Abstract
Background and aims
The genus Allium comprises more than 800 species, placing it among the largest monocotyledonous genera. It is a variable group that is spread widely across the Holarctic region. Previous studies of Allium have been useful in identifying and assessing its evolutionary lineages. However, there are still many gaps in our knowledge of infrageneric taxonomy and evolution of Allium. Further understanding of its phylogeny and biogeography will be achieved only through continued phylogenetic studies, especially of those species endemic to China that have often been excluded from previous analyses. Earlier molecular studies have shown that Chinese Allium is not monophyletic, so the goal of the present study was to infer the phylogeny and biogeography of Allium and to provide a classification of Chinese Allium by placement of Chinese species in the context of the entire phylogeny.Methods
Phylogenetic studies were based on sequence data of the nuclear ribosomal internal transcribed spacer (ITS) and chloroplast rps16 intron, analysed using parsimony and Bayesian approaches. Biogeographical patterns were conducted using statistical dispersal-vicariance analysis (S-DIVA).Key results
Phylogenetic analyses indicate that Allium is monophyletic and consists of three major clades. Optimal reconstructions have favoured the ancestors of Amerallium, Anguinum, Vvedenskya, Porphyroprason and Melanocrommyum as originating in eastern Asia.Conclusions
Phylogenetic analyses reveal that Allium is monophyletic but that some subgenera are not. The large genetic distances imply that Allium is of ancient origin. Molecular data suggest that its evolution proceeded along three separate evolutionary lines. S-DIVA indicates that the ancestor of Amerallium, Anguinum, Vvedenskya, Porphyroprason and Melanocrommyum originated from eastern Asia and underwent different biogeographical pathways. A taxonomic synopsis of Chinese Allium at sectional level is given, which divides Chinese Allium into 13 subgenera and 34 sections.Free full text
Phylogeny and biogeography of Allium (Amaryllidaceae: Allieae) based on nuclear ribosomal internal transcribed spacer and chloroplast rps16 sequences, focusing on the inclusion of species endemic to China
Abstract
Background and Aims
The genus Allium comprises more than 800 species, placing it among the largest monocotyledonous genera. It is a variable group that is spread widely across the Holarctic region. Previous studies of Allium have been useful in identifying and assessing its evolutionary lineages. However, there are still many gaps in our knowledge of infrageneric taxonomy and evolution of Allium. Further understanding of its phylogeny and biogeography will be achieved only through continued phylogenetic studies, especially of those species endemic to China that have often been excluded from previous analyses. Earlier molecular studies have shown that Chinese Allium is not monophyletic, so the goal of the present study was to infer the phylogeny and biogeography of Allium and to provide a classification of Chinese Allium by placement of Chinese species in the context of the entire phylogeny.
Methods
Phylogenetic studies were based on sequence data of the nuclear ribosomal internal transcribed spacer (ITS) and chloroplast rps16 intron, analysed using parsimony and Bayesian approaches. Biogeographical patterns were conducted using statistical dispersal–vicariance analysis (S-DIVA).
Key Results
Phylogenetic analyses indicate that Allium is monophyletic and consists of three major clades. Optimal reconstructions have favoured the ancestors of Amerallium, Anguinum, Vvedenskya, Porphyroprason and Melanocrommyum as originating in eastern Asia.
Conclusions
Phylogenetic analyses reveal that Allium is monophyletic but that some subgenera are not. The large genetic distances imply that Allium is of ancient origin. Molecular data suggest that its evolution proceeded along three separate evolutionary lines. S-DIVA indicates that the ancestor of Amerallium, Anguinum, Vvedenskya, Porphyroprason and Melanocrommyum originated from eastern Asia and underwent different biogeographical pathways. A taxonomic synopsis of Chinese Allium at sectional level is given, which divides Chinese Allium into 13 subgenera and 34 sections.
INTRODUCTION
The genus Allium L. comprises more than 800 species (Fritsch et al., 2010), making it one of the largest monocotyledonous genera; it is a variable group that is spread widely across the Holarctic region from the dry subtropics to the boreal zone. Allium dregeanum is the only exception; it is native to South Africa (De Wilde-Duyfjes, 1976). This genus has a major centre of diversity stretching from the Mediterranean Basin to Central Asia and Pakistan and a second less pronounced one located in western North America. It consists of perennial herbs mostly characterized by tunicated bulbs, narrow basal leaves, umbellate or head-like inflorescences, flowers with six free or almost free tepals, superior ovaries with one to several ovules per locule, septa often containing nectaries opening by pores at the base of the ovary, entire or three-cleft stigma, loculicidal capsule, rhomboidal or spheroidal black seeds, and an onion-like odour and taste due to the presence of cystine sulphoxides. The genus is diverse in cytology. The most common basic chromosome number is x = 8, but other numbers (x = 7, 9, 10, 11) and variation in ploidy also occurs (Traub, 1968; Friesen, 1992; Huang et al., 1995; Xu et al., 1998; Zhou et al., 2007). Allium contains many economically important species, including garlic, leek, onion, shallot, bunching onion, chives and Chinese chives cultivated as vegetables or spices, and species used as herbal crops, as traditional medicines and as ornamental plants (Fritsch and Friesen, 2002). Allium is a member of the family Amaryllidaceae J.St.-Hil., subfamily Allioideae Herb., tribe Allieae Dumort. (Fay and Chase, 1996; APG III, 2009; Chase et al., 2009). After Fay and Chase (1996), Friesen et al. (2000) and Chase et al. (2009), Allium (including Caloscordum Herb., Milula Prain and Nectaroscordum Lindl.) is the only genus in tribe Allieae.
The history of infrageneric classification in Allium dates back to Linnaeus (1753) who accepted 30 species in three alliances. Later authors recognized an increasing number of infrageneric groups: six sections and 285 species (Regel, 1875, 1887); nine sections and 228 species for the former USSR (Vvedensky, 1935) alone; three subgenera, 36 sections and subsections, and about 600 species (Traub, 1968); six subgenera, and 44 sections and subsections (Kamelin, 1973); three subgenera and 12 sections (Stearn, 1980); five subgenera and 16 sections (Hanelt, 1990). A recent classification was proposed by Hanelt et al. (1992), including six subgenera, 50 sections and subsections for 600–700 species based on a multidisciplinary approach including morphological, anatomical, karyological, serological and numerical investigations as well as studies of life cycles, distribution, ecology and isozyme data. Friesen et al. (2006) presented a new classification of the genus consisting of 15 subgenera and 72 sections for about 780 species based on their phylogenetic study. Many morphological and anatomical studies on Allium have also been performed, and numerous data have been published dealing with newly described taxa and regional revisions (e.g. Brullo et al., 1991; Cheremushkina, 1992; Kamenetsky, 1992; Hanelt and Fritsch, 1994; Friesen, 1995; Mathew, 1996; Khassanov, 1997; Xu and Kamelin, 2000; Dale et al., 2002; Fritsch, 2009; Fritsch and Friesen, 2009; Kovtonyuk et al., 2009). All of the above-mentioned works have been helpful in establishing and assessing the evolutionary lineages in the genus. However, due to their close morphological similarities, over-reliance on dried specimens, remarkable degrees of polymorphism and disagreements regarding the taxonomic importance of specific morphological traits (Hanelt et al., 1992; Khassanov and Fritsch, 1994; Khassanov, 1997; Mes et al., 1997; Gregory et al., 1998), there are still many gaps in our knowledge of infrageneric taxonomy and differentiation and evolution in the genus.
