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Representatives of seven sections of Buddleja in revised classification of Buddlejeae. (A) Buddleja salviifolia, section Salviifoliae, (B) Buddleja virgata, section Gomphostigma, (C) Buddleja saligna, section Chilianthus, (D) Buddleja pulchella, section Pulchellae, (E) Buddleja madagascariensis, section Nicodemia, (F) Buddleja davidii, section Alternifoliae, (G) Buddleja nitida, section Buddleja, (H) Buddleja anchoensis, section Buddleja. All photographs by J.H. Chau.
Source publication
Buddlejeae comprise c. 108 species in five commonly accepted genera: Buddleja, Chilianthus, Emorya, Gomphostigma
and Nicodemia. Conflicting generic and infrageneric level classifications based on morphology attest to a need to
evaluate relationships and trait evolution in a molecular phylogenetic framework. We use multiple independent loci
from the...
Context in source publication
Context 1
... species found in North and South America are placed in section Buddleja, including members of Emorya. Circumscriptions and species names in revised clas- sification are listed in Table A4 and select representa- tives of sections are shown in Figure 4. . Section Nicodemia (Tenore) Leeuwenberg, Meded. ...
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p> Background: Echeveria and Pachyphytum are two closely related Neotropical genera in the Crassulaceae. Several species in Echeveria possess characters cited as diagnostic for Pachyphytum such as a clearly defined stem, a nectary scale on the inner face of petals and as inflorescence a scorpioid cyme or cincinnus. Pachyphytum has been identified a...
Citations
... Though several recent phylogenetic studies have explored the spatiotemporal evolution of less inclusive groups, tribes, or genera, within Scrophulariaceae (G andara & Sosa, 2013;Navarro-P erez et al., 2013;Chau et al., 2017;Culshaw et al., 2021), there has been no attempt yet to reconstruct the biogeographic origins and lineage divergence times across the entire family. Some authors have ventured hypotheses regarding the origin of the family or specific taxa. ...
... For example, Oxelman et al. (2005) defined Scrophulariaceae as a mainly Southern Hemisphere family with Southern African ancestors, for which northern hemisphere Scrophularieae is the main exception. Chau et al. (2017) found a strong geographical signal at the continental level in infrageneric relationships in Buddlejeae, in which Southern African species formed a basal grade within the tribe, with two major clades distributed in the Old and New Worlds. The only family-level biogeographic analysis is Culshaw et al. (2021). ...
The figwort family, Scrophulariaceae, comprises c. 2000 species whose evolutionary relationships at the tribal level have proven difficult to resolve, hindering our ability to understand their origin and diversification.
We designed a specific probe kit for Scrophulariaceae, targeting 849 nuclear loci and obtaining plastid regions as by‐products. We sampled c. 87% of the genera described in the family and use the nuclear dataset to estimate evolutionary relationships, timing of diversification, and biogeographic patterns.
Ten tribes, including two new tribes, Androyeae and Camptolomeae, are supported, and the phylogenetic positions of Androya, Camptoloma, and Phygelius are unveiled. Our study reveals a major diversification at c. 60 million yr ago in some Gondwanan landmasses, where two different lineages diversified, one of which gave rise to nearly 81% of extant species. A Southern African origin is estimated for most modern‐day tribes, with two exceptions, the American Leucophylleae, and the mainly Australian Myoporeae. The rapid mid‐Eocene diversification is aligned with geographic expansion within southern Africa in most tribes, followed by range expansion to tropical Africa and multiple dispersals out of Africa.
Our robust phylogeny provides a framework for future studies aimed at understanding the role of macroevolutionary patterns and processes that generated Scrophulariaceae diversity.
... The genus Buddleja consists of 108 woody species (Chau et al. 2017). Most of the diversity is found in the New World section Buddleja (66 species) and Asian sect. ...
... Salviifoliae or sect. Gomphostigma (Chau et al. 2017). ...
