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The Monophyly of Bursera and Its Impact for Divergence Times of Burseraceae

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The Monophyly of Bursera and Its Impact for Divergence Times of Burseraceae TAXON 61 (2) • April 2012: 333–343 Becerra & al. • Monophyly of Bursera The monophyly of Bursera and its impact for divergence times of Burseraceae Judith X. Becerra,1 Kogi Noge,2 Sarai Olivier1 & D. Lawrence Venable3 1 Department of Biosphere 2, University of Arizona, Tucson, Arizona 85721, U.S.A. 2 Department of Biological Production, Akita Prefectural University, Akita 010-0195, Japan 3 Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721, U.S.A. Author for correspondence: Judith X. Becerra, [email protected] Abstract Bursera is one of the most diverse and abundant groups of trees and shrubs of the Mexican tropical dry forests. Its interaction with its specialist herbivores in the chrysomelid genus Blepharida, is one of the best-studied coevolutionary systems. Prior studies based on molecular phylogenies concluded that Bursera is a monophyletic genus. Recently, however, other molecular analyses have suggested that the genus might be paraphyletic, with the closely related Commiphora, nested within Bursera. If this is correct, then interpretations of coevolution results would have to be revised. Whether Bursera is or is not monophyletic also has implications for the age of Burseraceae, since previous dates were based on calibrations using Bursera fossils assuming that Bursera was paraphyletic. We performed a phylogenetic analysis of 76 species and varieties of Bursera, 51 species of Commiphora, and 13 outgroups using nuclear DNA data. We also reconstructed a phylogeny of the Burseraceae using 59 members of the family, 9 outgroups and nuclear and chloroplast sequence data. These analyses strongly confirm previous conclusions that this genus is monophyletic. New calculations of the age of Burseraceae date the beginning of its diversification to at least 93 million years ago. Keywords Bursera ; Burseraceae; divergence times; monophyly; phylogeny Supplementary Material The alignment files are available in the Supplementary Data section of the online version of this article (http://www.ingentaconnect.com/content/iapt/tax). INTRODUCTION & Venable, 1999a; Becerra & al., 2009). Phylogenetic relation- ships of Bursera and Blepharida have been central for testing Bursera Jacq. ex L. comprises about 105 species distrib- aspects of coevolution (Becerra, 2007; Becerra & al., 2009). uted from southern U.S. to Peru and the Caribbean. Most of Because of the tightness of their relationships and high degree the species (~ 85%) are endemic to Mexico, where they are of coadaptation, Bursera and Blepharida are now considered some of the most conspicuous woody members of the floras one of the model systems to study plant–herbivore coevolution of arid and semiarid regions (Rzedowski, 1978; Rzedowski (Hillis, 1997; Mitchell-Olds & Bergelson, 2000; Speight & al., & al., 2006). They are typically low- to medium-size trees. 2008; Futuyma, 2009; Futuyma & Agrawal, 2009). Further- The genus is relatively well known taxonomically, and it has more, because Bursera is highly adapted to the ecological and been divided into two subgenera of roughly equal size, B. subg. climatic conditions of the dry forests, and of great physiog- Bursera and subg. Elaphrium Jack. (McVaugh & Rzedowski, nomic importance in these forests, its evolution and diversifica- 1965; Rzedowski & Kruse, 1979). tion has been used as an indicator of the historical expansion of Bursera is an old tropical genus, whose distribution in the the tropical dry forests of Mexico (Rzedowski, 1978; Becerra, past extended across central North America. Fossil leaves of 2005; Pennington & al., 2006). B. serrulata (Lesquereux) MacGinitie, a putative relative of the Several hypotheses have been advanced to identify the phy- modern B. tecomaca (DC.) Standl., are abundant in the early logenetic relationships within Bursera using molecular markers. Oligocene beds of Florissant, in Colorado (MacGinitie, 1953; The most comprehensive study included 66 Bursera species Rzedowski & Kruse, 1979). Fossil pollen of Bursera has also and 5 outgroups, and was reconstructed using sequences from been reported from these beds (Meyer, 2003). Another fossil the internal transcribed spacer (ITS) region, the external tran- species belonging in the subg. Elaphrium, Bursera inaequi- scribed spacer (ETS) region, the 5.8S coding region, and the 5S lateralis MacGinitie, is known from the Eocene Green River, non-transcribed (5S-NTS) region of the nuclear ribosomal DNA Colorado-Wyoming, suggesting that the genus had began diver- (Becerra & Venable, 1999b; Becerra, 2003a). This molecular sifying by at least 45 million years (Ma) ago (MacGinitie, 1969). phylogeny shed light not only on the relationships