Recently, molecular approaches using plastid DNA and nuclear ribosomal DNA (nrDNA) sequences have been applied to understand the evolutionary processes and taxonomic relations within the genus. A first approach to structuring the genus Allium by molecular markers was published by Linne von Berg et al. (1996). The resulting phenogram largely confirmed the subgeneric classification based on an integration of morphological and other methods, but found that subgenera Amerallium Traub and Bromatorrhiza Ekberg could not be clearly distinguished. Later molecular studies focused on the classification and phylogeny of the entire genus Allium (Mes et al., 1997; Dubouzet and Shinoda, 1999; He et al., 2000; Fritsch and Friesen, 2002; Friesen et al., 2006) or specific subgenera such as Amerallium (Samoylov et al., 1995, 1999), Melanocrommyum (Webb & Berth.) Rouy (Dubouzet and Shinoda, 1998; Mes et al., 1999; Gurushidze et al., 2008, 2010; Fritsch et al., 2010) and Rhizirideum (G.Don ex Koch) Wendelbo (Dubouzet et al., 1997). Other researchers focused on the origins of major Allium crops (e.g. Friesen and Klaas, 1998; Friesen et al., 1999; Blattner and Friesen, 2006), phylogenetic relationships between Allium and the monotypic Himalayan genus Milula Prain (Friesen et al., 2000), the phylogeny of section Cepa (Mill.) Prokh (Gurushidze et al., 2007), the phylogenetic position of western North American species and their adaptation to serpentine soils (Nguyen et al., 2008), and the origins of A. ampeloprasum horticultural groups and a molecular phylogenetic analysis of the section Allium (Hirschegger et al., 2010). However, relatively few species endemic to China were included in these investigations.
One hundred and thirty-eight species of Allium (50 endemic, five introduced) occur in China (Xu and Kamelin, 2000), accounting for about one-sixth of recognized species. These represent five subgenera, namely Allium, Rhizirideum, Melanocrommyum, Bromatorrhiza and Caloscordum (Herb.) R.M.Fritsch (not the subgenus Amerallium) according to the treatment of the Gatersleben group (Hanelt et al., 1992), and four basic chromosome numbers, x = 7, 8, 10, 11 (not x = 9). These characteristics indicate that Chinese Allium is of particular interest for students of speciation, classification and phylogeny. Further understanding of Allium phylogeny and biogeography will be achieved only through continued phylogenetic studies, especially of those species endemic to China that have often been excluded from previous analyses.
The internal transcribed spacer (ITS) region of nrDNA is a valuable source of phylogenetic information at the generic and subgeneric level (Baldwin, 1992; Baldwin et al., 1995; Blattner, 2004; Hörandl et al., 2005) and has also proved to be informative in Allium (Dubouzet and Shinoda, 1999; Friesen et al., 2000, 2006; Gurushidze et al., 2007, 2008; Nguyen et al., 2008). The intron of the rpsl6 gene was first used for phylogenetic studies by Oxelman et al. (1997), and it has been shown to provide good resolution at the generic levels (e.g. Ingram and Doyle 2003; Marazzi et al., 2006).
In this study, we present the results of a molecular systematic study of Allium based on ITS and rps16 intron sequences. Previous molecular studies have shown that the Chinese Allium is not monophyletic, so the goals of the present study were to (1) clarify the phylogenetic relationships between subgenera within the genus, (2) infer the biogeography of Allium and (3) provide an intrageneric classification of Chinese Allium based on the placement of these Chinese species in the context of the entire genus.
MATERIALS AND METHODS
Taxon sampling
In total, 341 taxa (60 ITS sequences were generated in this study) were included in the present study for the single-marker (ITS) Allium phylogenetic analysis. The ingroup comprised 331 taxa covering all subgenera and almost all sections of the genus (see Friesen et al., 2006). Ipheion uniflorum, two Tulbaghia species, two Nothoscordum species and five Dichelostemma species were designated as outgroups according to previous phylogenetic analyses (Fay and Chase, 1996; Mes et al., 1997; Fay et al., 2000; Friesen et al., 2000, 2006; Nguyen et al., 2008). Fifty-five rps16 sequences generated in this study were combined with five rps16 sequences obtained from the GenBank database with a focus on Chinese Allium, with 58 ingroup taxa and two outgroup species, namely Nothoscordum gracile and Tulbaghia violacea.
All accessions in the collection stem from populations collected during field trips or from botanical gardens (Chengdu Botanical Garden and Kunming Botanical Garden for cultivated species and outgroups). Voucher specimens were deposited in the herbarium of the Sichuan University (SZ). Voucher information and GenBank accession numbers (GQ181063–GQ181108 and GU566611–GU566624 for ITS; GU566625–GU566679 for rps16) are listed in Appendix 1. ITS and rps16 accessions obtained from GenBank are presented in Appendix 2.
DNA extraction, amplification and sequencing
Genomic DNA was extracted from silica gel-dried or fresh leaves using the method of Doyle and Doyle (1987). Primers ITS4 and ITS5 (White et al., 1990) were used to amplify the ITS region. The PCR programme was as follows: 94 °C for 5 min; 30 cycles of 94 °C for 45 s, 55 °C for 45 s and 72 °C for 1 min; and 72 °C for 7 min. The rps16 intron was amplified with primers rpsF and rpsR2 (Oxelman et al., 1997) in accordance with the protocol of Marazzi et al. (2006). PCR products were separated using 1·5 % (w/v) agarose TAE gel and purified using Wizard PCR preps DNA Purification System (Promega, Madison, WI, USA) following the manufacturer's instructions. The purified PCR products were sequenced in an ABI 310 Genetic Analyzer (Applied Biosystems Inc.) in both directions using the PCR primers.
Sequence comparisons and phylogenetic analyses
DNA sequences were initially aligned using the default pairwise and multiple alignment parameters in Clustal X (Jeanmougin et al., 1998) and then rechecked and adjusted manually as necessary using MEGA4 (Tamura et al., 2007). Gaps were positioned to minimize nucleotide mismatches and treated as missing data in phylogenetic analyses.
