Molecular phylogeny of Subtribe Artemisiinae (Asteraceae), including Artemisia and its allied and segregate genera

BMC Evolutionary Biology 2BR2M0e0Cs2eE,vaorlucthionaarrytBiciolelogy x Molecular phylogeny of Subtribe Artemisiinae (Asteraceae), including Artemisia and its allied and segregate genera Linda E Watson 2 Paul L Bates 1 Timothy M Evans 0 Matthew M Unwin 2 James R Estes 3 0 Biology Department, Hope College , Holland, MI 49422 USA 1 School of Biological Sciences, University of Nebraska-Lincoln , NE 68588 USA 2 Department of Botany, Miami University , Oxford, OH 45056 USA 3 University of Nebraska State Museum , Lincoln, NE 68588 USA Background: Subtribe Artemisiinae of Tribe Anthemideae (Asteraceae) is composed of 18 largely Asian genera that include the sagebrushes and mugworts. The subtribe includes the large cosmopolitan, wind-pollinated genus Artemisia, as well as several smaller genera and Seriphidium, that altogether comprise the Artemisia-group. Circumscription and taxonomic boundaries of Artemisia and the placements of these small segregate genera is currently unresolved. Results: We constructed a molecular phylogeny for the subtribe using the internal transcribed spacers (ITS) of nuclear ribosomal DNA analyzed with parsimony, likelihood, and Bayesian criteria. The resulting tree is comprised of three major clades that correspond to the radiate genera (e.g., Arctanthemum and Dendranthema), and two clades of Artemisia species. All three clades have allied and segregate genera embedded within each. Conclusions: The data support a broad concept of Artemisia s.l. that includes Neopallasia, Crossostephium, Filifolium, Seriphidium, and Sphaeromeria. However, the phylogeny excludes Elachanthemum, Kaschgaria, and Stilnolepis from the Artemisia-group. Additionally, the monophyly of the four subgenera of Artemisia is also not supported, with the exception of subg. Dracunculus. Homogamous, discoid capitula appear to have arisen in parallel four to seven times, with the loss of ray florets. Thus capitular morphology is not a reliable taxonomic character, which traditionally has been one of the defining characters. - Background Artemisia L. (Asteraceae), as broadly conceived by Linnaeus, is the largest genus in Tribe Anthemideae [13] and one of the largest in the family [4]. It is widespread in midto high-latitudes, and shrubby species dominate most cold and many warm deserts in the Northern Hemisphere [513]. Because of the abundance of wind-dispersed Artemisia pollen in the geological column, it is used as an indicator of steppe climates [14]. Some members are foraged by ungulates, rodents, birds, and insects [11,15 19], despite the production of sesquiterpenes that afford a bitter taste to the herbage. The woody species increase dramatically under grazing pressure, thereby excluding desirable forage [11,20,21]. Many Artemisia species are a major cause of allergies in humans [22]. All Artemisia species produce aromatic oils, and several are culinary herbs or used as flavorings, hallucinogens, vermifuges, and pharmaceuticals [2326], and some are toxic [27]. Artemisia annua (annual wormwood) and A. mexicana produce antimalarial drugs [2830], and artemisinin (from A. annua) appears to selectively kill human breast cancer cells [31]. Despite the well-known importance of Artemisia, there is no consensus on taxonomic relationships, which have traditionally been inferred on the basis of floral and capitular morphology. In Artemisia s.l., the typical limb of the Anthemideae-type ray florets are reduced to a membranous vestige, giving the impression that the small capitula are composed only of disk florets, referred to as disciform capitula (inflorescence) by Bremer and Humphries [2]. In other members of the genus, the ray flowers are absent, thus the capitulum is composed only of disk florets, i.e., discoid. In addition, plants with discoid capitula are considered homogamous since all florets are of one sexual form (perfect-bisexual disk florets), and plants with disciform capitula are considered heterogamous with two or more sexual forms (i.e., pistillate rays and perfect disks, or pistillate rays and staminate disks). Taxonomic treatments for Artemisia over the past 50 years range from maintaining a single, large genus of over 500 species [3237] to the recognition of six to eight genera from within its taxonomic boundaries [2,38,39]. Artemisia of antiquity was divided into three genera (Artemisia, Absinthium, and Abrotanum) by Tournefort [40]. However, the concept of a more inclusive genus was resurrected by Linnaeus [41], hereinafter, referred to as Artemisia s.l. Besser [42] and de Candolle [43] recognized four sections within Artemisia s.l. primarily based on the presence or absence of ray florets and the fertility/sterility of disk florets: (1) Abrotanum Besser (Artemisia of later authors) ray florets pistillate and fertile; disk florets perfect and fertile; receptacle glabrous; (2) Absinthium (Mill.) DC ray florets pistillate and fertile; disk florets perfect and fertile; receptacle hairy; (3) Seriphidium (Besser) Besser ray florets absent; disk florets perfect and fertile; receptacle glabrous; and (4) Dracunculus Besser ray florets pistillate and fertile; disk florets functionally staminate; receptacle glabrous. The first phylogenetic treatment [44] recognized four sections within a broadly defined Artemisia s.l. with sect. Artemisia proposed as the progenitor to sect. Absinthium, Dracunculus, and Seriphidium. This phylogeny was based on two hypothesized evolutionary trends: loss of fertility in the disk florets and loss of ray florets. Sect. Artemisia and Absinthium were later united [45] and all sections were raised to the level of subgenus [46,47], i.e., subg. Artemisia, Dracunculus, and Seriphidium. In addition, a number of authors [20,21,34,35,47,48] considered the American woody sagebrushes to have an independent origin from the woody Asian species (subg. Seriphidium), and recognized sect. Tridentatae. Poljakov [38] and others [2] segregated subg. Seriphidium as a distinct genus along with several small genera from within the boundaries of Artemisia s.l. The more recent, major classifications [2,39,49,50] have agreed with the segregation of Seriphidium on the basis of discoid-homogamous capitula and recognized the smaller segregate genera as well. Ling [39,51,52], for instance, considered Artemisia s.s. and Seriphidium to be distinct and sister to each other, and with the small segregate and allied genera in turn sister to them [53]. In their landmark monograph of Tribe Anthemideae, Bremer and Humphries [2] placed Artemisia and its allied genera in Subtribe Artemisiinae. In contrast to Ling's hypothesis [53] regarding sister group relationships between Artemisia s.s. and Seriphidium, the Bremer and Humphries [2] morphologically based cladogram placed four small genera (Neopallasia, Turaniphytum, Mausolea, Picrothamnus; with a total of seven species) as closest sisters (i.e., segregates) of Artemisia s.s. (the Artemisia-clade sensu Bremer and Humphries), (...truncated)