| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Systematics |
The University of Texas at Austin, Section of Integrative Biology and Plant Resources Center, Austin, Texas 78712 USA
Received for publication September 11, 2003. Accepted for publication January 15, 2004.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Key Words: Bursera • Burseraceae • Caribbean flora • Commiphora • Hispaniola • hybrid taxa • interspecific hybridization
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). Species of the genus are found in a wide variety of low elevation habitats, including deserts and rainforests but are most common in dry tropical deciduous forests (Rzedowski, 1978
; Rzedowksi and Kruse, 1979
), where they can form a prominent component of the woody vegetation.
Since the beginning of detailed systematic work on Bursera in the 1930s, botanists have postulated that some species relationships within the genus may be reticulate due to interspecific hybridization. Numerous cases of introgression among species have been inferred, and the hybrid origins for seven Bursera species have been proposed, based on the supposition that morphologically intermediate individuals that share geographic distributions with putative parent species are derived from hybridization (Urban, 1929
; Bullock, 1936
, 1937
, 1938
; Cuatrecasas, 1957
; McVaugh and Rzedowski, 1965
; Rzedowski, 1968
; Wiggins and Porter, 1971
; Toledo-Manzur, 1982
; Rzedowski and Ortiz, 1988
; Rzedowski and Guevara-Féfer, 1992
). Although hybridization has been postulated to occur equally within the two subgenera of Bursera, B. subg. Elaphrium and B. subg. Bursera, no hybridization between subgenera has been reported even though they have sympatric ranges. Purported hybrid species are presumed to be diploid because none of the taxa examined to date has morphological features associated with polyploid taxa, such as enlarged pollen grains, leaves, and flowers (Stebbins, 1950
). Authors of the most recent taxonomic synopsis of Bursera, which includes only those species from western Mexico, accepted that hybridization occurred but did not comment on how it may have influenced the evolution of the genus (McVaugh and Rzedowski, 1965
, p. 322). They prescribed additional field studies of hybrid taxa in order to "profitably speculate about the extent of hybridization and introgression" within the genus Bursera.
Although Mexican Bursera species have been the focus of molecular phylogenetic work (Becerra, 1997
, 2003
; Becerra and Venable, 1999
), no published studies to date have used DNA markers to test putative hybrid species or to examine whether reticulate evolution is a component of Bursera's genetic history. The only detailed examination of a putative interspecific hybrid in Bursera focused on the reproductive biology of B. medranoana (B. subg. Bursera; Cortés-Palomec, 1998
) but did not test the hypothesized parentage (B. morelensis x B. schlechtendalii) or establish the directionality of the hybridization event. Cortés-Palomec's findings suggest that the role of Bursera hybrids in species formation or in the introgression of genes among existing species may be extremely limited because B. medranoana lacks viable pollen and reproduces asexually though apomixis.
During field collection of Bursera species on the Caribbean island of Hispaniola for our molecular systematic investigations of the Burseraceae and the genus sister to Bursera, Commiphora, we found three different putative interspecific hybrids involving members of B. subg. Bursera. The first two hybrids appeared to share B. simaruba as a parent. This species is common throughout the Caribbean and (sub)tropical regions of North, Central, and northern South America (Francis, 1990
). We hypothesized that the other parents of these two hybrids were species endemic to Hispaniola, B. nashii (Figs. 1, 2) and B. spinescens (Figs. 3, 4). We later determined that the two hybrids corresponded to two named endemic species, B. brunea and B. gracilipes, respectively. Interestingly, Urban (1929
, p. 59) noted that E. L. Ekman, who transferred Spondias brunea to Bursera, suspected that this species was a hybrid between B. simaruba and B. nashii. We inferred that a third endemic Hispaniolan species, B. ovata (Fig. 5), was also a hybrid based on its morphological similarity to B. gracilipes, the hypothesized hybrid of B. spinescens and B. simaruba.
|
|
; Populus, Keim et al., 1989
; Helianthus, Rieseberg, 1990
; Penstemon, Wolfe and Elisens, 1993
; Rhododendron, Milne et al., 1999
). Nuclear alleles are biparentally inherited, whereas plastids are typically inherited from the maternal parent in angiosperms (Corriveau and Coleman, 1988
; Hagemann and Schröder, 1989
; Harris and Ingram, 1991
). To test the parentage of these putative Bursera hybrids, DNA sequence data from the nuclear and chloroplast genomes were collected from the putative hybrids and all other Hispaniolan species, as well as other Caribbean and continental Bursera species in B. subg. Bursera. Multiple independent phylogenies of B. subg. Bursera, including the hybrid individuals, were constructed using these sequence data sets under the parsimony criterion.