Exploratory phylogenetic analyses were conducted separately with each dataset (ITS matrix with a global sampling of Allium species, a subset of ITS matrix including only 60 taxa focusing on Chinese Allium, rps16 matrix including the same 60 taxa, and the combined data matrix for the 60 taxa common to both ITS and rps16). Results from the ITS (a subset of ITS matrix) and rps16 analyses (Supplementary Data Figs 1 and and2,2, available online) did not show any major topological conflict and provided higher resolution when analysed together than separately. Consequently, molecular datasets were combined (ITS + rps16) in a single analysis for Chinese Allium. Finally, phylogenetic analyses for the individual data matrix (ITS matrix with a global sampling of Allium species) and combined datasets (ITS and rps16) were conducted by employing maximum-parsimony (MP) criteria and Bayesian inference (BI), using the programs PAUP* version 4·0b10 (Swofford, 2003) and MrBayes version 3·1.2 (Ronquist and Huelsenbeck, 2003), respectively. For MP, heuristic searches were carried with 1000 random addition sequence replicates. One tree was saved at each step during stepwise addition, tree-bisection-reconnection (TBR) was used to swap branches, and the maximum number of trees was set to 10 000. All characters were unordered and equally weighted. Gaps were treated as missing data. Bootstrap values were calculated from 1000 000 replicate analyses using ‘fast’ stepwise-addition of taxa and only those values compatible with the majority-rule consensus tree were recorded. Prior to a Bayesian analysis, MrModeltest version 2·2 (Nylander, 2004) was used to select a best-fit model of nucleotide substitution, and the GTR + I + G model under the Akaike infomation criterion was selected. The Bayesian Markov chain Monte Carlo (MCMC) algorithm was run for 2000 000 generations with one cold chain and three heated chains, starting from random trees and sampling trees every 100 generations. The first 5000 trees were considered as the burn-in and were discarded. A 50 % majority-rule consensus tree of the remaining trees was produced.
Phylogenetic tree resulting from a Bayesian analysis of the ITS sequences from species of Allium and ten outgroup species. The subgeneric and sectional classification according to Hanelt et al. (1992), Dubouzet and Shinoda (1999), Friesen et al. (2006), Gurushidze et al. (2008), Nguyen et al. (2008), Kovtonyuk et al. (2009), Fritsch et al. (2010) and our own results is indicated on the right. Values along branches represent Bayesian posterior probabilities (PP) and parsimony bootstrap (BS), respectively. Scientific names given in bold are those endemic to China, in bold italics those distributed in China and other areas, and in italics species distributed in other areas of the world.
Phylogenetic tree resulting from a Bayesian analysis of combined sequence data (ITS and rps16) focusing on Chinese Allium. The subgeneric and sectional classification according to Hanelt et al. (1992), Dubouzet and Shinoda (1999), Friesen et al. (2006), Nguyen et al. (2008), Kovtonyuk et al. (2009) and our own results is indicated on the right. Values along branches represent Bayesian posterior probabilities (PP) and parsimony bootstrap (BS), respectively. Scientific names given in bold are those endemic to China, in bold italics those distributed in China and other areas, and in italics species distributed in other areas of the world.
The incongruence length difference (ILD) test of ITS and rps16 intron datasets for the same 60 taxa was carried out in PAUP* (Farris et al., 1994) to assess potential conflicts between different DNA fragments. This test was implemented with 100 partition-homogeneity test replicates, using a heuristic search option with simple addition of taxa, TBR branch swapping and MaxTrees set to 1000.
Biogeographical analysis
Dispersal–vicariance analysis (DIVA) (Ronquist, 1996, 1997, 2001) is one of the most widely used methods for inferring biogeographical histories. Although model-based methods for inferring biogeography are available (e.g. Ree et al., 2005; Ree and Smith, 2008; Sanmartín et al., 2008), DIVA remains popular because it provides rapid results, requires little prior information, and gives results comparable with the model-based likelihood method Lagrange of Ree et al. (2005) and Ree and Smith (2008) (e.g. Ree et al., 2005; Burbrink and Lawson, 2007; Velazco and Patterson, 2008; Xiang and Thomas, 2008). Statistical DIVA (S-DIVA) (Yu et al., 2010) is a program which complements DIVA, implements the methods of Nylander et al. (2008) and Harris and Xiang (2009), and determines statistical support for ancestral range reconstructions using a novel method. Both the previous studies (Fritsch, 2001; Fritsch and Friesen, 2002; Friesen et al., 2006) and our molecular analyses indicate that evolution in Allium proceeded along three separate evolutionary lines, so we attempted to carry out a geographical analysis for each separate evolutionary line. Three separate taxonomic subsets with a focus on each evolutionary line with the ITS data realigned where necessary were obtained and then phylogenetic analyses for each evolutionary line were conducted by employing BI with the methods described above. Because of the lack of resolution within the third evolutionary line, however, we could not analyse its biogeography using S-DIVA. So finally, potential biogeographical scenarios of several specific subgenera [including Amerallium, Anguinum, Vvedenskya (Kamelin) R.M.Fritsch, Porphyroprason (Ekberg) R.M.Fritsch and Melanocrommyum] in the first and second evolutionary line were tested using statistical dispersal–vicariance analysis implemented in S-DIVA. Distribution areas of these subgenera and their close allies were defined according to the World Checklist of Selected Plant Families maintained by the Royal Botanic Gardens, Kew, UK (http://apps.kew.org/wcsp/home.do) and taxonomic and geographical studies of these Allium species (e.g. Xu and Kamelin, 2000; Dale et al., 2002). S-DIVA requires a fully resolved tree, and therefore polytomies were arbitrarily resolved. Allowing reconstruction, two optimizations were performed: first, with an unconstrained number of unit areas for each ancestral node; and second, with the number of ancestral areas restricted to two. The rationale for such a constraint is that vicariance is a proximate consequence of dispersal. Moreover, extant taxa used in the analyses rarely occur in more than two individual areas. Extinction events in DIVA are usually inferred ad hoc after the analysis in order to explain widespread ancestral distributions among areas that are not geographically adjacent (Sanmartín, 2003) and long-distance dispersals are inferred after the analysis by considering area relationships (Calviño et al., 2008) as in S-DIVA. For those subgenera not subject to a statistical dispersal-vicariance analysis (because resolution of relationships was poor), we speculate on the possible distribution of ancestors.
RESULTS
Molecular datasets
Two different datasets were generated: dataset 1 (only ITS) with a worldwide sampling of Allium species, and dataset 2 (ITS and rps16) focusing on Chinese Allium. Among the Allium sequences analysed, the ITS region varied in length from 589 bp (A. shevockii) to 665 bp (A. oreoprasoides), and the rps16 sequences ranged from 556 bp (A. caeruleum) to 901 bp (A. eduardii). The outgroup species had relatively long sequences, with ITS sequences ranging from 643 bp (Dichelostemma volubile) to 672 bp (Nothoscordum bivalve) and rps16 sequences ranging from 836 bp (N. gracile) to 876 bp (T. violacea). After introducing the necessary gaps, the ITS alignment (dataset 1) was 774 bp in length and resulted in 102 constant characters and 672 variable characters, 606 of which were potentially parsimony-informative. The mean G + C content of the ITS region was 46·67 %. Dataset 2 is a taxonomic subset of dataset 1 with a focus on Chinese Allium with the ITS data realigned where necessary and the addition of rps16 data. The subset of ITS sequences produced a matrix 706 bp in length, and for which 179 characters were constant, 92 autapomorphic and 435 potentially parsimony-informative. The mean G + C content of the rps16 region was 46·99 %. The aligned rps16 sequences produced a matrix 1148 bp in length, and for which 703 characters were constant, 208 autapomorphic and 237 potentially parsimony-informative. The mean G + C content of the rps16 region was 30·47 %. The combined aligned dataset was 1854 bp in length, with 882 characters constant, 300 autapomorphic and 672 potentially parsimony-informative; the mean G + C content was 37·69 %.