... Sixteen species of Buddleja (Buddlejeae, Scrophulariaceae; 19 specimens) were sampled: 14 species (17 specimens) were obtained from plants cultivated in the National Buddleja Collection at Longstock Park Nursery (Stockbridge, Hampshire, United Kingdom), one specimen of B. incompta came from a natural population (Sutherland, Northern Cape, South Africa), and a sample of B. saligna was obtained from a cultivated tree (Johannesburg, Gauteng, South Africa). Chau et al. (2017) that was supported by subsequent bark anatomical analyses by Frankiewicz et al. (2020), with sect. Gomphostigma marked in blue dashed line (representing uncertain position), and African taxa in bold. ...
Background
Bark (all tissues outside of the vascular cambium) has been extensively studied in recent years, especially its anatomy and physiology. Macromorphological bark characters can be important taxonomically for many plant groups, including the genus Buddleja (Scrophulariaceae). However, the relationship between macroscopic bark appearance and its microscopic structure remains obscure, hampering the use and interpretation of bark traits in plant taxonomy and phylogenetics as well as in other fields of botany. We studied micro- and macrostructure of bark in the species of Buddleja representing wide taxonomic and geographic diversity to identify general relationships between bark anatomy and morphology. We also examined Buddleja xylem and discussed the importance of anatomical traits for understanding the relationships between clades in this genus.
Results
The smooth bark surface in sect. Gomphostigma and the outgroup (Freylinia spp.) relates to the small number of periderms of superficial origin and limited sclerification. This allows for the retention of visible lenticels. In the rest of Buddleja, bark sloughs off and division of labour is present: collapsed phloem undergoes sclerification and acts as a protective layer, while thin-walled phellem forms the separation layers. A similar pattern is found in some groups (e.g., Lonicera), but in others (e.g., Vitis and the species of Eucalyptus with stringy bark), the pattern is inversed. Wood and bark anatomy supports a sister relationship between the southern African section Gomphostigma and the rest of Buddleja but is taxonomically uninformative among remaining clades.
Conclusions
Limited development of periderms and sclerification allow for the retention of a smooth bark surface and conspicuous lenticels. Sloughing off of bark requires division of labour into a lignified protective layer and a thin-walled separation layer. These two functions are never served by a single tissue but are rather divided between phloem and periderm. How more subtle features (e.g., size and shape of fissures) are determined requires further study. Simultaneously, bark anatomy could be a useful source of data to complement molecular phylogenetic studies in a total evidence approach for systematics.
... Dispersal between the two continents was possible by dispersal over the Tethys Sea from Africa to Asia directly, or to Australasia via India, which is thought to have had connections to Africa via the Kohistan-Ladakh Island Arc as it drifted northward toward Asia (Morley, 2018). Examples of plant groups that have dispersed from Africa to continental Asia are Annonaceae (Couvreur et al., 2011), Asteraceae (Funk et al., 2005), Begonia (Rajbhandary et al., 2011), and Buddleja (Chau et al., 2017). Conversely, the reverse dispersal path from Asia to Africa also would have been possible via the same routes, if the initial dispersal event was from South America to Australasia. ...
Intercontinental disjunct distributions can arise from vicariance, long distance dispersal, or both. Tecomeae (Bignoniaceae) are a nearly cosmopolitan clade of flowering plants providing us with an excellent opportunity to investigate global distribution patterns. While the tribe contains only about 57 species, it has achieved a distribution that is not only pantropical, but also extends into the temperate zones in both the Northern and Southern hemispheres. This distribution is similar to the distribution of its sister group, a clade of about 750 spp. that includes most remaining taxa in Bignoniaceae. To infer temporal and spatial patterns of dispersal, we generated a phylogeny of Tecomeae by gathering sequence data from chloroplast and nuclear markers for 41 taxa. Fossil calibrations were used to determine divergence times, and ancestral states were reconstructed to infer its biogeographic history. We found support for a South American origin and a crown age of the tribe estimated at ca. 40 Ma. Two dispersal events seem to have happened during the Eocene-Oligocene, one from South America to the Old World, and another from South America to North America. Furthermore, two other dispersal events seem to have taken place during the Miocene, one from North America to Asia, and another from Australia to South America. We suggest that intercontinental dispersal via land bridges and island hopping, as well as sweepstakes of long distance dispersal from the Eocene to the present explain the global distribution of Tecomeae.