Selection of molecular markers
Our pilot sequencing studies revealed very low levels of sequence variation in the nuclear and chloroplast genome of Bursera species. This indicated that only sequence data from rapidly evolving DNA regions would be useful for elucidating species relationships. From the nuclear genome, the external transcribed spacer (ETS) and the fourth intron of the phosphoenolpyruvate carboxylase gene (PEPC) were selected for the phylogenetic study. The ETS is part of the 3' end of the intergenic spacer located between the 26S and 18S genes of the nuclear ribosomal (nrDNA) repeat region; it may participate in the post-transcriptional processing and maturation of the ribosomal subunits (Musters et al., 1990
; Hitchen et al., 1997
). This region has provided informative variation at the species level for various groups of the Asteraceae and allied families (Baldwin and Markos, 1998
; Linder et al., 2000
; Markos and Baldwin, 2001
), Rosaceae (Vanden Heuvel and Linder, 1999
), Fabaceae (Bena et al., 1998
), and Myrtaceae (Wright et al., 2001
). Phylogenies derived from nuclear markers not associated with the nrDNA repeat region can provide an additional test of the concordance between species phylogenies and nuclear gene phylogenies (Sang, 2002
). Phosphoenolpyruvate carboxylase catalyzes the synthesis of oxaloacetate from phosphoenolpyruvate and bicarbonate. It is ubiquitous in plants, and in C4 or crassulacean acid metabolism (CAM) plants, it replaces ribulose bisphosphate carboxylase as the enzyme responsible for the initial capture of dissolved carbon dioxide from the cytosol (Latzko and Kelly, 1983
; Westhoff and Gowik, 2004
). It is part of a low copy gene family, and cDNA studies of phosphoenolpyruvate for C3 species suggest these copies are orthologous, whereas those for C4 and CAM species are not (Gehrig et al., 1998
). Studies of the fourth intron of PEPC within the Moringaceae (Olson, 2002
) have shown that only one copy is directly amplified from DNA extracts and that it can provide levels of sequence variation appropriate for infrageneric studies.
From the chloroplast genome, the rps16 intron and the psbA-trnH spacer were selected for the phylogenetic study from 10 other genes, intergenic spacers, and introns tested: rpl16 intron, trnL intron, trnL-trnF spacer, trnT-trnL spacer, trnS-trnG spacer, psbB-psbF spacer, atpB-rbcL spacer, matK, the 5' and 3' trnK-matK spacers. The rps16 intron is easily amplified using primers anchored in the highly conserved regions of the flanking exons, and, as a chloroplast group II intron, it is likely to have been inserted into its current position only once (Kelchner, 2002
). This intron has been used in molecular phylogenetic studies at the infrafamilial level and above (Sileneae, Oxelman et al., 1997
; Rubioideae, Andersson and Rova, 1999
) but has been shown to provide some infrageneric sequence variation as well (Margaritopsis, Andersson, 2001
; Alectryon, Edwards and Gadek, 2001
; Silene, Popp and Oxelman, 2001
). The psbA-trnH intergenic spacer is located between the photosystem II gene, psbA, and a component gene for the tRNA-histidine complex, trnHGUU (Aldrich et al., 1988
). The gene psbA is adjacent to the right-hand copy of the chloroplast inverted repeat, and genetic mapping studies have shown this region can undergo structural mutation (Palmer, 1985
). Sequencing studies of the psbA-trnH spacer (Sonchus, Kim et al., 1999
; Aconitum, Utelli et al., 2000
) have shown that this region can provide informative base pair and length variation among species.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
; Weeks, 2003
). Whole genomic DNA was extracted following the protocol of Doyle and Doyle (1987)
using a modified extraction buffer including 1% (w : v) polyvinylpyrrolidone and 0.2% (v : v) beta-mercaptoethanol. DNA extracts were cleaned further using cesium gradient centrifugation (Palmer, 1986
) at 20°C at 60 000 rpm for 10 h.
Amplifying nuclear markers
We sequenced a 330-base pair (bp) fragment from the 3' end of the ETS upstream from the 18S gene using Bur-ETS1F (5' TTC GGT ATC CTG TGT TGC TTA C 3') and a previously published 18S primer (Baldwin and Markos, 1998
). The polymerase chain reaction (PCR) volumes of 25 µL included: 10–100 ng of template DNA, 2x PCR buffer (Epicentre, Madison, Wisconsin, USA), 1 mmol/L MgCl2, 400 µmol/ L each dNTP, 0.4 mmol/L of each primer, and 1 unit of Taq polymerase. This region was amplified using an initial denaturation of 95°C (5 min; after which Taq was added to each reaction), 35 cycles of denaturation at 94°C (3 min), 56°C (1 min), 72°C (1 min 20 s + 3 s/cycle), and a final extension period of 72°C (7 min). The PCR products of ETS were cloned for each nonhybrid and hybrid taxon sampled (TOPO-TA Cloning; Invitrogen, Carlsbad, California, USA) using one-third the recommended reaction volumes. Three or more positively transformed colonies were sequenced bidirectionally for each accession.
