespread in disturbed habitats (Liston et al., 1989), as ob-
served for Reseda species introduced in North America.
In the last years, there has been an increase in the govern-
mental initiatives for the conservation of biodiversity. These
usually include programs that aim to reduce the negative effects
of alien invasive species on the native fl ora by means of their
eradication or control. Therefore, it would be important to as-
sess 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 deter-
mine whether the intercontinental disjunction found in O. lini-
folia 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. Specifi cally, we
addressed the following objectives: (1) to determine the origin
of the disjunct O. linifolia American populations (i.e., vicari-
ance, 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 dis-
junction to the biology of the species.
MATERIALS AND METHODS
Sampling, DNA extraction, amplifi cation, 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 individ-
ual 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 ( Mart í n-Bravo et al., 2007 ), were
included as outgroup taxa. Nine ITS and three trnL-F sequences were obtained
from a previous molecular study ( Mart í n-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 (Qia-
gen, Valencia, California, USA).
The ITS and trnL-F regions were amplifi ed and sequenced as detailed by
Mart í n-Bravo et al. (2007) . The rps16 intron was amplifi ed 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 ( Oligom-
eris , Resedaceae). Specifi cally, 49 Resedaceae accessions were included for
this analysis: 22 of Oligomeris taxa (fi ve of O. linifolia from the Old World and
eight from the New World; six of O. dipetala ; and three of O. dregeana ), 19
(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 Scle-
ropodium 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 ; Mart í n-Bravo et al., 2007 ). Oligomeris Cambess. is a
monophyletic genus ( Mart í n-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 (M ü ll. Arg.) M ü ll.
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 south-
western 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.
Apart from O. linifolia , four species of Resedaceae ( Reseda
alba L., R. lutea L., R. luteola L., and R. odorata L.) are found
in America, but are undoubtedly introduced, both because there
are no records until recent times (except for R. luteola , which
was probably introduced as a dye plant by Spanish settlers), and
most of them have become invasive weeds ( Torrey and Gray,
1838 ; Abdallah and de Wit, 1978 ; Mart í n-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 popula-
tions 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 dis-
tribution, 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
Fig. 1. Approximate distribution map of Oligomeris linifolia (shaded) and geographic range of ITS ribotypes (upper semicircle) and trnL-F / rps16
haplotypes (lower semicircle) of 24 populations sampled throughout the species range. Additional plastid haplotypes retrieved when coding indels are
represented together with the correspondent haplotype without coded indels in the two middles of the lower semicircle (four populations in America).
Numbers inside circles indicate population number listed in Appendix 1. We only obtained a trnL-F sequence for population number 3 (Somalia).
MART Í N-BRAVO ET AL. — BIOGEOGRAPHY OF OLIGOMERIS LINIFOLIA
lowed 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% di-
vergence/Ma for cpDNA sequences [ Wolfe et al., 1987 ]). This approach would
overestimate divergence times and therefore would favor acceptance of vicari-
ance hypotheses ( Dick et al., 2007 ). PAUP* was used to calculate pairwise se-
quence 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 ( K obs ) between Old and New World pop-
ulations were below levels expected by the vicariance hypotheses ( K exp ), corre-
sponding to less than 20 Ma of genetic isolation, these were rejected in favor of
a relatively recent long-distance dispersal or anthropogenic introduction.
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 chro-
matograms 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 distrib-
uted across the entire species range and was present in most pop-
ulations (R1; 19 Old and New World populations, 82% of all
populations). Two ITS ribotypes were represented by single indi-
viduals from the Old World (R3, Yemen-Hadramaut; R4, Israel).
A fourth (R2) was exclusive to the New World (North Baja Cali-
fornia and San Nicolas Island populations).
