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A Molecular Phylogenetic Perspective

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A Molecular Phylogenetic Perspective Astragalus (Fabaceae): A molecular phylogenetic perspective MARTIN F. WOJCIECHOWSKI Wojciechowski, M. E (School of Life Sciences, Arizona State University, Tem- pe, AZ, 85287-4501, U.S.A.; e-mail: [email protected]). Astragalus (Fa- baceae): A molecular phylogenetic perspective. Brittonia 57: 382-396. 2005.-- Nucleotide sequences of the plastid mark gene and nuclear rDNA internal tran- scribed spacer region were sampled from Astragalus L. (Fabaceae), and its closest relatives within tribe Galegeae, to infer phylogenetic relationships and estimate ages of diversification. Consistent with previous studies that emphasized sampling for nrDNA ITS primarily within either New World or Old World species groups, Astragalus, with the exception of a few morphologically distinct species, is strongly supported as monophyletic based on maximum parsimony and Bayesian analyses of matK sequences as well as a combined sequence dataset. The matK data provides better resolution and stronger clade support for relationships among Astragalus and traditionally related genera than nrDNA ITS. Astragalus sensu stricto plus the genus Oxytropis are strongly supported as sister to a clade com- posed of strictly Old World (African, Australasian) genera such as Colutea, Suth- erlandia, Lessertia, Swainsona, and Carrnichaelia, plus several morphologically distinct segregates of Eurasian Astragalus. Ages of these clades and rates of nucleotide substitution estimated from a fossil-constrained, rate-smoothed, Bayes- ian analysis of matK sequences sampled from Hologalegina indicate Astragalus diverged from its sister group, Oxytropis, 12-16 Ma, with divergence of Neo- Astragalus beginning ca. 4.4 Ma. Estimates of absolute rates of nucleotide sub- stitution for Astragalus and sister groups, which range from 8.9 to 10.2 x 10 -~0 substitutions per site per year, are not unusual when compared to those estimated for other, mainly temperate groups of papilionoid legumes. The results of previ- ously published work and other recent developments on the phylogenetic rela- tionships and diversification of Astragalus are reviewed. Key words: Astragalus, diversification, Fabaceae, Neo-Astragalus. The legume genus Astragalus L., with an spp.), and the Andes of South America (ca. estimated 2500 species of herbaceous peren- 100 spp.). The geographic center of diversity nial and annual species in the subfamily Pap- and presumed origin of Astragalus, like most ilionoideae of the Fabaceae (Mabberley, of its close relatives in the tribe Galegeae 1997; Lewis et al., 2005) and the largest of (Polhill, 1981a, 1981b), is Eurasia, and spe- 19 or so genera of angiosperms with more cifically the steppes and mountains of south- than 1000 species, is an example of an adap- western to south-central Asia and the Hima- tive radiation on a global scale. Astragalus is layan plateau. Of the two Galegean genera distributed mainly in cool to warm arid and with distributions in the New World, the other semiarid regions of the northern hemisphere, being Oxytropis DC. with ca. 330 spp. in the South America, tropical East Africa, and is northern hemisphere (Bobrov et al., 1972; especially diverse in southwestern and Sino- Welsh, 2001), only Astragalus has undergone Himalayan regions of Asia (ca. 1500-2000 extensive diversifications in both North and spp.), western North America (ca. 400-450 South America. Brittonia, 57(4), 2005, pp. 382-396. ISSUED: 28 December 2005 2005, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A. 2005] WOJCIECHOWSKI:MOLECULAR PHYLOGENETIC OF ASTRAGALUS 383 Given its huge species diversity and two current species of the Asian Sphaero- widespread distribution, it is hardly surpris- physa were originally included in the Lin- ing that no comprehensive monographic in- naean genus Phaca, but Gray (1864) and vestigation of Astragalus has been attempt- Bunge (1868, 1869) among others subse- ed since the taxonomic treatments of the quently treated these as a subgenus of As- late 19 th century (Bunge, 1868, 1869; Taub- tragalus. While these taxa share a number ert, 1894). With the exception of Rydberg of important morphological characters, Bar- (1929), who recognized 28 genera within neby (1964; p. 1162) and Isely (1998) treat- North American Astragalus, in a revision ed this genus separate from Astragalus (lat- not supported by subsequent authors (Bar- er corroborated by molecular phylogenetic neby, 1964; Isely, 1998), and the segrega- analysis; Sanderson & Wojciechowski, tion of the Eurasian subgenus Tragacantha 1996). Since then, a number of other "mor- as Astracantha (Podlech, 1983, but later re- phologically isolated" Eurasian Astragalus versed by Zarre & Podlech, 1997), the cir- species have