The PEPC intron was amplified using the primer pair PPCX4F and PPCX5R (Olson, 2002
). The PCR reaction volumes of 25 µL included: 10– 100 ng of template DNA, 1x Triton-X PCR buffer, 2 mmol/L MgCl2, 400 µmol/L each dNTP, 0.4 mmol/L each primer, and 1 unit of Taq polymerase. This region was amplified using the temperature cycling protocol as outlined in Olson (2002)
. For each putative hybrid taxon, PEPC intron PCR products were cloned and three or more positively transformed colonies were sequenced bidirectionally. Two sizes of PCR product were detected by gel electrophoresis for B. microphylla. One fragment was similar in length to those from other Bursera species sampled and one fragment was shorter (ca. 500 bp). These two copies were cloned and sequenced. The longer copy, which consisted of one type within B. microphylla, was easily alignable to the rest of the data matrix, whereas the shorter copy was unalignable with our other sequences from Bursera, although it did partially match other PEPC coding regions published in GenBank. At a higher annealing temperature of 59°C, only the longer fragment was amplified. We concluded that the shorter fragment was not the functional fourth intron of the PEPC gene complex. Instead, it may be the first, second, or third PEPC intron or be a part of a nonfunctional PEPC gene complex that was amplified due to similarity of primer annealing sites.
Amplifying chloroplast markers
The rps16 intron and the psbA-trnH intergenic spacer were amplified using previously published primers (Oxelman et al., 1997
; Sang et al., 1997
). The PCR protocols were identical to those listed for the PEPC intron. The two chloroplast regions were amplified using an initial denaturation step of 95°C (5 min; after which 1 unit Taq polymerase was added to each reaction), and 35 cycles of 94°C (3 min), 50°C for psbA-trnH (1 min) or 57°C for rps16 (1 min), 72°C (1 min 20 s + 3 s/cycle) and a final extension period of 72°C (7 min). Although chloroplast PCR products from all putatively hybrid taxa could be amplified and sequenced directly without cloning, PCR products of chloroplast regions for B. brunea and B. gracilipes were cloned to test whether only one of two (or more) divergent haplotypes was being amplified due to PCR bias. Two or three clones from each of the two species were sequenced bidirectionally.
DNA sequencing
The PCR products were verified prior to sequencing using agarose gel electrophoresis and were cleaned using Qiaquick columns (Qiagen, Valencia, California, USA) or Centri-Sep columns (Princeton Separation, Aldelphia, New Jersey, USA) packed with G-50 Sephadex (Amersham Biosciences, Uppsala, Sweden). Each region was prepared for bidirectional sequencing following a cycle sequencing protocol including the original amplification primers, Big Dye fluorescent dye-terminator reagent mix (Applera, Norwalk, Connecticut, USA), and 20–40 ng of template DNA. The PCR cycling protocol used a temperature ramping rate of 1°C/s and included an initial denaturation of 96°C (1 min) followed by 25 cycles of 96°C (10 s), 50°C (5 s), 60°C (4 min) with a final extension period of 72°C (7 min). Samples were cleaned with Centri-Sep columns and sequenced either at the Institute of Cellular and Molecular Biology DNA Core Facility, The University of Texas at Austin using an ABI Prism 3700 automated sequencer (Applied Biosystems, Foster City, California, USA), or by the authors using a BaseStation automated sequencer (MJ GeneWorks, San Francisco, California, USA).
Sequence alignment and analysis
Sequence strands were assembled and edited in Sequencher (Gene Codes, 1995
). The sequences were aligned automatically in ClustalX (Thompson et al., 1997
) and then adjusted manually in SeqApp (Gilbert, 1992
) and MacClade (Maddison and Maddison, 2000
). To search the maximum amount of potential tree space within a reasonable computational time, 1000 random addition replicates of the data were searched holding and swapping on 10 trees at each step, greater than 1 step in length, using tree-bisection-reconnection (TBR) branch swapping with Multrees in effect in PAUP* version 4 beta 10 (Swofford, 2002
). These trees were saved and were then used as the basis for another round of TBR swapping up to an arbitrary maximum of 20 000 trees. From these 20 000 trees (or fewer), a strict consensus was generated. Bootstrap support for clades was assessed using 1000 pseudoreplicates of the data within PAUP*.
The ETS clone data set was reduced for nonhybrid taxa to compare and combine it with the PEPC intron data set and to reduce homoplasy due to the presence of multiple, orthologous copies. The full ETS data set, including all clones, was reduced to a single ETS clone for each nonhybrid taxon three times, while still retaining all clones from putatively hybrid taxa, and was analyzed using the parsimony method as outlined previously. Clones from each species were numbered based on the order by which they were amplified. The three reduced data sets consisted of (1) the lowest numbered clones, (2) the intermediate numbered clones, (3) the highest numbered clones from each of the nonhybrid taxa plus all the clones from putatively hybrid taxa. The number of trees generated from these three data sets varied widely (44, 352, 704 trees), although the topologies of their strict consensus trees did not disagree with the species relationships as outlined by the phylogeny of all ETS clones. As an alternative solution, consensus sequences were generated for each nonhybrid taxon by condensing into ambiguities (= polymorphisms) all base-pair differences among clones. This data set was chosen for further analysis because it retained all base-pair variations present within taxa and did not inflate the number of autapomorphic characters.