... Genus Camptoloma was placed as sister to tribes Buddlejeae and Teedieae. The first includes the cosmopolitan genus Buddleja L. (~108 species) and four other genera with a mostly South African distribution (Chilianthus, Nicodemia, Gomphostigma, and Emorya) have been recently synonymized within a larger Buddleja (Chau et al., 2017). The second is composed of six genera (Teedia, Freylinia, Oftia, Dermatobrothys, Phygelius, and Ranopisoa) and only 12 species distributed in southern Africa. ...
... Because the branch of Plantago was so long and uninformative, the tree was pruned to remove its branch. Note that genera Gomphostigma and Emorya are now synonymized within genus Buddleja (Chau et al., 2017). *: Samples used in the Hyb-Seq phylogenomic study, †: Samples used for both Sanger and Hyb-Seq phylogenomic studies A B F I G U R E 3 (See caption on next page) ...
... Symbol * next to a taxon name indicates the number of markers that failed sequencing for that taxon. Note that genera Gomphostigma and Emorya are now synonymized within genus Buddleja (Chau et al., 2017) F I G U R E 4 Bayesian biogeographic reconstruction of Camptoloma and representative outgroups in Scrophulariaceae using the Dispersal-Extinction-Cladogenesis (DEC) model implemented in RevBayes. The phylogeny is the MCC tree from the nested-dating analysis of the outgroup dataset ( Figure 3A), where the tree was pruned to leave one individual per species. ...
Premise:
Genera that are widespread, with geographically discontinuous distributions and represented by few species, are intriguing. Is their achieved disjunct distribution recent or ancient in origin? Why are they species-poor? The Rand Flora is a continental-scale pattern in which closely related species appear codistributed in isolated regions over the continental margins of Africa. Genus Camptoloma (Scrophulariaceae) is the most notable example, comprising three species isolated from each other on the northwest, eastern, and southwest Africa.
Methods:
We employed Sanger sequencing of nuclear and plastid markers, together with genomic target sequencing of 2190 low-copy nuclear genes, to infer interspecies relationships and the position of Camptoloma within Scrophulariaceae by using supermatrix and multispecies-coalescent approaches. Lineage divergence times and ancestral ranges were inferred with Bayesian Markov chain Monte Carlo (MCMC) approaches. The population history was estimated with phylogeographic coalescent methods.
Results:
Camptoloma rotundifolium, restricted to Southern Africa, was shown to be a sister species to the disjunct clade formed by C. canariense, endemic to the Canary Islands, and C. lyperiiflorum, distributed in the Horn of Africa-Southern Arabia. Camptoloma was inferred to be sister to the mostly South African tribes Teedieae and Buddlejeae. Stem divergence was dated in the Late Miocene, while the origin of the extant disjunction was inferred as Early Pliocene.
Conclusions:
The current disjunct distribution of Camptoloma across Africa was likely the result of fragmentation and extinction and/or population bottlenecking events associated with historical aridification cycles during the Neogene; the pattern of species divergence, from south to north, is consistent with the "climatic refugia" Rand Flora hypothesis.
... The divergence time of B. alternifolia from B. globosa was set to the range of 8.5-25.0 Ma, according to the estimate by Chau (2017). ...
... Fastsimcoal analysis however, showed that HDM diverged from LP < 1000 years after the divergence of the Himalaya, around 2.3 Ma, only 0.6 Ma after the divergence of B. alternifolia itself (Chau, 2017). However, BioGeoBEARS indicated that divergence occurred by vicariance, rather than dispersal. ...
Understanding processes that generate and maintain large disjunctions within plant species can provide valuable insights into plant diversity and speciation. The butterfly bush Buddleja alternifolia has an unusual disjunct distribution, occurring in the Himalaya, Hengduan Mountains (HDM) and the Loess Plateau (LP) in China.
We generated a high‐quality, chromosome‐level genome assembly of B. alternifolia, the first within the family Scrophulariaceae. Whole‐genome re‐sequencing data from 48 populations plus morphological and petal colour reflectance data covering its full distribution range were collected.