TCS constructed a simple network for the four ITS ribotypes
( Fig. 3A ). The most common and widespread ribotype (R1; 19
populations) occupies an internal position in the network and
has four mutational connections. The four other O. linifolia ac-
cessions (R2: North Baja California and San Nicolas Island;
R3: Yemen-Hadramaut; R4: Israel) are tip ribotypes. Seven
mutations were needed to connect R1 to the two Oligomeris
species from southern Africa.
Within the plastid trnL-F / rps16 matrix, 11 sites were vari-
able 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 ; Ta-
ble 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 popula-
tions (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 identifi ed 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 fi ve haplotypes exclu-
sive to the New World when coding indels. No variable sites were
found within the three rbcL - matK accessions of O. linifolia
accessions of fi ve Reseda species, and four accessions each of Caylusea and
Sesamoides (Appendix 1). Sixty accessions from other Brassicales taxa (Cari-
caceae, Moringaceae, Bataceae, Koeberliniaceae, Tovariaceae, Pentadiplan-
draceae, Gyrostemonaceae, Capparaceae, Forchhammeria , Cleomaceae,
Brassicaceae; Appendix 1) were primarily taken from the GenBank. These se-
quences were mainly obtained in previous systematic studies of Brassicales
(e.g., Rodman et al., 1993 ; Hall et al., 2002 , 2004 ; Mart í n-Bravo et al., 2007 ).
Standard primers were used for the amplifi cation 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. Amplifi ca-
tion 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 fi nal extension
of 7 min at 72 ° C.
Phylogenetic and haplotype data analyses — We manually aligned two ma-
trices 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 per-
formed, as in Mart í n-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 topol-
ogy (1000 replicates each) as implemented in the program PAUP* version
4.0b10 (Swofford, 2002).
Statistical parsimony analyses of Oligomeris haplotypes were performed us-
ing the program TCS version 1.21 ( Clement et al., 2000 ) with a 95% parsimony
connection limit. We estimated completeness of the ribotype (ITS) and haplo-
type ( trnL-F / rps16 ) sampling using a Stirling probability distribution as de-
scribed by Dixon (2006) .
Estimating divergence times — We used two independent approaches to in-
fer divergence times of Oligomeris lineages. The fi rst was a penalized likeli-
hood 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 evalu-
ated rate heterogeneity among lineages by means of a Langley and Fitch (LF)
test ( Langley and Fitch, 1974 ). The null hypothesis of molecular clock (con-
stant rate) was rejected for both the ITS and plastid data sets. As a result, diver-
gence 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 recom-
mended in the r8s manual. Penalized likelihood search parameters included fi ve
initial and fi ve 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 Wik-
str ö m 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 analy-
ses, representing the species distribution (Old/New World) and sequence diver-
sity found in our sampling ( Fig. 2 ).
The second approach was a test to evaluate the three vicariance hypotheses
traditionally invoked to explain such intercontinental disjunct pattern (see In-
troduction): (1) Beringian land bridge (ca. 20 Ma), (2) Madrean-Tethyan belt
(ca. 40 – 25 Ma), and (3) boreotropical land bridge (54 – 35 Ma). This test of vi-
cariance hypotheses was performed following the methods recently described
by Dick et al. (2007) , 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 nu-
cleotide substitution rates. These mutation rates, calibrated with fossil data, al-
AMERICAN JOURNAL OF BOTANY
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 evolu-
tion for the trnL-F / rps16 matrix. Tree topology and clade sup-
port obtained with the two different approaches were identical.
BI majority rule consensus trees obtained from the analy-
ses of the single (ITS, trnL-F / rps16 ; not shown) and com-
bined matrices ( Fig. 4 ) are consistent with the strict consensus
trees of the MP analyses. Accessions of Oligomeris form a
(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 cod-
ing indels, reveals genealogical relationships between haplo-
types, 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 fi ve 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: Cali-
fornia-Imperial County; H4: Yemen-Hadramaut; H5: Argelia
and China). Coding indels (three) revealed three additional hap-
lotypes (H6, H7, H8), in agreement with previous network to-
pologies, 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. Interest-
ingly, 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 codifi cation of two indels (indicated
with asterisks in the network, Fig. 3C ), is homoplasic in haplo-
types 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
Fig. 2. Chronograms of Bayesian inference (BI) trees based on the penalized likelihood analysis of (A) plastid rbcL - matK - trnL-F and (B) nuclear ITS
sequences. Branch lengths represent millions of years (Ma). Posterior probabilities and bootstrap values are given above and below branches, respectively.
