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Consolida and Aconitella Are an Annual Clade of Delphinium (Ranunculaceae) That Diversified in the Mediterranean Basin and the Irano-Turanian Region

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Consolida and Aconitella Are an Annual Clade of Delphinium (Ranunculaceae) That Diversified in the Mediterranean Basin and the Irano-Turanian Region TAXON 60 (4) • August 2011: 1029–1040 Jabbour & Renner • Consolida and Aconitella belong in Delphinium Consolida and Aconitella are an annual clade of Delphinium (Ranunculaceae) that diversified in the Mediterranean basin and the Irano-Turanian region Florian Jabbour & Susanne S. Renner Systematic Botany and Mycology, Department of Biology, University of Munich, Menzinger Str. 67, 80638 Munich, Germany Author for correspondence: Florian Jabbour, [email protected] Abstract The Mediterranean and Irano-Turanian biogeographic regions are biodiversity hotspots for mesophytic and xerophytic species, including many Delphinieae. This phylogenetically poorly understood tribe of Ranunculaceae consists of Consolida and Aconitella, with together ca. 52 species, and Delphinium and Aconitum, each with ca. 300 species. To infer the phylogeny of Consolida and Aconitella, we analyzed nuclear and chloroplast DNA sequences from 39 of their species and subspecies (44 taxa) plus a set of 30 exemplar species of Delphinium and Aconitum. We used a Bayesian relaxed clock model to estimate divergence times and a maximum likelihood approach to reconstruct ancestral areas. Aconitella forms a clade embedded in Consolida, and the latter is embedded in Delphinium. Consolida s.l. (including Aconitella) comprises two clades in the Irano- Turanian region and three in the Mediterranean basin. The latter clades’ inferred crown ages of 5.1, 4.4, and 2.8 Ma suggests that the repeated drying-up of the Mediterranean, concomitant with and following the Messinian salinity crisis (5.96–5.33 Ma), may have facilitated their westward expansion. While there is clear geographic structure towards the tips of the Consolida s.l. tree, a likely ancestral area could not be inferred. However, the initial diversification of Consolida s.l., which occurred ca. 17 Ma ago, falls in a period when the climate in the Anatolian region became more arid, which may have favoured the annual life cycle that characterizes all species in this clade. To achieve a classification of mutually monophyletic genera in Delphinieae may require transferring the species of Aconitella and Consolida into Delphinium. Keywords Aconitella ; Bayesian relaxed clock; Consolida ; Delphinieae; Irano-Turanian region; Mediterranean region Supplementary Material The alignment is available in the Supplementary Data section of the online version of this article (http://www.ingentaconnect.com/content/iapt/tax). INTRODUCTION and Aconitella lies in the Mediterranean/Irano-Turanian region (Davis, 1965; Davis & Sorger, 1982; Munz, 1967a, b; Carlström, Plant clades that diversified in the Mediterranean biodi- 1984; Iranshahr, 1987, Misirdali & al., 1990; Chater, 1993), versity hotspots often have biogeographic links to the Irano- a few species occur east as far as Kazakhstan, Afghanistan, Turanian region and Central Asia (Quézel, 1985; Ribera and Pakistan (an example is Consolida schlagintweitii (Huth) & Blasco-Zumeta, 1998; Mansion & al., 2008, 2009; Lo Presti Munz; Munz, 1967b; Alam & Ali, 2010). & Oberprieler, 2009; Médail & Diadema, 2009; Blondel & al., Consolida and Aconitella are characterized by an an- 2010). The Irano-Turanian phytogeographic region encom- nual life cycle, probably as an adaptation to seasonal drought passes Anatolia, parts of Jordan, Syria, the Israeli-Palestinian (Constantinidis & al., 2001). Annuals survive unfavourable region, the Sinai Peninsula, upper Mesopotamia, a large part of periods as seeds and are statistically overrepresented in the the Armenian Highlands, southern and eastern Transcaucasia, Mediterranean biome (Raunkiaer, 1918). Delphinium also in- the Caspian shore of Iran, the Iranian Plateau (without the tropi- cludes a few annual species, all in subg. Delphinium. cal deserts), the westernmost Himalayas, and the arid territory of south-eastern European Russia to the Gobi desert (Takhtajan, 1986). This is an area with highly uneven botanical collecting Table 1. Generic classification of Consolida. and many diverse and poorly understood genera. Among the genera centred in this region and extending into the Mediter- Consolida included Consolida considered as in Delphinium a separate genus ranean are Consolida (DC.) S.F. Gray and Aconitella Spach. To- gether these genera comprise ca. 52 species, occurring from sea Candolle, 1824 (sect., 11 spp.) Gray, 1821 (monospec.: C. regalis) level to 2000 m altitude, often on dry stony slopes, in steppes, Boissier, 1867 (sect., 32 spp.) Soό, 1922 semi-deserts, or even deserts (Trifonova, 1990; our Fig. 1). Huth, 1895 (subg., 45 spp.) Davis, 1965 Their closest