Congruence among data sets within each genome was determined by the incongruence length difference test (partition homogeneity test option in PAUP*) using 100 bi-partitions of the data. The condensed ETS and PEPC intron data sets were combined by concatenating sequence data of nonhybrid taxa and by inserting missing data in hybrid clone sequences such that all hybrid clones were included as individual terminal taxa in the expanded aligned data set. Data sets of the rps16 intron and psbA-trnH spacer were combined similarly.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
|
|
|
Chloroplast markers
Parsimony analysis of rps16 intron sequence data, including those cloned copies from the putative interspecific hybrids, yielded four trees of 52 steps (Fig. 12). Of 842 characters in the aligned matrix, 793 were constant, 26 were autapomorphic, and 23 were informative. Clones of Bursera brunea clustered only in the B. nashii clade (none to two sites), and clones of B. gracilipes clustered only in the B. spinescens clade (none to three sites). Bursera ovata, which was represented by an uncloned sequence, nested in the unresolved B. simaruba-B. longipes clade. Parsimony analysis of the psbA-trnH intergenic spacer region yielded 16 trees of 56 steps (Fig. 13). Of 557 characters in the aligned matrix, 510 were constant, 20 were autapomorphic, and 27 were informative. Clones of B. gracilipes clustered in the B. spinescens clade (one site) and clones of B. brunea clustered in the unresolved clade (no sites) containing B. nashii, B. frenningae, and B. inaguensis. The uncloned sequence of B. ovata was reduced to a polytomy with B. simaruba and B. longipes.
Combined genome data sets
Nonsignificant results from incongruence length difference tests of the nuclear (1024 bp) and chloroplast (1399 bp) data sets established that each was internally congruent (P = 0.57, 0.52, respectively). Parsimony and bootstrap analyses of the combined nuclear and combined chloroplast data sets (figures not shown) gave results consistent with those from the individual data sets.
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
, 1996
). The presence of a single chloroplast haplotype in each putative Bursera hybrid indicates that the inheritance of the chloroplast genome is uniparental but does not prove that inheritance is maternal in all cases. We assume that inheritance of plastids in Bursera is maternal, as is the case in most (73%) angiosperms (Harris and Ingram, 1991
). Bursera spinescens is indicated as the maternal parent of B. gracilipes, whereas B. nashii is indicated as the maternal parent of B. brunea. Bursera gracilipes and B. brunea also combine the nuclear alleles of their maternal parents and their other hypothesized parent species, B. simaruba, which demonstrates the genetic additivity of their hybrid nuclear genomes. Thus, we can infer from these results that B. gracilipes equals B. spinescens (
) x B. simaruba (
) and that B. brunea equals B. nashii () x B. simaruba ().
It is impossible to determine from the phylogenies of Hispaniolan Bursera whether B. gracilipes and B. brunea represent F1 generation hybrids or later backcrosses because of the erratic behavior of concerted evolution. Studies of molecular evolution in hybrid as well as nonhybrid plants have revealed that paralogous copies of the nrDNA repeat may be maintained in ancient lineages despite sexual recombination and cladogenesis (cf., Winteraceae, Suh et al., 1993
; Paeonia, Sang et al., 1995
; Gossypium, Wendel et al., 1995
; Pinus, Gernandt et al., 2001
; Quercus, Muir et al., 2001
). Investigation of the reproductive biology in these hybrids would help explain the origin and persistence of these divergent nuclear alleles. For instance, if the hybrids cannot reproduce sexually, as has been documented for B. medranoana, persistence of interspecific copies would suggest that it is a F1 hybrid. In the absence of meiosis, concerted evolution has been shown to proceed slowly (Amelanchier, Campbell et al., 1997
) although gene conversion (Hillis et al., 1991
) can still occur.
Phylogenetic incongruence of Bursera ovata between nuclear and chloroplast phylogenies indicates a more complicated evolutionary history for this species. In nuclear phylogenies, all clones of nuclear markers for B. ovata nested with those of B. spinescens, whereas in chloroplast phylogenies B. ovata either nested in resolved clades or polytomies with B. simaruba. The existence of unobserved B. simaruba nuclear alleles in B. ovata is improbable based on the fact that cloning studies of two nuclear markers failed to isolate them and the fact that both nuclear markers can be sequenced directly without cloning. Lineage sorting may be responsible for the loss of ancestral polymorphic nuclear alleles although this phenomenon is not observed among the multiple copies of ETS present in nonhybrid Bursera taxa (Fig. 9). If B. ovata is derived from hybridization, it would represent B. simaruba () x B. spinescens (), which is the reciprocal of B. gracilipes (= B. spinescens x B. simaruba). However, the lack of nuclear markers from B. simaruba in B. ovata does not confirm whether B. ovata is a stabilized hybrid taxon, a backcross generation, or merely a well-homogenized F1.