Vertical bars indicate supraspecifi c taxa from the same taxonomic group. Maximum and minimum ages of the nodes used to constrain divergence times
between different lineages within the Brassicales ( Wikstr ö m et al., 2001 ) are shown within boxes for each of the two chronograms and represented by
circled letters on the trees (A – E). Numbers (1 – 3) indicate nodes (Resedaceae, Oligomeris , O. linifolia ; see Table 2 ) whose age was estimated. Geographical
origin of the population (Old/New World) and the trnL-F / rps16 haplotype or ITS ribotype are also indicated for O. linifolia accessions included. OW = Old
World; NW = New World; Pli = Pliocene; P = Pleistocene.
MART Í N-BRAVO ET AL. — BIOGEOGRAPHY OF OLIGOMERIS LINIFOLIA
methods (K2P, HKY85 for ITS; K2P, F81 for cpDNA) were
identical. Observed levels of ITS and trnL-F / rps16 sequence
divergence between the disjunct populations of O. linifolia ( K obs
= 0 – 0.29 for ITS sequences; K obs = 0 – 0.13 for trnL-F / rps16
sequences) fall far below the values expected by any of the
three vicariance hypotheses. This result was obtained using
both a conservative approach based on the slowest published
rates ( K exp ³ 1.52 for ITS; K exp ³ 4 for trnL-F / rps16 ), as well as
using rates from the Brassicaceae ( K exp ³ 18.18 for ITS; K exp ³
7.14 for trnL-F / rps16 ). The application of the latter mutation
rates to the maximum levels of sequence divergence between
O. linifolia lineages ( K obs = 0.29 for ITS; K obs = 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).
Origin and time estimates for the intercontinental disjunc-
tion — 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 be-
tween American and Old World conspecifi c populations. These
values are far below those expected by any of the three vicari-
ance hypotheses ( Table 3 ). Likewise, this result is also sup-
ported 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 Rese-
daceae is pollen from Miocene (c. 5.3 – 1.8 Ma) sediments from
the Sahara ( Beucher, 1975 ), in agreement with our estimated
Our results are not unexpected considering morphological
differentiation and palaeogeological events. Land bridges be-
tween North America and the Old World postulated by differ-
ent biogeographic theories (Beringian bridge, Madrean-Tethyan
belt, boreotropical land bridge) date back at least to the Mio-
cene (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 ; Mum-
menhoff et al., 2001 ; Gladenkov et al., 2002 ). However, at this
time, plant exchange was likely limited to cool-tolerant and bo-
real taxa, unlike thermophilic lineages like Oligomeris ( Tiffney
and Manchester, 2001 ; Davis et al., 2002 ). Therefore, no pa-
laeogeological/climatical evidence exists for a connection be-
tween the arid regions of the Old – New World during the
Pleistocene (Liston et al., 1989; Coleman et al., 2003 ). In addi-
tion, morphological uniformity within O. linifolia ( Jepson,
1936 ; Abdallah and de Wit, 1978 ; Daniel, 1993 ; Mart í n-Bravo
et al., in press ) and the sharing of the most frequent and wide-
spread ITS (R1) and cpDNA (H1) sequences between popula-
tions 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 ex-
planations for the disjunction: intercontinental dispersal event
or introduction by man. One ITS ribotype and several cpDNA
haplotypes were exclusively found in the New World popula-
tions ( 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.
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. lini-
folia : 100% PP; 69% BS; Fig. 2A ). These results are in agree-
ment with a previous molecular study ( Mart í n-Bravo et al.,
2007 ), which, however, did not include any O. linifolia sam-
ple 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 ).