Phylogenetic analyses
For dataset 1, trees inferred from BI and MP showed no significant difference in their topologies, and therefore only the Bayesian tree with posterior probabilities (PP) and bootstrap support values (BS) is shown in Fig. 1. In all analyses, the genus Allium proved to be monophyletic and robustly separated from the outgroup species (PP = 1·00, BS = 100 %). Three major clades were found within Allium: the first major clade (PP = 1·00, BS = 82 %) comprising subgenera Nectaroscordum (Lindl.) Asch. & Graebn. (x = 9), Amerallium (x = 7, 8, 9, 10, 11) and Microscordum (Maxim.) N.Friesen (x = 8); the second major clade (PP = 1·00, BS = 67 %) comprising subgenera Caloscordum, Anguinum, Vvedenskya, Porphyroprason and Melanocrommyum (all x = 8); and the third major clade (PP = 1·00, BS = 83 %) comprising subgenera Butomissa (Salisb.) N.Friesen, Cyathophora (R.M.Fritsch) R.M.Fritsch, Rhizirideum (G.Don ex Koch) Wendelbo sensu stricto (s.s.), Allium, Cepa (Mill.) Radić, Reticulatobulbosa (Kamelin) N.Friesen and Polyprason Radić (all x = 8). For dataset 2, the ILD test conducted on the combined data matrix of common ITS and rps16 accessions was significant (ILD probability value = 0·01), indicating that the two data sets are heterogeneous. The ITS and rps16 trees placed some species (mainly those in the third evolutionary line) in contradictory positions, which may reflect reticulate events in the evolutionary history of these species, the potential mechanism of which is beyond the scope of the present paper. However, the combined tree was better resolved than any of the separate ITS and rps16 trees, and trees derived from the combined dataset were mostly consistent with respect to their major groupings; we therefore describe the combined tree here. These results corroborated the irrelevance of the significant ILD values in terms of combinability, as proposed or confirmed by previous authors (Reeves et al., 2001; Barker and Lutzoni, 2002; Inda et al., 2008; Mitsui et al., 2008). The topology of the Bayesian tree was similar to that of the MP consensus tree. The 50 % majority-rule consensus tree from BI is presented in Fig. 2, with PP and BS support values. The monophyly of Allium was also recovered by the combined analysis (PP = 1·00, BS = 100 %). Three major clades were detected in this tree: the first major clade (PP = 1·00, BS = 100 %) containing taxa from subgenera Amerallium, the second major clade (PP = 1·00, BS = 78 %) with species from subgenera Caloscordum and Anguinum, and the third major clade (PP = 1·00, BS = 93 %) with species from subgenera Butomissa, Cyathophora, Rhizirideum, Allium, Cepa, Reticulatobulbosa and Polyprason.
The major clades resulting from the combined analysis were similar to those based on ITS, and are therefore not discussed separately. In the first major clade, the Nectaroscordum clade including two species was well supported (Fig. 1A, PP = 1·00, BS = 100 %) and the Microscordum clade was represented by A. monanthum. The Amerallium clade is the largest in the first major clade. Within this clade, the New World Amerallium clade is sister to the Old World Amerallium clade (Fig. 1A, PP = 1·00, BS = 75 %). The New World Amerallium clade (Fig. 1A, PP = 1·00, BS = 82 %) contains two groups. One group includes several subclades corresponding to sections Amerallium Traub + Caulorhizideum Traub + Rhopetoprason Traub with species native to the mid-west and south-west USA (with a few exceptions, e.g. A. validum). The other group includes the monophyletic section Lophioprason Traub (Fig. 1A, PP = 1·00, BS = 51 %) with species restricted to western North America (the only exceptions are A. cernuum and A. stellatum). Within the Old World Amerallium clade (Fig. 1A, PP = 1·00, BS = 53 %), two sister subclades are evident, one with species from the Mediterranean region and the other with species from the Himalayas and south-west China. In the Mediterranean subclades, section Narkissoprason Kam. is sister to a clade containing sections Briseis (Salisb.) Stearn, Arctoprasum Kirschl. and Molium G.Don ex Koch (Fig. 1A, PP = 1·00, BS = 84 %). In the Himalayas and south-west China clade, A. wallichii var. wallichii, A. wallichii var. platyphyllum and A. macranthum are sister to a clade containing other species of section Bromatorrhiza Ekberg (Fig. 1A, PP = 0·77, BS < 50 %). In the combined (ITS and rps16) analyses, A. wallichii var. wallichii and A. wallichii var. platyphyllum are sister to a clade comprising A. macranthum, A. omeiense, A. fasciculatum, A. hookeri var. hookeri and A. hookeri var. muliense (Fig. 2, PP = 1·00, BS = 100 %).
In the second major clade, the Caloscordum clade was represented by A. neriniflorum and A. tubiflorum in the ITS analysis and by A. tubiflorum in the combined analysis. The Anguinum clade contains two sister groups (Fig. 1B, PP = 1·00, BS = 99 %). In one sister group, species from Eurasia (A. listera, A. microdictyon and A. victorialis) form a trichotomy (Fig. 1B, PP = 1·00, BS = 99 %) and this trichotomy is sister to the north-eastern North American species A. tricoccum (Fig. 1B, PP = 1·00, BS = 84 %). In the other sister group, species from eastern Asia (A. ovalifolium var. ovalifolium, A. ovalifolium var. cordifolium, A. ovalifolium var. leuconeurum, A. nanodes and A. prattii) form a polytomy (Fig. 1B, PP = 1·00, BS = 100 %; Fig. 2, PP = 1·00, BS = 100 %). The Vvedenskya and Porphyroprason clades were represented by A. kujukense and A. oreophilum, respectively. In the Melanocrommyum clade, Allium fetisowii from section Longibidentata (R.M.Fritsch) R.M.Fritsch is at the base of the clade and is sister to the remaining species of Melanocrommyum. Then, A. decipiens, A. robustum, A. tulipifolium and A. chelotum from section Decipientia (Omelczuk) R.M.Fritsch, A. viridulum from section Decipientia and A. zergericum from section Acmopetala R.M.Fritsch form three successive lineages sister to the remaining clade (Fig. 1B, PP = 1·00, BS = 79 %).