One of the hypothesized mechanisms of concerted evolution is unequal crossing over during meiosis, which reduces and eventually eliminates heterogeneous alleles of high-copy gene regions in the gamete haploid genome (Hillis and Dixon, 1991
). Complete elimination of heterogeneous copies either by uneven crossing over or by gene conversion can require multiple backcross generations (Armeria, Fuertes Aguilar et al., 1999
) or may happen immediately during F1 formation (Zea, Zimmer et al., 1988
). Repeated backcrossing of B. simaruba x B. spinescens (as the maternal parent) to B. spinescens (as the paternal parent) could also reduce or eliminate the number of maternally inherited copies of nuclear alleles from B. simaruba within the hybrid lineage. In this sense, B. ovata could represent the introgression of B. simaruba cytoplasm into a B. spinescens nuclear genetic background. Given that sterility barriers between species of Hispaniolan Bursera appear to be low, the backcross scenario may be a more probable explanation for the phylogenetic incongruence of B. ovata than the other alternatives discussed.
Additional tests of the reproductive biology of all Hispaniolan Bursera species and finer-scale genetic investigations of multiple accessions of the hybrids are needed to determine whether these hybrids are first generation hybrids, backcross generations, or stabilized species. Trees identified as B. ovata, B. brunea, and B. gracilipes have been collected from multiple localities within low-elevation, arid, karstic habitats of Barahona and Pedernales Provinces in the southeastern portion of the Dominican Republic as well as from Haiti (except B. ovata). None of the hybrids may represent a stable species; instead, each may be an assemblage of independently derived hybrids or backcross generations. The long life cycle of Bursera precludes breeding experiments that might investigate the long-term genetic fate of these interspecific hybrids. In one study of population dynamics of Bursera in the Galápagos, individual trees were estimated to have a 200-year lifespan (Hamann, 2001
) although no published data about the reproductive phenology of Bursera exist. Natural hybrid zones, such as the region in southwestern Dominican Republic, offer a chance to observe multiple hybrid generations with varying genetic backgrounds simultaneously. Their value is tempered by the fact that detrimental epistatic interactions between genomes (Rieseberg and Buerkle, 2002
; Levin, 2003
) and other unfit hybrid combinations are less likely to be observed due to natural selection.
Of the 17 Bursera species distributed in the Caribbean, 15 belong to B. subgenus Bursera and 15 are endemic to this region (Table 2). These endemic species include B. inaguensis, B. spinescens, and B. ovata, which have been transferred to Commiphora (Moncada-Ferrera, 1989
; Borhidi, 1992
) but are clearly part of B. subg. Bursera based on our phylogenetic results. The long history of Bursera collection in the Caribbean may have resulted in redundant species descriptions and, as a result, precise enumeration of all Caribbean Bursera species will require a taxonomic revision. Interestingly, our phylogenetic analyses suggest that nonhybrid Bursera species endemic to the Caribbean share a common ancestor (Fig. 11). The need for a revision of Caribbean Bursera is highlighted further by results of this study that indicate interspecific hybridization can complicate species identification (e.g., B. brunea, B. gracilipes, and B. ovata). It is possible that other described species of Caribbean Bursera may be interspecific hybrids that involve the widespread species B. simaruba and the island endemic species.
|
). The two interspecific hybrids collected in the Dominican Republic, B. brunea and B. gracilipes, may be sterile like B. medranoana but await further experimental field tests. Bursera ovata may be a sexually reproducing, stabilized hybrid taxon or a backcross generation. In either scenario, the sexual reproduction of B. ovata could have significant implications for interpreting the evolutionary history of Bursera. Cross-breeding experiments of Bursera species and genetic tests of seed progeny should reveal the ease with which hybrid combinations can form.