Three distinct genetic lineages of B. alternifolia were uncovered, corresponding to Himalayan, HDM and LP populations, with the last also differentiated morphologically and phenologically, indicating occurrence of allopatric speciation likely to be facilitated by geographic isolation and divergent adaptation to distinct ecological niches. Moreover, speciation with gene flow between populations from either side of a mountain barrier could be under way within LP. The current disjunctions within B. alternifolia might result from vicariance of a once widespread distribution, followed by several past contraction and expansion events, possibly linked to climate fluctuations promoted by the Kunlun–Yellow river tectonic movement. Several adaptive genes are likely to be either uniformly or diversely selected among regions, providing a footprint of local adaptations.
These findings provide new insights into plant biogeography, adaptation and different processes of allopatric speciation.
... These loci were successful in resolving phylogenetic relationships among the species of the Lantana/Lippia clade. In addition to the ITS and ETS regions, which are linked as part of the nuclear ribosomal repeat, the remaining loci are members of the pentatrichopeptide repeat (PPR) gene family, which have proven useful for phylogenetic inference in plants (Yuan et al., 2009a(Yuan et al., , 2009bLu-Irving and Olmstead, 2013;Crowl et al., 2014;Lu-Irving et al., 2014;Chau et al., 2017Chau et al., , 2018, including in targeted sequence capture approaches using next-generation sequencing methods, where they exceed other commonly used targeted sequence markers in terms of both average sequence length and variability (Chau et al., 2018). ...
Premise:
Lantana and Lippia (Verbenaceae) are two large Linnean genera whose classification has been based on associated fruit traits: fleshy vs. dry fruits and one vs. two seed-bearing units. We reconstruct evolutionary relationships and the evolution of the two fruit traits to test the validity of these traits for classification.
Methods:
Previous studies of plastid DNA sequences provided limited resolution for this group. Consequently, seven nuclear loci, including ITS, ETS, and five PPR loci, were sequenced for 88 accessions of the Lantana/Lippia clade and three outgroups.
Results:
Neither Lantana nor Lippia is monophyletic. Burroughsia, Nashia, Phyla, and several Aloysia species are included within the clade comprising Lantana and Lippia. We provide a hypothesis for fruit evolution and biogeographic history in the group and their relevance for classification.
Conclusions:
Fleshy fruits evolved multiple times in the Lantana/Lippia clade and thus are not suitable taxonomic characters. Several sections of Lantana and Lippia and the small genera are monophyletic, but Lippia section Zappania is broadly paraphyletic, making circumscription of genera difficult. Lippia sect. Rhodolippia is a polyphyletic group characterized by convergence in showy bracts. Species of Lantana sect. Sarcolippia, previously transferred to Lippia, are not monophyletic. The clade originated and diversified in South America, with at least four expansions into both Central America and the Caribbean and two to Africa. The types species of Lantana and Lippia occur in small sister clades, rendering any taxonomy that retains either genus similar to its current circumscription impossible.
... The aim of this study was to test the hypothesis that B. × wardii plants are natural hybrids, in two sites in Tibet. We used three chloroplast DNA regions and four nuclear genes used in previous studies on Buddleja (nrETS, gapC2, PPR24, PPR123) [16,36] to answer the following questions: 1) Are the B. wardii plants in fact hybrids between B. crispa and B. alternifolia at these two sites? 2) If yes, are there any differences between the genetic patterns at these two hybrid zones, both of which have serious habitat disturbance, and 3) does the genetic structure of hybrid zones such as these provide clues to the mechanism of reproductive isolation between parental species? ...
... Total DNA was extracted from approximately 50 mg dried leaves using the modified cetyl trimethyl ammonium (CTAB) method [64], and then stored at − 20°C before further analyses. Three low-copy nuclear genes (gapC2, PPR24, PPR123), the nrETS region, and three plastid regions (rpl16, trnD-trnT, trnS-trnfM) that had been successfully PCR amplified in Buddleja in previous publications were selected for sequencing [16,36,65]. NrETS, gapC2 and PPR are part of the nuclear ribosomal external transcribed spacer, the gapC gene family and the pentatricopeptide repeat gene family, respectively. ...
Background
It has been recognized that a certain amount of habitat disturbance is a facilitating factor for the occurrence of natural hybridization, yet to date we are unaware of any studies exploring hybridization and reproductive barriers in those plants preferentially occupying disturbed habitats. Buddleja plants (also called butterfly bush) generally do grow in disturbed habitats, and several species with hybrid origin have been proposed, based solely on morphological evidence.