Splits within the third major clade are complex. In the Butomissa clade, section Butomissa is sister to section Austromontana (Fig. 1C, PP = 1·00, BS = 99 %; Fig. 2, PP = 1·00, BS = 100 %). Noteworthy here is that A. heldreichii from subgenus Allium section Allium is sister to A. tuberosum (Fig. 1C, PP = 1·00, BS = 61 %). As only one sequence of A. heldreichii from GenBank was included in the present study, additional sequences from multiple exemplars would be necessary to test this relationship. In the Cyathophorum clade, section Coleoblastus is sister to a clade comprising section Cyathophora and the monotypic section Milula (Fig. 1C, PP = 0·96, BS = 72 %). However, unexpected relationships were recovered for A. cyathophorum and A. weschniakowii from subgenus Cepa section Annuloprason T.V.Egorova (Fig. 1C, PP = 1·00, BS = 97 %). A larger sample of species and more molecular markers would have to be analysed to exclude technical causes for the incongruence between molecular data and the morphology-based taxonomy and to test the relationships further. In the Rhizirideum clade, section Eduardia is sister to a group comprising Rhizirideum, Caespitosoprason and Tenuissima (Fig. 2, PP = 0·88, BS < 50 %). Section Caespitosoprason is sister to the clade consisting of sections Tenuissima and Rhizirideum (Fig. 1C, PP = 0·88, BS < 50 %; Fig. 2, PP = 0·59, BS < 50 %). Species from section Rhizirideum form polytomies (Fig. 1C, PP = 1·00, BS = 100 %) and their relationship is beyond the resolution of the ITS. Allium subtilissimum from subgenus Polyprason section Oreiprason F.Herm. is sister to A. mongolicum in our study (Fig. 1C, PP = 1·00, BS = 100 %; Fig. 2, PP = 1·00, BS = 100 %), and additional sequences from multiple exemplars of this species would have to be analysed to exclude technical causes. Species from subgenera Allium, Cepa, Reticulatobulbosa and Polyprason form a large clade (Fig. 1C, PP = 1·00, BS < 50 %; Fig. 2, PP = 0·97, BS < 50 %). Within this large clade, A. macrostemon, A. eremoprasum, A. haneltii, A. schoenoprasoides, A. kurssanovii, four species from section Caerulea (Omelcz.) F.O.Khassanov and four species from section Annuloprason form two successive lineages sister to all other examined members of these four subgenera (Fig. 1C, PP = 1·00, BS < 50 %). The remaining members are divided into seven subclades and form a large polytomy.
Biogeographical analysis
The following five areas were considered for biogeographical analysis of Amerallium and its allies: (A) eastern Asia, (B) the Mediterranean region, (C) central North America, (D) western North America and (E) eastern North America. The optimal reconstruction (Fig. 3) required eight dispersals to explain the present distribution of Amerallium and their allies and favoured the ancestor of Amerallium as having originated in eastern Asia (node 1; A: 64·91 %, AB: 35·08 %). The most favoured reconstructions at node 2 (AD: 63·31 %, BD: 36·69 %) indicated both eastern Asia and North America as ancestral areas for Amerallium. For Anguinum, Vvedenskya, Porphyroprason, Melanocrommyum and their allies, the following seven areas were defined: (A) eastern Asia, (B) eastern North America, (C) western North America, (D) Europe and Siberia, (E) West Asia and adjacent areas, (F) Central Asia and (G) the Mediterranean. The optimal reconstruction (Fig. 4) required 26 dispersals to explain the present distribution of Anguinum, Vvedenskya, Porphyroprason, Melanocrommyum and their allies and indicated that their ancestor originated in eastern Asia (node 1). The reconstruction of ancestral areas suggested an eastern Asia origin for Anguinum (node 13) and a central Asian origin for Vvedenskya, Porphyroprason and Melanocrommyum (node 3).
Dispersal–vicariance scenarios for Amerallium and its allies reconstructed by statistical dispersal–vicariance (S-DIVA) optimization with the maximum number of area units set to two. The phylogeny is a Bayesian tree with ambiguities resolved arbitrarily. Pie charts at internal nodes represent the marginal probabilities for each alternative ancestral area derived by using S-DIVA. Triangle: vicariance event; rhomb: duplication event (speciation within the area); arrow (+): dispersal event. Letters denote area units as described in the text.
Dispersal–vicariance scenarios for Anguinum, Vvedenskya, Porphyroprason, Melanocrommyum and their allies reconstructed by statistical dispersal–vicariance (S-DIVA) optimization with the maximum number of area units set to two. The phylogeny is a Bayesian tree with ambiguities resolved arbitrarily. Pie charts at internal nodes represent the marginal probabilities for each alternative ancestral area derived by using S-DIVA. Triangle: vicariance event; rhomb: duplication event (speciation within the area); arrow (+): dispersal event. Letters denote area units as described in the text.
DISCUSSION
Variation in the ITS and rps16 intron sequences
Genetic distances in ITS and atpB-rbcL sequences are apparently high (Klaas and Friesen, 2002) and in genetic variation the genus Allium resembles plant families in other groups of the angiosperms (Baldwin et al., 1995). Our analysis suggests large genetic distances are also found in the plastid rps16 intron (up to 9 %). These findings imply that the genus Allium is of ancient origin and molecular evolution has not been accompanied with a rise in pronounced morphological divergence (Friesen et al., 2006). The wide area of distribution and pronounced molecular differences of Allium indicate that this genus was probably already well differentiated in the early Tertiary (Hanelt et al., 1992; Dubouzet and Shinoda, 1999). Janssen and Bremer (2004) reported that divergence within the crown group Amaryllidaceae began about 87 Mya, providing additional evidence. Allium could be one of the many herbaceous groups that, according to Tiffney (1985), formed part of the floor of the boreotropical forests that covered northern latitudes during the Eocene.
In contrast, our data show some species (e.g. A. ovalifolium var. ovalifolium, A. ovalifolium var. cordifolium, A. ovalifolium var. leuconeurum, A. nanodes and A. prattii) share almost identical ITS and/or rps16 intron sequences, and the low average pairwise genetic distances in terminal groups consisting of several species suggest that these groups underwent recent radiation.
Phylogeny within the genus Allium
The results presented here robustly support the earlier finding that Allium is monophyletic (Friesen et al., 2006). Previous evidence for three main evolutionary lines in the evolution of Allium reported in Fritsch (2001), Fritsch and Friesen (2002) and Friesen et al. (2006) has been largely corroborated in our present work. Our molecular data allow us to conclude that Allium evolution proceeded along three separate evolutionary lines. The most ancient line consists of only bulbous plants from subgenera Nectaroscordum, Microscordum and Amerallium (Fig. 1A), which rarely produce a notable rhizome (Fritsch and Friesen, 2002). The second evolutionary line comprises subgenera Caloscordum, Anguinum, Vvedenskya, Porphyroprason and Melanocrommyum (Fig. 1B), the third evolutionary line comprises subgenera Butomissa, Cyathophora, Rhizirideum, Allium, Cepa, Reticulatobulbosa and Polyprason (Fig. 1C), and these two evolutionary lines contain both rhizomatous and bulbous taxa.
Phylogeny in the first evolutionary line
In the first evolutionary line (Fig. 1A), Amerallium is sister group to either Microscordum or Nectaroscordum and their close affinities are also supported by some common characters of leaf anatomy (Fritsch, 1988).