|
FOOTNOTES |
|---|
2 E-mail: aweeks{at}mail.utexas.edu
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Andersson L. 2001 Margaritopsis (Rubiaceae, Psychotrieae) is a pantropical genus. Systematics and Geography of Plants 71: 73-85[CrossRef]
Andersson L. J. H. E. Rova 1999 The rps16 intron and the phylogeny of the Rubioideae (Rubiaceae). Plant Systematics and Evolution 214: 161-168[CrossRef][ISI]
Baldwin B. G. S. Markos 1998 Phylogenetic utility of the external transcribed spacer (ETS) of 18S–26S rDNA: congruence of ETS and its trees of Calycadenia (Compositae). Molecular Phylogenetics and Evolution 10: 449-463[CrossRef][ISI][Medline]
Becerra J. X. 1997 Insects on plants: macroevolutionary chemical trends in host use. Science 276: 253-256
Becerra J. X. 2003 Evolution of Mexican Bursera (Burseraceae) inferred from ITS, ETS, and 5S nuclear ribosomal DNA sequences. Molecular Phylogenetics and Evolution 26: 300-309[CrossRef][ISI][Medline]
Becerra J. X. D. L. Venable 1999 Nuclear ribosomal DNA phylogeny and its implication for evolutionary trends in Mexican Bursera (Burseraceae). American Journal of Botany 86: 1047-1057
Bena G. M.-F. Jubier I. Olivieri B. Lejeune 1998 Ribosomal external and internal transcribed spacers: combined use in the phylogenetic analysis of Medicago (Leguminosae). Journal of Molecular Evolution 46: 299-306[CrossRef][ISI][Medline]
Borhidi A. 1992 New names and new species in the flora of Cuba and Antilles, IV. Acta Botanica Hungarica 37: 75-90
Bullock A. A. 1936 Notes on the Mexican species of the genus Bursera. Bulletin of Miscellaneous Information, Kew 1936: 346-387[CrossRef]
Bullock A. A. 1937 Further notes on the genus Bursera. Bulletin of Miscellaneous Information, Kew 1937: 447-457[CrossRef]
Bullock A. A. 1938 Further notes on the genus Bursera. Bulletin of Miscellaneous Information, Kew 1938: 163-168[CrossRef]
Campbell C. S. M. F. Wojciechowski B. G. Baldwin L. A. Alice M. J. Donoghue 1997 Persistent nuclear ribosomal DNA sequence polymorphism in the Amelanchier agamic complex (Rosaceae). Molecular Biology and Evolution 14: 81-90[Abstract]
Corriveau J. L. A. W. Coleman 1988 Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. American Journal of Botany 75: 1443-1458[CrossRef][ISI]
Cortés-Palomec A. 1998 Biología reproductiva de Bursera medranoana Rzedowski and Ortiz (Burseraceae), una especie de orígen híbrido. Tesis de licentura, Universidad Nacional Autónoma de México, México, Districto Federal, México
Cuatrecasas J. 1957 Prima flora colombiana, 1. Burseraceae. Webbia XII 426-433
Doyle J. J. J. L. Doyle 1987 A rapid DNA isolation procedure for small quantities of fresh leaf material. Phytochemical Bulletin 19: 11-15
Edwards K. J. P. A. Gadek 2001 Evolution and biogeography of Alectryon (Sapindaceae). Molecular Phylogenetics and Evolution 20: 14-26[CrossRef][ISI][Medline]
Francis J. K. 1990 Bursera simaruba (L.) Sarg. United States Department of Agriculture Research Paper SO-ITS-SM-35: 1-5
Fuertes Aguilar J. J. A. Rossello G. Nieto Feliner 1999 Nuclear ribosomal DNA (nrDNA) concerted evolution in natural and artificial hybrids of Armeria (Plumbaginaceae). Molecular Ecology 8: 1341-1346[CrossRef][Medline]
Gehrig H. H. V. Heute M. Kluge 1998 Toward a better knowledge of the molecular evolution of phosphoenolpyruvate by comparison of partial cDNA sequences. Journal of Molecular Evolution 46: 107-114[CrossRef][ISI][Medline]
Gene Codes. 1995 Sequencher, version 4.0. Gene Codes, Ann Arbor, Michigan, USA
Gernandt D. S. A. Liston D. Piñero 2001 Variation in the nrDNA ITS of Pinus subsection Cembroides: implications for molecular systematic studies of pine species complexes. Molecular Phylogenetics and Evolution 21: 449-467[CrossRef][ISI][Medline]
Gilbert D. G. 1992 SeqApp, version 1.9a169. Distributed by the author, website: ftp//:ftp.bio.indiana.edu /molbio/seqapp
Hagemann R. M.-B. Schröder 1989 The cytological basis of the plastid inheritance in angiosperms. Protoplasma 152: 57-64[CrossRef][ISI]
Hamann O. 2001 Demographic studies of three indigenous stand-forming plant taxa (Scalesia, Opuntia, and Bursera) in the Galápagos Islands, Ecuador. Biodiversity and Conservation 10: 223-250[CrossRef][ISI]
Harris S. A. R. Ingram 1991 Chloroplast DNA and biosystematics: the effects of intraspecific diversity and plastid transmission. Taxon 40: 393-412