of the main Bursera has been the subject of several ecological, chemi- lineages but also on the relations between many of the individual cal, and evolutionary studies. These plants have a long history species. Analyses strongly supported the monophyly of Bursera, of interaction with the phytophagous beetle genus Blepharida as well as monophyly of its two subgenera. It also suggested that Chevrolat (Chrysomellidae) (Becerra, 1997, 2003b; Becerra Bursera is sister to Commiphora Jacq. 333 Becerra & al. • Monophyly of Bursera TAXON 61 (2) • April 2012: 333–343 Other studies using molecular markers as well as morpho- MATERIALS AND METHODS logical characteristics have also explored relationships of Bursera and its allied genera within Burseraceae (Gillett, 1980; Harley Phylogenetic analysis of Bursera and Commiphora & Daly, 1995; Clarkson & al., 2002; Weeks & al., 2005). Burs- era + Commiphora is well supported as a monophyletic group, Taxonomic sampling. — Our taxonomic sample consisted Bursereae, subtribe Burserinae. Molecular dating analyses using of 76 species and varieties of Bursera (see Appendix), including fossils of Bursera and Canarium L. (a more distantly related 42 species of subg. Bursera and 34 of subg. Elaphrium. This genus) to calibrate a phylogeny of Burseraceae indicated that the sampling represents about 72% of the genus and its entire range family began to diversify after 58 Ma ago (Weeks & al., 2005). of geographic distribution (i.e., all the main regions of distri- Recently, however, the monophyly of Bursera was chal- bution of the genus in Mexico, including Baja California, and lenged. A phylogenetic analysis of 50 Burseraceae species also Central and South America, and the Caribbean). Fifty-one including 10 species of Commiphora, and 12 Bursera spe- species of Commiphora were sampled also representing all the cies based on sequences of the ETS region, the chloroplast major regions of geographic distribution of the genus (includ- psbA-trnH spacer region, and the rps16 intron, suggested that, ing Madagascar, Africa, South America, and India). Because while Commiphora is monophyletic, Bursera is not (Weeks C. leptophloeos (Mart.) J.B. Gillett has a disjunct distribution in & al., 2005). In this phylogeny Bursera is either paraphyletic, South America, we sampled both regions with possibly distinct with Commiphora nested within Bursera and with B. subg. populations. Our outgroups were chosen so as to sample taxa Elaphrium in a basal position and subtending the sister pair of that are closely related to Commiphora and Bursera as well as subg. Bursera and Commiphora; or these three clades form a some that are more distantly related, but still with sequences polytomy. Another phylogenetic reconstruction that included that are straightforward to align. They included seven species 37 species of Commiphora and 13 Bursera species could not of three Burseraceae genera that are closely related to Burseri- support Bursera’s monophyly using the same markers as Weeks nae (Protium Bu r m . f., Crepidospermum Hook. f., Tetragastris & al. (2005) with Burseraceae (Weeks & Simpson, 2007). Ac- Gaertn.), three species of two more distantly related genera cording to Weeks & al. (2005) the discrepancies of their results (Canarium, Boswellia Roxb. ex Colebr.) as well as three spe- with previously published phylogenies supporting the mono- cies of Anacardiaceae. phyly of Bursera were due to their more comprehensive sam- DNA sequencing. — To reconstruct the phylogeny we used pling of Commiphora species compared to the earlier studies the ITS1 and ITS2 and the 5.8S coding region (ITS region), as (Becerra, 2003a) which included only five species. However, well as part of the ETS region of nuclear ribosomal DNA. We the paraphyly of Bursera was inferred using only 13 species have used these markers for Bursera and Commiphora previ- (Weeks, & al., 2005), whereas previous studies indicating ously, and they provided nearly full resolution at the deeper and monophyly included 66 species. Therefore, it seems that none medium branching levels in both genera (Becerra & Venable, of the phylogenetic studies carried out to date have used a suf- 1999b; Becerra, 2003a). ficiently comprehensive taxonomic sampling of both Bursera Many of the sequences of Bursera and some of Commi- and Commiphora to test for the monophyly of Bursera. phora used in this study were already available in GenBank Whether Bursera is or is not a monophyletic genus has im- from our previous studies and also from studies by others (Ap- portant consequences. First, conclusions about the evolutionary pendix). For species not considered in previous studies and interactions between Bursera and its herbivores could change for which sequences were thus not available (a total of 49), we depending on the phylogenetic hypotheses considered. Sec- collected
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