Molecular clock analyses — Our penalized likelihood ap-
proach indicates that after the divergence of the two main
lineages in the core Brassicales ( Forchhammeria , Gyrostemo-
naceae, Pentadiplandraceae, Resedaceae, and Tovariaceae vs.
Capparaceae, Cleomaceae, and Brassicaceae; Fig. 2A ) approx-
imately 33 – 42 Ma (latter Eocene; Wikstr ö m et al., 2001 ), 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 Oligom-
eris 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 ).
In the test of vicariance hypotheses ( Table 3 ), O. linifolia
sequence divergences calculated with the different distance
TABLE 1. List of (A) ITS ribotypes and (B) trnL-F / rps16 haplotypes found
in the 24 Oligomeris linifolia populations sampled. Variable sites in
the corresponding matrices are shown, excluding mononucleotide
repeat units. Nucleotide position (numbered from 5 ′ to 3 ′ ) is given
separately for each of the two plastid regions.
269 808223235 501576 653
H6 AC — TATA
H7 ACT — ATA
H8 — CT — ATA
AMERICAN JOURNAL OF BOTANY
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
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 ; Mart í n-Bravo et al.,
2007 ), all the evidence presented led us to suggest that a long-
distance dispersal from the Old World to North America ap-
pears the most likely explanation for this intercontinental
disjunction. The application of an approximate molecular
TABLE 2. Penalized likelihood age estimates (mean, standard deviation, minimum and maximum) for the most important unconstrained nodes in the
Resedaceae, based on the analysis of two matrices (plastid rbcL-matK-trnL-F , nuclear ITS).
rbcL - matK - trnL-F ITS
NodeMean age (Ma)SD (Ma)Minimum age (Ma)Maximum age (Ma)Mean age (Ma) SD (Ma) Minimum age (Ma) Maximum age (Ma)
2 ( Oligomeris )
3 ( O. linifolia )
Notes: Nodes numbered as in Fig. 2 . Ma = million years ago; SD = standard deviation.
Fig. 3. Statistical parsimony networks depicting Oligomeris genealogical relationships based on (A) ITS sequences and (B) trnL-F / rps16 sequences
with uncoded and (C) coded indels. Oligomeris linifolia ribotype/haplotype numbers are enclosed in colored circles, and lines connecting them represent
mutational changes in the corresponding ITS or trnL-F / rps16 sequence. Numbers of ribotypes/haplotypes shared between Old and New World populations
(R1, H1) are in bold italic font, whereas those exclusive from the Old World are in bold and those only found in the New World are in italics. Dots represent
inferred intermediate ribotypes/haplotypes extinct or not sampled. Homoplasious indel codifi cations are marked by asterisks. Color key used for ribotypes/
haplotypes as in Fig. 1 .
MART Í N-BRAVO ET AL. — BIOGEOGRAPHY OF OLIGOMERIS LINIFOLIA
Fig. 4. Majority rule consensus tree of the 49 800 trees retained in the Bayesian inference of the 28 combined ITS/ trnL-F - rps16 sequences of Oligom-
eris plus two outgroup sequences. Posterior probabilities and bootstrap values are given above and below branches, respectively. Vertical bars indicate
outgroup sequences, accessions from South African Oligomeris , and O. linifolia Old and New World populations sequenced.