Nectaroscordum comprises species distributed in the eastern Mediterranean. Lindley (1836) recognized this group as the segregated genus Nectaroscordum; this taxonomy induced a great deal of controversy. Some authors (Vvedensky, 1935; Traub, 1968, 1972; Dahlgren et al., 1985; Mes et al., 1997; Friesen et al., 2006) considered Nectaroscordum to be a subgenus of Allium, while others (Stearn, 1978; Davis, 1984; Hanelt et al., 1992) excluded Nectaroscordum from classifications of the genus Allium. Our phylogenetic analysis supports inclusion of Nectaroscordum as a separate subgenus in Allium and indicates its close relationship with Amerallium and Microscordum. Its subgeneric level was also suggested in previous molecular and morphological studies. Phylogenetic analysis of rbcL sequences (Fay and Chase, 1996) and ITS sequences (Dubouzet and Shinoda, 1998; Friesen et al., 2006) affirmed that Nectaroscordum was closely related to Allium. The vascular bundles of Nectaroscordum and Amerallium are arranged in one row (Traub, 1968) and the laticifers in subgenera Amerallium and Nectaroscordum are hypodermal in the bulb scale (Traub, 1972). The joint occurrence of several specific characters such as large and three- to seven-veined tepals, a wider than long ovary, multiovulate locules, heavy seed with three sharp edges, a wide secretory channel and a basic chromosome number of x = 9 implies a long and separate phylogenetic history of this subgenus (Stearn, 1955, 1978; Mathew and Baytop, 1984; Fritsch, 1992,b; Friesen et al., 2006).
Microscordum is characterized by one- or two-flowered inflorescences, feathery ends of the stigmatic lobes and the occurrence of dioecy. This monotypic eastern Asian group shares similar morphological characters of bulbs, bulb tunics, leaves and flowers with species of subgenus Amerallium (Friesen et al., 2006). Plants of A. monanthum were shown to constitute a polyploid complex, consisting of diploid, triploid and tetraploid individuals based on the basic chromosome number x = 8. Such cytological peculiarities form the background of the complex sexuality and predominant asexual reproduction of A. monanthum (Noda and Kawano, 1988; Kawano et al., 2005). Our molecular data verify its systematic position close to Amerallium and Nectarosordum.
Amerallium is the largest subgenus in the first evolutionary line and is extremely diverse morphologically and ecologically. Morphological synapomorphies for Amerallium include one row of vascular bundles, absence of palisade parenchyma and a subepidermal position of laticifers (Fritsch, 1988). Furthermore, strong serological affinities and the predominant basic chromosome number of x = 7 strongly support its separate status, although x = 8, 9, 10 and 11 (Traub, 1968; Huang et al., 1995; Xu et al., 1998) also occur in several groups. The results provide additional support for earlier findings that Amerallium is monophyletic (Samoylov et al., 1995; Dubouzet and Shinoda, 1999) and further verify its close relationships with subgenus Microscordum and Nectaroscordum (Friesen et al., 2006). In accordance with studies of Dubouzet and Shinoda (1999), our molecular data underline the existence of two distinct biogeographical clades, namely the Old World clade and the New World clade. This also agrees with a uniform electrophoretic banding pattern of salt-soluble seed storage proteins (Maass, 1992). Furthermore, the present results indicate that Amerallium comprises three isolated geographical groups: one consisting mainly of all Allium species native to North America (New World) and the remainder containing two smaller groups from the Mediterranean region and eastern Asia (Old World).
Phylogeny in the second evolutionary line
In the second evolutionary line (Fig. 1B), subgenus Caloscordum is sister to Anguinum, Vvedenskya, Porphyroprason and Melanocrommyum. Anguinum is sister to Vvedenskya, Porphyroprason and Melanocrommyum. Vvedenskya and Porphyroprason form a clade sister to the large clade consisting of the Melanocrommyum species.
Caloscordum is an oligotypic group with three species restricted to eastern Asia (Hanelt et al., 1992). Its different geographical distribution, anatomy of the scape and root and structure of septal nectaries (Fritsch, 1992a, b, 1993), three-lobed stigma, peculiar ultrastructure of testa (Kruse, 1992b) and winter dormancy (Pistrick, 1992) justify its delimitation as a separate subgenus near Melanocrommyum (Ohri et al., 1998). Our molecular data indicate that Anguinum, Vvedenskya, Porphyroprason and Melanocrommyum are equally related to Caloscordum through their common ancestor and Caloscordum is monophyletic. It shows an affinity with Melanocrommyum on the basis of multiovulate locules, seed weight, leaf arrangement, subterranean leaf sheaths, partially joined tepals and the presence of relatively large inner vascular bundles in the scapes (Friesen et al., 1986; Hanelt et al., 1992; Fritsch, 1993; Hanelt and Fritsch, 1994). Simple characters of seed testa cells (Kruse, 1984, 1988) support its relationship with subgenus Anguinum morphologically.
Anguinum has a disjunct distribution in high mountains from south-western Europe to eastern Asia and in north-eastern North America (Fritsch and Friesen, 2002). It is characterized by specific root anatomical characters (Fritsch, 1992a), leaf and bulb structure (Pastor and Valdes, 1985), hypogeal seed germination and A. victorialis-type seedlings (Druselmann, 1992), uniovulate locules (Hanelt, 1992), narrow, branched and lengthwise-twisted septal nectaries (Fritsch, 1992b) and a short vegetative period with adaptation to the light regime under deciduous forest conditions (Pistrick, 1992). Species of Anguinum also share the basic chromosome number x = 8, the 2A type karyotype and similar metaphase chromosomes (Jing et al., 1999). Based on the consistency of its morphological, anatomical and cytological characteristics, it is thus a rather distinct and specialized group. According to our molecular studies, Anguinum is monophyletic and shares a most recent common ancestor with Vvedenskya, Porphyroprason and Melanocrommyum and is the sister group to Caloscordum. Its simple seed testa sculpture (Kruse, 1984, 1988), which shares most characters with Caloscordum, implies their close relationships, and serological data reveal its affinity with Melanocrommyum (Hanelt et al., 1992). In agreement with Friesen et al. (2006), two sister groups exist in this subgenus: one with a Eurasian–American distribution and the other restricted to eastern Asia. The polytomy formed by the eastern Asia species was interpreted as a rapid radiation that coincided with the colonization of the Hengduan Mountains and adjacent areas.
Our molecular data indicate that subgenera Vvedenskya and Porphyroprason have a recent common ancestor and those two monotypic groups form a clade sister to Melanocrommyum. Multiovulate locules and the narrowly campanulate flowers of Vvedenskya indicate its affinity with Melanocrommyum, and the lax inflorescence with rather few flowers and the small subglobose bulbs with several stalked side bulbs and membranous tunics also imply its close relationship with Porphyroprason (Friesen et al., 2006). The scape and the cylindrical and tubular leaves of Vvedenskya are densely ribbed and bear short hairs differing considerably from Porphyroprason, which may support its delimitation as a separate subgenus. Porphyroprason is characterized by several specific morphological characters, including planar venation of leaf blades, occurrence of up to three veins in the outer tepals, a tripartite stigma, three or four ovules per locule, and evenly granulous periclinal walls and only slightly undulate anticlinal walls of the seed testa cells (Friesen et al., 2006). Shape and position of nectaries and excretory tubes and serological characters underline its close relationship with Melanocrommyum (Hanelt et al., 1989).