Results
In the present study, we test the hypothesis that B. × wardii is of natural hybridization origin in two sympatric populations of three taxa including B. × wardii and its parents (B. alternifolia and B. crispa) plus 4 referenced parental populations, using four nuclear genes and three chloroplast intergenic spacers, as well as with 10 morphological characters. Our results suggest that at both sites B. × wardii is likely to be a hybrid between B. alternifolia and B. crispa, and moreover, we confirm that most of the hybrids examined are F1s. That these plants are F1s is further supported by morphology, as no transgressive characters were detected. B. crispa was found to be the maternal parent in the Bahe (BH) population, from cpDNA evidence. However, in the Taji (TJ) population, the direction of hybridization was difficult to establish due to the shared cpDNA haplotypes between B. alternifolia and B. crispa, however we still predicted a similar unidirectional hybridization pattern due to results from cross-specific pollination treatments which supported the “SI × SC rule”.
Conclusions
The presence of mainly F1 hybrids can successfully impede gene flow and thus maintain species boundaries in parental species in a typical distribution of Buddleja, i.e. in disturbed habitats.
... We generated sequence data from the nuclear ribosomal locus external transcribed spacer (nrETS), two low-copy nuclear genes from the pentatricopeptide repeat (PPR) gene family (PPR24 and PPR123) [55] , one low-copy nuclear gene from the gapC gene family (gapC2) [24] , and three plastid regions (rpl16, trnD-trnT, trnS-trnfM). The nrETS region was ampli ed using the universal primers ETS-B and 18S-IGS. ...
... The gapC2 locus was ampli ed following Liao et al. [24] . The trnD-trnT region was ampli ed using the primers trnD GUC F and trnT GGU , the trnS-trnfM region with primers trnS UGA and trnfM CAU from Chau et al. [55] , and the rpl16 region with rpl16-F71 and rpl16-R1516 from Borg et al. [56] . Sequences of all the primers used are listed in Additional le 5: Table S5. ...
Background: F1 hybrids acting as a bridgehead for producing later generation hybrids can have evolutionary significance through strengthening reproductive isolation or facilitating gene flow between parental species, depending on whether backcrossing can occur. It had been suggested that the Tibetan plant Buddleja wardii was a hybrid species between B. alternifolia and B. crispa based on their sympatric distributions and the morphological characters in last century. Till now however, we still have limited evidence to prove key issues to B. wardii, like if it is of hybrid origin indeed and whether it is currently a true hybrid species already.
Results: In the present study, two sympatric populations of these three taxa were examined and compared using four nuclear genes and three chloroplast intergenic spacers, as well as with 10 morphological characters. Our results suggest that at both sites B. × wardii was likely to be a hybrids between B. alternifolia and B. crispa, and moreover, most of the hybrids present were confirmed to be F1s. This was further supported by morphology as no transgressive characters were detected. B. crispa was found to be the maternal parent in one population (BH), while in the second population (TJ), it was difficult to distinguish the hybridization direction due to shared haplotypes of cpDNA between B. alternifolia and B. crispa.
Conclusions: These results provide evidence that the natural hybrids between B. alternifolia and B. crispa mainly comprise F1 hybrids, which have subsequently been given the name B. wardii. The F1 hybrids have also contributed to strong reproductive isolation between parental species.
... We generated sequence data from the nuclear ribosomal locus external transcribed spacer (nrETS), two low-copy nuclear genes from the pentatricopeptide repeat (PPR) gene family (PPR24 and PPR123) [51] , one low-copy nuclear gene from the gapC gene family (gapC2) [24] , and three plastid regions (rpl16, trnD-trnT, trnS-trnfM). The nrETS region was ampli ed using the universal primers ETS-B and 18S-IGS. ...
... For the locus PPR24, primers PPR24-140F and PPR24-1354R were used. For the locus PPR123, primers PPR123-550F and PPR123-1890R were used [51] . The gapC2 locus was ampli ed following Liao et al. [24] . ...