AMERICAN JOURNAL OF BOTANY
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 sug-
gested that seeds dispersed over long distances during the
Quaternary postglacial colonization of North America, were
mainly carried by birds. Alternatively, the seeds of O. linifo-
lia are very small (c. 0.5 mm) and light, and as a result wind
currents could have been involved in a long-distance disper-
sal event. However, plants without specifi c wind-dispersal
mechanisms have rarely been reported to have been dispersed
long distances ( Wilkinson, 1997 ; Cain et al., 2000 ). In addi-
tion, no evidence is reported of prevailing wind currents con-
necting 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 sug-
gested 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 fl oras 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,
Our data from cpDNA indels ( Fig. 3C ) indicate a possible
colonization of Guadalupe Island (H7), followed by coloniza-
tion of San Nicolas Island (H8). However, because H8 haplo-
type was generated from the codifi cation of a homoplasic indel,
a cautious interpretation of this genealogical relationship is
The considerable trnL-F / rps16 haplotype diversity in the
New World contrasts with the relatively poor genetic differ-
entiation 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
Interestingly, the other Oligomeris species ( O. dipetala and
O. dregeana ) are southern African endemics and therefore
represent another remarkable disjunction within the family
Resedaceae ( Mart í n-Bravo et al., 2007 ), providing further evi-
dence of dispersal and colonization success within the genus
showing the same biogeographic pattern, not only in the esti-
mated 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 lin-
eage 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) pro-
vide several examples of intercontinental disjunctions originat-
ing 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,
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 an-
thropogenic introduction. Furthermore, the case of O. linifo-
lia , 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 ex-
amples 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 subspe-
cies ( Coleman et al., 2001 , 2003 ) or varieties (Meyers and Li-
ston, 2008), respectively, whereas no infraspecifi c distinction
has been recognized within O. linifolia ( Jepson, 1936 ; Abdal-
lah and de Wit, 1978 ; Daniel, 1993 ; Mart í n-Bravo et al., in
An epizoochoric dispersal event has been suggested in
Senecio mohavensis ( Coleman et al., 2003 ) and Plantago
ovata (Meyers and Liston, 2008), while Oligomeris lacks ob-
vious specifi c mechanisms for long-distance dispersal ( “ un-
assisted dispersal, ” according to Ridley  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 match-
ing the disjunction of O. linifolia ( Lincoln, 1979 ), vagrant
birds (migrants widely deviating from their normal route)
TABLE 3. Test of vicariance hypotheses. K exp and K obs represent the expected and observed levels of nucleotide divergence between the disjunct populations
of Oligomeris linifolia . Values represent percentages of pairwise nucleotide divergence (K2P). See materials and methods for a detailed explanation.
K exp conservative rate K exp Brassicaceae rate K obs O. linifolia K exp conservative rate K exp Brassicaceae rate K obs O. linifolia
> 20 Ma
> 25 Ma
> 35 Ma
0 – 0.13
0 – 0.29
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Bataceae — Batis maritima L. M88341 ( rbcL ), J.R. Manhart s.n. ; AY483219
( matK ), Hawaii, H. Iltis 30500 (WIS).
Brassicaceae — Aethionema arabicum (L.) DC. AY254539 (ITS), France,
Nancy, cultivated, 267 . A. grandifl orum Boiss. & Hohen. AF144354
( matK ), Germany, Jena, cultivated ; AP009367 ( trnL-F ). A. saxatile R. Br.
AY483262 ( rbcL ), Moore s.n. (WIS). Arabidopsis thaliana (L.) Heynh.
DQ528813 (ITS); U91966 ( rbcL ), PGR97-074 ; AF144348 ( matK ),
Germany, Lower Saxony, Hagen A.T.W. ; NC_000932 ( trnL-F ).
Capparaceae — Apophyllum anomalum F. Muell. AY483264 ( rbcL ),
AY483227( matK ), AY122409 ( trnL-F ), Covery 12044 (MO). Capparis
hastata Jacq. M95754 ( rbcL ), AY483228 ( matK ), AY122420 ( trnL-F ), H.
Iltis 30315 (WIS). Forchhammeria macrocarpa Standl. FJ212197 (ITS),
DQ986977 ( trnL-F ), Mexico, Petlalcingo, B. Hansen 1750 (M). F. pallida
Liebm. AY122437 ( trnL-F ), H. Iltis 29350a (WIS). F. sp. AY483276
( rbcL ), AY483244 ( matK ), H. Iltis 30784 (WIS). F. trifoliata Radlk.