Melanocrommyum is the largest subgenus in the second evolutionary line and is extremely diverse morphologically. Species of Melanocrommyum occur from the Mediterranean to the Near and Middle East, reaching north-western China and Pakistan in the east, and southern Siberia in the north, with Central Asia being the important centre of evolution (Fritsch, 1990; Hanelt et al., 1992; Khassanov and Fritsch, 1994; Mes et al., 1999). Well-developed leaf sheaths restricted to subterranean parts, the extremely short developmental period and several anatomical characters, including two opposite rows of vascular bundles in leaf blades and true palisade parenchyma composed of radial-only, slightly elongated cells, are considered synapomorphies for this subgenus (Fritsch, 1992a; Hanelt et al., 1992). Furthermore, all members show epigeal germination with seedlings of the A. karataviense type (Druselmann, 1992) and share uniform karyotypes without any clear species-specific or section-specific characteristics (Fritsch and Astanova, 1998). A strongly unreduced, salt-soluble seed storage protein with molecular weight of 65 000–70 000 was found in this subgenus only (Maass, 1992). None of the above character states occurs in any other subgenus of Allium, and it is obviously a monophyletic group. Our ITS data corroborate the monophyly of Melanocrommyum and indicate its close affinity with subgenera Vvedenskya and Porphyroprason.
Phylogeny in the third evolutionary line
The evolutionary history in the third evolutionary line is complex. Subgenera Butomissa and Cyathophora form two successive lineages sister to the clade formed by the remaining species. Subgenus Rhizirideum is sister to subgenera Allium, Cepa, Reticulatobulbosa and Polyprason, and relationships among the last four subgenera are not well resolved (Figs 1C and 2).
Butomissa forms the first branching group in the third evolutionary line. This small subgenus includes about four species (Friesen et al., 2006), some of which inhabit the Siberian–Mongolian–North Chinese steppes, and the others are distributed in mountains from eastern to central Asia and into the eastern Mediterranean area (Fritsch and Friesen, 2002). Position, shape and excretory tube of the nectaries show rather simple character states (Fritsch, 1992b), which may imply it is the earliest-branching group in the third evolutionary line. Its growth form (Kruse, 1992a) and chromosome morphology are as simple as in section Rhizirideum G.Don ex Koch (Friesen, 1988), but multiovulate locules, serological data and rather high TKW (thousand kernel weight) (Hanelt, 1992) show relationships to subgenera Melanocrommyum and Anguinum. Our phylogenetic analysis suggests that Butomissa occupies a position between these subgenera closer to subgenera Cyathophora and Rhizirideum.
Cyathophora includes about five species mainly distributed in Tibet and the Himalayas (Friesen et al., 2006). All species have biovulate locules (Hanelt, 1992). Furthermore, all species share only one row of identically orientated vascular bundles in the leaf blades combined with the presence of palisade parenchyma and subcortical laticifers, which is perhaps the most ancient character combination in Allium (Fritsch, 1988). Our results indicate Milula has close relationships with Cyathophora and Coleoblastus, which is also suggested by Friesen et al. (2000) based on a molecular study and anatomical investigations of leaf characters.
Species of Rhizirideum are Eurasian steppe taxa showing the most diversity in southern Siberia and Mongolia. The simple form of nectaries without an excretory tube (Fritsch, 1992b) and differing karyotypes in every section (Friesen, 1988) reveal its phylogenetically rather ancient state. Short periods of time between speciation events would readily explain the polytomies observed in section Rhizirideum, and the occurrence of the polyploid complex in the A. senescens alliance (Friesen, 1992; He, 1999) could be connected with the recent origin of these species.
Species from subgenera Allium, Cepa, Reticulatobulbosa and Polyprason form the largest clade in the third evolutionary line. Our molecular data suggest that these subgenera are not monophyletic. Furthermore, the systematic position of some species should also be reconsidered. For example, on the basis of our molecular results, A. kaschianum, formerly attributed to section Oreiprason, fell in a clade comprising species from section Falcatifolia N.Friesen and A. togashii, formerly attributed to section Rhizirideum, clustered with species from section Reticulatobulbosa Kamelin s.s. However, better sampling, multiple unlinked loci and improved analyses would be desirable before suggesting any taxonomic change for these species and would be necessary to better understand the evolutionary history of these Allium species. We propose that the large polytomy formed by species from these subgenera reflects a rapid diversification of their ancestors. Similarly, the reason that species from section Schoenoprasum are placed in a polytomy could be a recent origin.
Implications for biogeography
Amerallium.
The separation between the Old and New World branches of subgenus Amerallium, evidenced by geographical and molecular data, has fuelled doubts in many researchers (Dubouzet and Shinoda, 1999), and the origin and migration about Amerallium has been long in dispute. Hanelt et al. (1992) postulated that Amerallium had its origins in Asia and spread to North America via the Bering Land Bridge, but they did not discuss the origins of the Mediterranean Amerallium species. The alternative hypothesis is a predominantly unidirectional migration via the Bering and North Atlantic land bridges (Dubouzet and Shinoda, 1999). Although Dubouzet and Shinoda (1999) made analyses of every possible route and provided a time frame for every route in their research on the relationships among Old and New World Allium species, the migration routes in Amerallium are still not clear.