relatives are Delphinium L. and Aconitum L., Nevskii, 1937 (subg.) Munz, 1967a, b each with an estimated 300 species; morphological similarities Blanché & al., 1987 to Delphinium even led to the inclusion of Consolida in Del- phinium (Table 1). While the centre of diversity of Consolida Chater, 1993 1029 Jabbour & Renner • Consolida and Aconitella belong in Delphinium TAXON 60 (4) • August 2011: 1029–1040 The mutual monophyly of Consolida and Aconitella and MATEriALS AND METHODS their relationship(s) with the remaining genera of Delphinieae, viz. Aconitum and Delphinium, have never been tested with Taxon sampling, DNA sequencing, cloning, alignment, adequate DNA sequence data. Studies so far have included and phylogenetic analyses. — The present study includes only C. ajacis (synonymous with C. ambigua) to represent 39 species and subspecies (44 taxa) of Consolida and Aco- Consolida (Ro & al., 1997) and one species each of Delphinium nitella, including the types of the generic names C. regalis and Aconitum (Ro & al., 1997; Wang & al., 2009). A study S.F. Gray (Delphinium consolida L.) and A. aconiti (L.) Soják that focused on the American larkspurs included 62 species (Delphinium aconiti L.). For C. ajacis, C. pubescens, and C. re- of Delphinium and two species of Aconitum (Koontz & al., galis we included two or three samples each to represent the 2004). Here we investigate the relationships and biogeography geographic ranges of these widespread species. Twenty-two of Consolida and Aconitella with a sampling of 75% of their sequences of Delphinium and eight of Aconitum were included, species plus representatives of the different subgenera of Del- with a focus on the short-lived species of Delphinium because phinium and Aconitum. Specific questions we are addressing of our interest in the evolution of an annual life cycle in Del- are: (1) Are Consolida and Aconitella mutually monophyletic phinieae. The subgeneric classification accepted for Delphin- and what is their relationship to Delphinium ? (2) When and ium is that of Malyutin (1987) who recognized two short-lived where did Consolida and Aconitella diversify? (3) What is the subgenera, subg. Staphisagria (J. Hill) Peterm. (three biennial relationship of the annual species of Delphinium to those in species, all sampled) and subg. Delphinium sect. Anthrisci- Consolida and Aconitella? folium Wang (three annual species, one sampled) and sect. Fig. 1. Consolida and Aconitella plants and their natural habitats. A, Consolida persica (Iran, prov. Esfahan, 51°13′10″ E, 33°58′11″ N, altitude = 1360 m); B, Aconitella teheranica (Iran, prov. Mazandaran, Haraz road, 80 km NE Tehran); C, Garedji (Georgia), steppe region where Aconitella grows; D, Wardsia (Georgia), collecting site of Aconitella hohenackeri. Photos A and B: Shahin S. Zarre; C and D: Andreas Gröger. 1030 TAXON 60 (4) • August 2011: 1029–1040 Jabbour & Renner • Consolida and Aconitella belong in Delphinium Delphinium (19 annual species, 10 sampled). The perennial lists all DNA sources, species names with authors, and Gen- species of Delphinium are represented by eight species from Bank accession numbers. The aligned trnL-trnF, trnK-matK, China and North America (subg. Delphinastrum (DC.) Peterm., trnS-trnG, and ITS matrices comprised 1338, 1560, 947 and subg. Oligophyllon Dimitrova). Aconitum is represented by 661 nucleotides respectively. There was no statistically sup- species from each of its three subgenera (classification of Ta- ported conflict (defined as > 80% bootstrap support) between mura, 1990: (1) the monospecific biennial subg. Gymnaconitum topologies obtained from the individual data partitions, and (Stapf) Rapaics is represented by Aconitum gymnandrum from the chloroplast and nuclear data were therefore combined, China; (2) the perennial subg. Lycoctonum (DC.) Peterm. (ca. yielding a matrix of 4506 characters and 76 taxa. All tree 50 species) by Aconitum septentrionale; and (3) the biennial searches relied on maximum likelihood (ML) as implemented subg. Aconitum (ca. 250 species) by six Asian species. Based in RAXML (Stamatakis, 2006; Stamatakis & al., 2008), using on the Ranunculaceae trees of Wang & al. (2009) we selected the GTR + G model (with four rate categories), with separate species of Actaea L. and Nigella L. to root our trees; the ap- partitions for the nuclear and chloroplast data. Statistical sup- propriateness of this choice was tested using Path-O-Gen v.1.3 port for nodes was assessed by bootstrap resampling of the data (Drummond & al., 2003), which can help infer the root of a under the same model (100 replicates). FindModel (http://hcv. tree as long as the molecular clock assumption fits the data lanl.gov/content/sequence/findmodel/findmodel.html; using reasonably well (below). the ModelTest script; Posada & Crandall, 1998) selected this DNA isolation and sequencing relied on commercial kits model or the slightly less parameter rich HKY85 model
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