AY483277 ( rbcL ), AY483245 ( matK ), Hansen 3002 (WIS).
Cleomaceae — Cleome hassleriana Chodat. M95755 ( rbcL ), I. Al Shehbaz
s.n. (MO). C. spinosa Jacq. AY254535 (ITS), USA, Wisconsin, Madison,
cultivated ; DQ649093 ( trnL-F ). C. viridifl ora Schreb. AY483232 ( matK ),
Solomon s.n. (MO); Podandrogyne chiriquensis (Standl.) Woodson.
AY483269 ( rbcL ), AY483233 ( matK ), AY122450 ( trnL-F ), Nepokroeff
450 (WIS). P. macrophylla (Turcz.) Woodson. DQ455815 (ITS),
Venezuela, M é rida, T. Ruiz 4982 (MY).
Caricaceae — Carica papaya L. AY461547 (ITS), Ecuador, Loja, Catacocha,
E.H. Romeijn-Peeters RUG 57 (GENT); M95671 ( rbcL ), AY483221
( matK ), USA, Wisconsin, cultivated ; NC_010323 ( trnL-F ).
Gyrostemonaceae — Codonocarpus cotinifolius (Desf.) F. Muell. DQ987074
(ITS), Australia, Gindalbie, K.H. Rechinger 59399 (MA). Gyrostemon
thesioides (J.D. Hook) A.S. George. DQ987075 (ITS), FJ212210 ( rbcL ),
FJ212199 ( matK ), DQ986975 ( trnL-F ), Australia, Naraacorte, C.R.
Alcock 3115 (MA). Tersonia cyathifl ora (Fenzl) A.S. George. L22441
( rbcL ), AY483238 ( matK ), AY122462 ( trnL-F ), Australia, Cranfi eld s.n.
Koeberliniaceae — Koeberlinia spinosa Zucc. L14600 ( rbcL ), AY483222
( matK ), I. Al Shehbaz s.n. (MO).
Moringaceae — Moringa oleifera Lam. AY845130 (ITS), DQ061137 ( trnL-F ),
Belgium, Meise, cultivated, 1975-2855 ; L11359 ( rbcL ), AY483223
( matK ), H. Iltis 30501 (WIS).
Pentadiplandraceae — Pentadiplandra brazzeana Baill. U38533 ( rbcL ), T.
Hart 180 (MO); AY483239 ( matK ), AY122463 ( trnL-F ), Gabon, J. Hall
Tovariaceae — Tovaria pendula Ruiz & Pav. DQ987073 (ITS), Peru, San Mart í n,
Rioja, M. Weigend 2000/926 (MSB); FJ212196 (ITS), FJ212209 ( rbcL ),
FJ212198 ( matK ), FJ212280 ( trnL-F ), Germany, M ü nich, cultivated, C.
Br ä uchler 3542 (M); M95758 ( rbcL ), AY483242 ( matK ), AY122465
( trnL-F ), Smith 1834 (WIS).
Resedaceae — Caylusea hexagyna (Forssk.) M.L. Green. DQ987227 (ITS),
FJ212220 ( rbcL ), FJ212207 ( matK ), Saudi Arabia, Riyadh, O. Hedberg
9220A (UPS); DQ987069 ( trnL-F ), Cape Verde, Sal, H. Rustan 2653
(O). Oligomeris dipetala (Aiton) Turcz. var. dipetala . DQ987168 (ITS),
DQ987037 ( trnL-F ), FJ212247 ( rps16 ), South Africa, Kimberley, L. Smook
10164 (PRE). O. dipetala var. burchelli (M ü ll. Arg.) Abdallah & de Wit.