been segregated as monotypic cumscription of Astragalus remains rela- genera, largely on the basis of pod mor- tively unchanged since that proposed by phology (e.g., Barnebyella, Podlech, 1994; Bunge. During the 20 th century, taxonomic Ophiocarpus (Bunge) Ikonn.; Ikonnikov, work has been more floristic and regional 1977). Perhaps the most obvious example in scope, such as Johnston's (1938, 1947) of recent taxonomic uncertainty regarding compilations of South American species, the circumscription of Astragalus was the Gillett's (1963) treatment of the few species elevation of the entire subgenus Tragacan- that extend into tropical East Africa, Bar- tha (sensu Bunge, 1868, 1869) to generic neby's (1964) comprehensive revision of rank. This taxon, consisting of more than the more than 400 North American species, 200 species with striking spinescent habit Goncharov's (1965) treatment for the Flora and reduced inflorescences and fruits, was of the [former] USSR, and Lock and Simp- first recognized at the generic rank as Tra- son's (1991) checklist of legumes from west gacantha Mill. (Borissova, 1937) and more Asia. Recent taxonomic studies, largely recently as Astracantha by Podlech (1983), limited to Old World taxa, have emphasized which was later rejected (Zarre & Podlech, primarily revisionary work at the sectional 1997). Given these uncertainties surround- level and anatomical/morphological inves- ing the circumscription of the genus, the tigations (e.g., Podlech, 1982, 1983, 1984, question of the monophyly of Astragalus 1990, 1994; Engel, 1992; Wenninger, 1991; itself has remained open. Worse still, the Zarre & Podlech, 1997). In South America, view of Astragalus as a paraphyletic assem- species-level and floristic work has contin- blage or "wastebasket," basal within Gal- ued (G6mez-Sosa, 1979, 1981, 1997), but egeae with other genera (and other tribes) has not yet resulted in an infrageneric-level potentially nested within it (e.g., Polhill, classification comparable to that of Barne- 1981b), has prevailed well into the late 20 ~h by's (! 964) monograph. century. In addition to the lack of comprehensive In this context then, the first cladistic monographic studies, the relationship of As- studies on Astragalus began with analyses tragalus to certain morphologically similar of North American species using morpho- genera in Galegeae, especially Oxytropis, logical characters (Sanderson, 1991) and but also Sphaerophysa DC., and Swainsona molecular sequence and length polymor- Salisb., has always been problematic. In- phism data (Liston, 1992; Sanderson & deed, both Ledingham (1957, 1960), on the Doyle, 1993; Wojciechowski et al., 1993) basis of cytogenetic evidence, and Barneby in order to identify monophyletic groups (1952) on the basis of a number of mor- and begin to resolve their higher-level (in- phological similarities, suggested that Oxy- frageneric) relationships to Eurasian and tropis was derived from within Eurasian South America taxa. This was followed by Astragalus. More recently, Podlech (1982) broader-scale analyses of molecular data also implied that Oxytropis was nested from representative taxa of Galegeae and within Old World Astragalus. Similarly, the related tribes (Liston & Wheeler, 1994; 384 BR1TTONIA [VOL. 57 Sanderson & Wojciechowski, 1996) to re- scribed previously (Wojciechowski et al., solve the relationships of Astragalus to Ox- 1999, 2004). DNA sequencing was per- ytropis, and certain other genera in Gale- formed on an Applied Biosystems 3100 se- geae, within the larger "temperate herba- quencer at the Arizona State University ceous group" of papilionoids circumscribed (DNA Laboratory, Tempe, Arizona, USA). by Polhill (1981a). The most recent molec- Sequencer output files were assembled into ular phylogenetic analyses (Wojciechowski contigs and edited using the program Se- et al., 1999; Kazempour Osaloo et al., 2003, quencher 4.1 (GeneCodes, Ann Arbor, 2005), though still sparse in terms of sam- Michigan, USA) before alignment. pling (<10% of species), have focused more on a selection of Eurasian and North PHYLOGENETIC ANALYSES American species, based on morphological and cytogenetic diversity or the current sec- Phylogenetic analyses of the combined tional classification, to test the monophyly matK plus nrDNA ITS sequence data set, of infrageneric level groups as well as of consisting of 44 terminal taxa, utilized max- the genus itself. imum parsimony (MP) and Bayesian ap- In this paper, I review how our ideas of proaches. Parsimony analyses were per- Astragalus, both with respect to that of its formed using PAUP* (version 4.0b10; phylogenetic relationships, at the infrage- Swofford, 2002) on Macintosh or Linux neric level and among closely related gen- computers. Multiple tree searches were con- era, and its diversification within the
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