... The gapC2 locus was ampli ed following Liao et al. [24] . The trnD-trnT region was ampli ed using the primers trnD GUC F and trnT GGU , the trnS-trnfM region with primers trnS UGA and trnfM CAU from Chau et al. [51] , and the rpl16 region with rpl16-F71 and rpl16-R1516 from Borg et al. [52] . Sequences of all the primers used are listed in Additional le 9: Table S9. ...
Background: F1 hybrids acting as a bridgehead for producing later generation hybrids can have evolutionary significance through strengthening reproductive isolation or facilitating gene flow between parental species, depending on whether backcrossing can occur. It had been suggested that the Tibetan plant Buddleja wardii was a hybrid species between B. alternifolia and B. crispa based on their sympatric distributions and the morphological characters in last century. Till now however, we still have limited evidence to prove key issues to B. wardii, like if it is of hybrid origin indeed and whether it is currently a true hybrid species already.
Results: In the present study, two sympatric populations of these three taxa were examined and compared using four nuclear genes and three chloroplast intergenic spacers, as well as with 10 morphological characters. Our results suggest that at both sites B. × wardii was likely to be a hybrids between B. alternifolia and B. crispa, and moreover, most of the hybrids present were confirmed to be F1s. This was further supported by morphology as no transgressive characters were detected. B. crispa was found to be the maternal parent in one population (BH), while in the second population (TJ), it was difficult to distinguish the hybridization direction due to shared haplotypes of cpDNA between B. alternifolia and B. crispa.
Conclusions: These results provide evidence that the natural hybrids between B. alternifolia and B. crispa mainly comprise F1 hybrids, which have subsequently been given the name B. wardii. The F1 hybrids have also contributed to strong reproductive isolation between parental species.
... The aim of this study was to test the hybrid origin hypothesis of B. ×wardii in two sites in Tibet. Speci cally, we used three chloroplast DNA region and four nuclear genes applied in former studies on Buddleja (nrETS, gapC2, PPR24, PPR123) [19,36] to answer the following questions: 1) Are the B. wardii plants in fact hybrids between B. crispa and B. alternifolia at these two sites? 2) If yes, are there any differences between the genetic patterns at these two hybrid zones and 3) does the genetic structure of hybrid zones such as these provide clues to the mechanism of reproductive isolation between parental species? ...
... Total DNA was extracted from approximately 50 mg dried leaves using the modi ed cetyl trimethyl ammonium (CTAB) method [63] , and then stored at -20°C before further analyses. Three low-copy nuclear genes (gapC2, PPR24, PPR123), the nrETS region, and three plastid regions (rpl16, trnD-trnT, trnS-trnfM) that had been successfully PCR ampli ed in Buddleja were selected for sequencing by previous publications [19,36,64] . NrETS, gapC2 and PPR are part of the nuclear ribosomal external transcribed spacer, the gapC gene family and the pentatricopeptide repeat gene family, respectively. ...
Background: It has been recognized that certain amount of habitat disturbance is a prerequisite for occurrence of natural hybridization, yet we are currently still not aware of any studies exploring hybridization and reproductive barriers to those plants preferably occupying disturbed habitats. Buddleja plants (also called butterfly bush) generally grow in disturbed habitat, and several species with hybrid origin only on basis of morphology evidence have been proposed.
Results: In the present study, we test the natural hybridization origin hypothesis of B. × wardii in two sympatric populations of three taxa including B. × wardii and its parents (B. alternifolia and B. crispa) plus 4 referenced parental populations, using four nuclear genes and three chloroplast intergenic spacers, as well as with 10 morphological characters. Our results suggest that at both sites B. × wardii was likely to be hybrids between B. alternifolia and B. crispa, and moreover, most of the hybrids examined were confirmed to be F1s. This was further supported by morphology as no transgressive characters were detected. B. crispa was found to be the maternal parent in Bahe (BH) population from the cpDNA. While in the Taji (TJ) population was difficult to distinguish the hybridization direction due to the shared haplotypes of cpDNA between B. alternifolia and B. crispa, we still predicted the similar unidirectional hybridization pattern due to results from cross-specific pollination treatments which supported the “SI x SC rule”.
Conclusions: Hybrids mainly consisting of F1s can successfully impede gene flow and thus maintain species boundaries of parental species in its typical distribution of Buddleja, i.e. disturbed habitats.