DQ987170 (ITS), FJ212217 ( rbcL ), FJ212278 ( trnL-F ), FJ212249 ( rps16 ),
South Africa, Outjo, W. Giess 5982 (PRE). O. dipetala var. spathulata
(Mey. ex Turcz.) Abdallah & de Wit. DQ987169 (ITS), FJ212216 ( rbcL ),
FJ212277 ( trnL-F ), FJ212248 ( rps16 ), Namibia, Diamond Area, C.J. Ward
10202 (PRE). O. dregeana (M ü ll. Arg.) M ü ll. Arg. DQ987166 (ITS),
FJ212204 ( matK ), DQ987038 ( trnL-F ), FJ212245 ( rps16 ), South Africa,
Transvaal, J.C. Scheepers 1447 (PRE); DQ987167 (ITS), FJ212276
( trnL-F ), FJ212246 ( rps16 ), South Africa, Wolverand, W.J. Hanekom
2010 (PRE). O. linifolia (Vahl) J.F. Macbr. FJ212187 (ITS), FJ212262
( trnL-F ), FJ212232 ( rps16 ), China, Yunnan, Diqing Prefecture (pop.1),
B. Alden 1108 (CAS); FJ212178 (ITS), FJ212261 ( trnL-F ), FJ212231
( rps16 ), Iran, Jaz Murian (pop.2), J. Leonard 5700 (WAG); FJ212271
( trnL-F ), Somalia, Erigavo (pop.3), P.R. Bally 15989 (EA); DQ987164
(ITS), FJ212254 ( trnL-F ), FJ212224 ( rps16 ), Yemen, Hadramaut (pop.4),
M. Thulin 8136 (UPS); FJ212195 (ITS), FJ212275 ( trnL-F ), FJ212244
( rps16 ), Yemen, Arhab (pop.5), J.R. Wood 2057 (BM); FJ212193 (ITS),
FJ212273 ( trnL-F ), FJ212242 ( rps16 ), Saudi Arabia, Riyadh (pop.6), I.
Hedberg 92212 (UPS); FJ212176 (ITS), FJ212259 ( trnL-F ), FJ212229
( rps16 ), Israel, Negev (pop.7), M. Zohary 504 (Z); FJ212189 (ITS),
FJ212260 ( trnL-F ), FJ212230 ( rps16 ), Egypt, El Cairo-Suez (pop.8),
G. Rom é e 900 (LD); FJ212194 (ITS), FJ212274 ( trnL-F ), FJ212243
( rps16 ), Algeria, Tamanrasset, Hoggar Massif (pop.9), D. Podlech 33289
(HUJ); DQ987162 (ITS), FJ212253 ( trnL-F ), FJ212223 ( rps16 ), Western
Sahara, El Aioun (pop.10), F.J. Fern á ndez-Casas (RNG); DQ987163
(ITS), FJ212252 ( trnL-F ), FJ212222 ( rps16 ), Spain, Canary Islands,
Fuerteventura (pop.11), H. Kuschel s.n. 1991 (HBG); FJ212183 (ITS),
FJ212272 ( trnL-F ), FJ212241 ( rps16 ), Spain, Canary Islands, Lanzarote
(pop.12), S. Mart í n-Bravo 662SMB05 (UPOS); FJ212188 (ITS), FJ212213
( rbcL ), FJ212201 ( matK ), FJ212257 ( trnL-F ), FJ212227 ( rps16 ), Spain,
Canary Islands, Gran Canaria (pop.13), S. Mart í n-Bravo 105SMB06
(UPOS); FJ212184 (ITS), FJ212258 ( trnL-F ), FJ212228 ( rps16 ), Spain,
Canary Islands, Tenerife (pop.14), D. Bramwell 3243 (RNG); FJ212177
(ITS), FJ212264 ( trnL-F ), FJ212234 ( rps16 ), Mexico, Coahuila, Monclova
(pop.15), W.F. Mahler 5658 (UCR); FJ212179 (ITS), FJ212270 ( trnL-F ),
FJ212240 ( rps16 ), Mexico, Sonora, Navajoa (pop.16), T.R. van Devender
95-116 (UCR); FJ212191 (ITS), FJ212255 ( trnL-F ), FJ212225 ( rps16 ),
Mexico, North Baja California, Tres Enriques (pop.17), J. Henrickson
32570 (WU); FJ212190 (ITS), FJ212263 ( trnL-F ), FJ212233 ( rps16 ),
Mexico, Guadalupe Island (pop.18), S. Carlquist 477 (RSA); FJ212185
(ITS), FJ212269 ( trnL-F ), FJ212239 ( rps16 ), USA, Texas, Starr Co.