Hillis D. M. M. T. Dixon 1991 Ribosomal DNA: molecular evolution and phylogenetic inference. Quarterly Review in Biology 66: 411-453[CrossRef]
Hillis D. M. C. Moritz C. A. Porter R. J. Baker 1991 Evidence for biased gene conversion in concerted evolution of ribosomal DNA. Science 251: 308-310
Hitchen J. E. Ivakine Y. F. Melekhovets A. Lalev R. N. Nazar 1997 Structural features in the 3' external transcribed spacer affecting intragenic processing of yeast rRNA. Journal of Molecular Biology 274: 481-490[CrossRef][ISI][Medline]
Keim P. K. N. Paige K. G. Lark 1989 Genetic analysis of an interspecific hybrid swarm of Populus: occurrence of unidirectional introgression. Genetics 123: 557-565
Kelchner S. A. 2002 Group II introns as phylogenetic tools: structure, function, and evolutionary constraints. American Journal of Botany 89: 1651-1669
Kim S.-C. D. J. Crawford R. K. Jansen A. Santos-Guerra 1999 The use of a non-coding region of chloroplast DNA in phylogenetic studies of the subtribe Sonchinae (Asteraceae: Lactuceae). Plant Systematics and Evolution 215: 85-99[CrossRef][ISI]
Latzko E. G. J. Kelly 1983 The many-faceted function of phosphoenolpyruvate carboxylase in C3 plants. Physiologie Vegetale 21: 805-815
Levin D. A. 2003 The cytoplasmic factor in plant speciation. Systematic Botany 28: 5-11
Linder C. R. L. R. Goertzen B. Vanden Heuvel J. Francisco-Ortega R. K. Jansen 2000 The external transcribed spacer of the rDNA repeat: a nuclear region for low-level taxonomic analysis of the Asteraceae and closely allied families. Molecular Phylogenetics and Evolution 14: 285-303[CrossRef][ISI][Medline]
Maddison W. P. D. R. Maddison 2000 MacClade, version 4.0. Sinauer, Sunderland, Massachusetts, USA
Markos S. B. G. Baldwin 2001 Higher-level relationships and major lineages of Lessingia (Compostiae, Asteraceae) based on nuclear rDNA internal and external transcribed spacer (ITS and ETS) sequences. Systematic Botany 26: 168-183[ISI]
McVaugh R. J. Rzedowski 1965 Synopsis of the genus Bursera L. in western Mexico, with notes on the material of Bursera collected by Sessé and Mociño. Kew Bulletin 18: 317-346[CrossRef]
Milne R. I. R. J. Abbott K. Wolff D. F. Chamberlain 1999 Hybridization among sympatric species of Rhododendron (Ericaceae) in Turkey: morphological and molecular evidence. American Journal of Botany 86: 1776-1785
Moncada-Ferrara M. 1989 Reporte del género Commiphora Jacq. (Burseraceae) para Cuba. Revista del Jardin Botanico Nacional X 3-9
Muir G. C. C. Fleming C. Schlötterer 2001 Three divergent rDNA clusters predate the species divergence in Quercus petraea (Matt.) Liebl. and Quercus robur L. Molecular Biology and Evolution 18: 112-119
Musters W. K. Boon C. A. M. F. van der Sande H. van Heerikhuizen R. Planta 1990 Functional analysis of transcribed spacers of yeast ribosomal DNA. The EMBO Journal 9: 3989-3996[ISI][Medline]
Olson M. E. 2002 Combining data from DNA sequences and morphology for a phylogeny of Moringaceae (Brassicales). Systematic Botany 27: 55-73
Oxelman B. M. Liden D. Berlund 1997 Chloroplast rps16 intron phylogeny of the tribe Sileneae (Carophyllaceae). Plant Systematics and Evolution 206: 393-410[CrossRef][ISI]
Palmer J. D. 1985 Comparative organization of chloroplast genomes. Annual Review of Genetics 19: 325-354[CrossRef][ISI][Medline]
Palmer J. D. 1986 Isolation and structural analysis of chloroplast DNA. Methods in Enzymology 118: 167-186[ISI]
Popp M. B. Oxelman 2001 Inferring the history of the polyploid Silene aegaea (Caryophyllaceae) using plastid and homeologous nuclear DNA sequences. Molecular Phylogenetics and Evolution 20: 474-481[CrossRef][ISI][Medline]
Rieseberg L. H. 1990 Molecular tests of the hypothesized hybrid origin of two diploid Helianthus species (Asteraceae). Evolution 44: 1498-1511[CrossRef][ISI]
Rieseberg L. H. 1996 Molecular marker incongruence in plant hybrid zones and phylogenetic trees. Acta Botanica Neerlandica 45: 243-262[ISI]
Rieseberg L. H. C. A. Buerkle 2002 Genetic mapping in hybrid zones. American Naturalist 159: S36-S50[CrossRef][ISI]
Rzedowksi J. 1968 Notas sobre el género Bursera (Burseraceae) en el estado de Guerrero (México). Anales de la Escuela Nacional des Ciencias Biológicas de México 17: 17-36
Rzedowski J. 1978 Vegetación de México. Limusa, México, Districto Federal, México