(pop.19), D.S. Correll 32311 (UC); FJ212186 (ITS), FJ212268 ( trnL-F ),
FJ212238 ( rps16 ), USA, Texas, Hudspeth Co. (pop.20), R.D. Worthington
32549 (UCR); FJ212181 (ITS), FJ212215 ( rbcL ), FJ212203 ( matK ),
FJ212267 ( trnL-F ), FJ212237 ( rps16 ), USA, Arizona, Maricopa Co.
(pop.21), R.S. Felger 03-431 (RSA); FJ212180 (ITS), FJ212266 ( trnL-F ),
FJ212236 ( rps16 ), USA, Nevada, Nye Co. (pop.22), M. de Decker 4606
(RSA); FJ212182 (ITS), FJ212214 ( rbcL ), FJ212202 ( matK ), FJ212256
( trnL-F ), FJ212226 ( rps16 ), USA, California, Imperial Co. (pop.23), R.
Rutherford 33581 (WU); FJ212192 (ITS), FJ212265 ( trnL-F ), FJ212235
( rps16 ), USA, California, Ventura Co., San Nicolas Island (pop.24), S.A.
Junak SN-888 (RSA). Reseda alba L. DQ987192 (ITS), Greece, Crete,
Iraklio, S. Mart í n Bravo 345SMB05 (UPOS); AY483273 ( rbcL ), AY483241
( matK ), AY122464 ( trnL-F ), J.E. Rodman 535 (WIS) (misidentifi ed as R.
lutea L. in Genbank). R. battandieri Pitard. FJ212175 (ITS), FJ212279
( trnL-F ), FJ212251 ( rps16 ), Morocco, Tifl et, S. Mart í n-Bravo 35SMB06
(UPOS). R. complicata Bory. DQ987172 (ITS), DQ987046 ( trnL-F ),
FJ212250 ( rps16 ), Spain, Granada, Sierra Nevada, S. Mart í n-Bravo
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.
Family — Taxon , GenBank accession no., Voucher , (Herbarium).
AMERICAN JOURNAL OF BOTANY
62SMB04 (UPOS); FJ212218 ( rbcL ), FJ212205 ( matK ), Spain, Almer í a,
Sierra Nevada , P. Jim é nez-Mej í as 152PJM06 (UPOS). R. crystallina
Webb & Berthel. DQ987088 (ITS), FJ212212 ( rbcL ), FJ212200 ( matK ),
DQ987021 ( trnL-F ), Spain, Canary Islands, Fuerteventura, S. Snogerup
16461 (LD). R. luteola L. DQ987187 (ITS), FJ212219 ( rbcL ), FJ212206
( matK ), DQ987050 ( trnL-F ), Greece, Crete, S. Mart í n-Bravo 391SMB05
(UPOS). R. scoparia Brouss. ex Willd. DQ987152 (ITS), FJ212211
( rbcL ), FJ212282 ( trnL-F ), Spain, Canary Islands, Tenerife, R. Elven s.n.
1987 (O). Sesamoides purpurascens (L.) G. L ó pez. DQ987216 (ITS).
Spain, Seville, El Castillo de las Guardas, S. Mart í n-Bravo 36SMB04
(UPOS); FJ212221 ( rbcL ), FJ212208 ( matK ), FJ212286 ( trnL-F ), Spain,
Guadalajara, Sig ü enza, B. Guzm á n 122BGA04 (UPOS).