Rzedowski J. 1988 Diversity and origins of the phanerogamic flora of Mexico. In T. P. Ramamoorthy, R. Bye, A. Lot, and J. Fa [eds.], Biological diversity of Mexico: Origins and distribution, 129–144. Oxford University Press, Oxford, UK
Rzedowski J. F. Guevara-Féfer 1992 Familia Burseraceae. In J. Rzedowski and G. Calderón de Rzedowski [eds.], Flora del Bajío y regiones adyacentes, 1–46. Instituto de Ecología, A. C. Central Regional del Bajío, Pátzcuaro, Michoacán, México
Rzedowski J. H. Kruse 1979 Algunas tendencias evolutivas en Bursera (Burseraceae). Taxon 28: 103-116[CrossRef][ISI]
Rzedowski J. E. Ortiz 1988 Estudios quimotaxonómicos de Bursera (Burseraceae). II. Una especie de nueva origen híbrido de la Barranca de Tolantongo, estado de Hidalgo. Acta Botánica Mexicana 1: 11-19
Sang T. 2002 Utility of low-copy nuclear gene sequences in plant phylogenetics. Critical Reviews in Biochemistry and Molecular Biology 37: 121-147[CrossRef][ISI][Medline]
Sang T. D. J. Crawford T. F. Stuessy 1997 Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). American Journal of Botany 84: 1120-1136[Abstract]
Stebbins G. L. 1950 Variation and evolution in plants. Columbia University Press, New York, New York, USA
Suh Y. L. B. Thein H. E. Reeve E. A. Zimmer 1993 Molecular evolution and phylogenetic implications of internal transcribed spacer sequences of ribosomal DNA in Winteraceae. American Journal of Botany 80: 1042-1055[CrossRef][ISI]
Swofford D. L. 2002 PAUP*. Phylogenetic analysis using parsimony (* and other methods), version 4 b10. Sinauer, Sunderland, Massachusetts, USA
Thompson J. D. T. J. Gibson F. Plewniak F. Jeanmougin D. G. Higgins 1997 The ClustalX windows interface: flexible strategies for multiple alignments aided by quality analysis tools. Nucleic Acids Research 25: 4876-4882
Toledo-Manzur C. A. 1982 El género Bursera (Burseraceae) en el estado de Guerrero (México). Tesis profesional, Universidad Nacional Autónoma de México, México, Districto Federal, México
Urban I. 1929 Plantae Haitienses et Domingenses novae vel rariores V. a cl. E.L. Ekman 1924–27 lectae. Arkiv för Botanik 22A: 1-98
Utelli A.-B. B. A. Roy M. Baltisberger 2000 Molecular and morphological analyses of European Aconitum species (Ranunculaceae). Plant Systematics and Evolution 224: 195-212[CrossRef][ISI]
Vanden Heuvel B. C. R. Linder 1999 Use of a novel nuclear region of DNA for phylogenetic reconstruction of Cercocarpus H.B.K. (Rosaceae). XVI International Botanical Congress Abstracts: 436
Weeks A. 2003 The molecular systematics and biogeography of the Burseraceae. Ph.D. dissertation, The University of Texas at Austin, Austin, Texas, USA
Wendel J. F. A. Schnabel T. Seelanan 1995 Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proceedings of the National Academy of Sciences, USA 92: 280-284
Westhoff P. U. Gowik 2004 Evolution of C4 phosphoenolpyruvate carboxylase. Genes and proteins: a case study with the genus Flaveria. Annals of Botany 93: 13-23
Whittemore A. T. B. A. Schaal 1991 Interspecific gene flow in sympatric oaks. Proceedings of the National Academy of Sciences, USA 88: 2540-2544
Wiggins I. L. D. M. Porter 1971 Flora of the Galápagos Islands. Stanford University Press, Stanford, California, USA
Wolfe A. D. W. J. Elisens 1993 Diploid hybrid speciation in Penstemon (Scrophulariaceae) revisited. American Journal of Botany 80: 1082-1094[CrossRef][ISI]
Wright S. D. C. G. Yong S. R. Wichman J. W. Dawson R. C. Gardner 2001 Stepping stones to Hawaii: a trans-equatorial dispersal pathway for Metrosideros (Myrtaceae) inferred from nrDNA (ITS + ETS). Journal of Biogeography 28: 769-774[CrossRef][ISI]
Zimmer E. A. E. R. Jupe V. Walbot 1988 Ribosomal gene structure, variation and inheritance in maize and its ancestors. Genetics 120: 1125-1136
This article has been cited by other articles:
|
|
 |
|
  P. Lubinsky, K. M. Cameron, M. C. Molina, M. Wong, S. Lepers-Andrzejewski, A. Gomez-Pompa, and S.-C. Kim Neotropical roots of a Polynesian spice: the hybrid origin of Tahitian vanilla, Vanilla tahitensis (Orchidaceae) Am. J. Botany, August 1, 2008; 95(8): 1040 - 1047. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. D Noyes Intraspecific nuclear ribosomal DNA divergence and reticulation in sexual diploid Erigeron strigosus (Asteraceae) Am. J. Botany, March 1, 2006; 93(3): 470 - 479. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||