Using a molecular phylogenetic reconstruction, the optimal solution and the current geographical distribution pattern of species (Fig. 3), we suggest the following biogeographical hypotheses for Amerallium. The sister group of Amerallium is Nectaroscordum and Microscordum, which are confined to the Mediterranean and eastern Asia, respectively. Thus, the Old World is implicated as the centre of origin for Amerallium. The basal Old World–New World split (node 2) in Amerallium might reflect an early vicariance event that did not impact the other taxa, perhaps because transcontinental distributions had not yet been established in these groups (Donoghue, 2001). The ancestor of Amerallium originated at high latitudes of eastern Asia during the transition from Cretaceous to Tertiary (node 1); this was followed by an early dispersal to western North America (+D, the internode leading to node 2). The dispersion and vicariance (node 2) may have occurred first, before diversification within either the Old World or the New World. One lineage of Amerallium probably spread eastward to North America via the Bering Land Bridge and expanded their range southward. Two separate groups (sections Lophioprason and Rhophetoprason + Caulorhizideum + Amerallium) were isolated and this isolation resulted in the divergence of North America Amerallium (Nguyen et al., 2008). Western North America has acted as an important centre of diversification within North America Amerallium. S-DIVA optimal reconstructions suggest that western North America was the ancestral area in the basal duplication events, where it underwent duplication (speciation within the area), and gave rise to two different lineages. One of them, the ancestor of section Lophioprason, remained in western North America, where it diversified, and afterward dispersed to central North America (+C) followed by vicariance between west and central North American (node 9). Then for A. cernuum, dispersal events occurred from western North America into central North America (+C) and eastern North America (+E). The second North America lineage (sections Rhophetoprason + Caulorhizideum + Amerallium) probably dispersed from western North America to central North America (+C) followed by vicariance between western and central North America (node 7) and resulted in local diversification in central North America. Then for A. canadense var. canadense, a dispersal event occurred from central North America into eastern North America (+E). Dispersal events for A. canadense var. canadense and A. cernuum occurred at terminal tips (i.e. they are not inferred as ancestral areas at terminal nodes), indicating that these events correspond to recent range expansions (Sanmartín, 2003). The other lineage of Amerallium expanded its range from east to west and ended up in the Mediterranean region, not across the North Atlantic. Diversification within Old World Amerallium presumably involved dispersal to the Mediterranean region (+B), followed by a vicariance event (node 6). One part of this lineage (eastern Asian Amerallium) survived in the Himalayan region and the area south of the Qinglin Mountains (China) and diverged into section Bromatorrhiza – comprising about eight species and two varieties – whereas the other part of this lineage (Mediterranean region Amerallium) originated in the Mediterranean region (B) by duplication, probably after dispersal from eastern Asia. Successive duplication events within the Mediterranean region gave rise to several sections including Narkissoprason, Briseis, Arctoprasum and Molium. The unidirectional migration is less probable, because it involves two intercontinental dispersals, whereas the first route requires only one.
Anguinum.
Two distinct groups exist in Anguinum, one with a Eurasian–American distribution and the other restricted to the Hengduan Mountains and adjacent areas. For Anguinum, the basal sister group is Caloscordum. Thus, eastern Asia is implicated as the centre of origin for the ancestor of Anguinum. Using molecular phylogenetic reconstruction, the optimal solution and the current distribution of species (Fig. 4), we suggest the following biogeographical hypotheses for Anguinum. The ancestral reconstruction for node 13 suggests eastern Asian as the ancestral area for Anguinum, where it underwent duplication, and gave rise to two different lineages. One of them, the ancestor of the eastern Asia alliance clade (node 23), remained in eastern Asia (eastern Himalaya and areas south of the Qinlin Mountains), and successive duplication events within eastern Asia gave rise to several closely related taxa (A. ovalifolium var. ovalifolium, A. ovalifolium var. cordifolium, A. ovalifolium var. leuconeurum, A. funckiifolium, A. nanodes and A. prattii). The low average pairwise genetic distances (0·00–0·31 % for ITS; 0·07–0·41 % for rps16) among these species and polytomies formed by these species in the Bayesian tree (Figs 1B and 2) suggest that this lineage underwent a recent radiation, and the region from the Hengduan Mountains to the Qinling Range is the centre of the present distribution and source of differentiation of this lineage (Jing et al., 1999). The second eastern Asian lineage (the ancestor of the Eurasian–American alliance clade, node 22) probably dispersed westward and across the North Atlantic Land Bridge to north-eastern North America (+B), where A. tricoccum originated and diverged into two varieties (A. tricoccum var. tricoccum and A. tricoccum var. burdickii). The other descendant of this lineage perhaps stayed in eastern Asia and diverged into several species including A. listera, A. microdictyon, A. ochotense and A. victorialis and then several dispersal events occurred at terminal tips. For A. microdictyon, a dispersal event occurred from eastern Asia to Siberia (+D). For A. victorialis, dispersal events occurred from eastern Asia to western North America (+C), Europe and Siberia (+D) and Central Asia (+F). Furthermore, A. victorialis sensu lato (s.l.) is found in North America only on Attu Island, where it is reported to be native, and on Unalaska Island, where it is reported to have been introduced from Attu Island (Dale et al., 2002). We agree with Hultén (1933) and propose that A. victorialis s.l. from the Kamchatka Peninsula was dispersed to Attu Island by natural means.
Vvedenskya, Porphyroprason and Melanocrommyum.
Phylogenetic reconstruction suggests that Vvedenskya, Porphyroprason and Melanocrommyum have close affinities with Caloscordum and Anguinum and together they comprise the second evolutionary line in the evolution of Allium. Vvedenskya, Porphyroprason and Melanocrommyum are late-branching groups, whereas Caloscordum and Anguinum are early branching. Caloscordum is restricted to eastern Asia and Anguinum is mainly distributed in eastern Asia. Thus, eastern Asia is implicated as the ancestral distribution area for the ancestor of Vvedenskya, Porphyroprason and Melanocrommyum. S-DIVA to the second evolutionary lineage indicates that the ancestor of Porphyroprason, Vvedenskya and Melanocrommyum originated in eastern Asia (Fig. 4, node 1), then dispersed to Central Asia (+F, the internode leading to node 2) along the north coast of the Tethys sea, namely the Cayan–Alai Mountain ranges. The ancestral reconstruction for node 3 including all Porphyroprason, Vvedenskya and Melanocrommyum species favours Central Asia as the ancestral area. We propose the following biogeographical hypotheses for Vvedenskya and Porphyroprason. The two subgenera evolved in Central Asia and differentiated into two species, A. kujikense and A. oreophilum, respectively. Then for A. oreophilum, a dispersal event occurred from Central Asia into western Asia and adjacent areas (+E). The upheaval of the Tien-shan/Alai mountain range and retreat of the former Tethys sea during the late Oligocene and early Miocene (Guo et al., 2002) would have left the Asian interior more arid and would also have formed many new ecological niches. Based on the optimal solution and palaeogeographical data, we propose the following biogeographical hypotheses for Melanocrommyum. Melanocrommyum evolved in Central Asia, where it underwent duplication, and quickly colonized the territories of the former Tethys sea and radiated in Central Asia. The resulting taxa expanded their ranges via dispersal into other areas such as western Asia (+E, i.e. the internode leading to nodes 15, 16, 35, 37, 46, 53, 59, 74 and 79 and another four dispersal events occurred at terminal tips) and the Mediterranean (i.e. +G, the internode leading to node 27) and diversified in these regions, followed by dispersion from western Asia to Central Asia (+F, i.e. the internode leading to nodes 75 and 77 and another dispersal event occurred at terminal tip) and from western Asia to the Mediterranean (+G, i.e. the internode leading to node 36 and the other dispersal event occurred at terminal tip). The striking morphological variability of the species is hardly reflected by molecular data (Linne von Berg et al., 1996), which may also indicate that the radiation is a relatively recent phenomenon.
Because of the lack of resolution within the third evolutionary line of Allium, we could not analyse the biogeography using S-DIVA. Species of this evolutionary line have a wide distribution in Eurasia, which may indicate that the ancestor of these species originated in Asia. Butomissa is the first branching group and is now distributed in Siberia, eastern Asia, central Asia and the eastern Mediterranean area. Cyathophora is a solely Asian (Tibet and the Himalayas) group and is sister to the remaining groups including Rhizirideum, Allium, Cepa, Polyprason and Reticulatobulbosa. The lack of resolution among these remaining groups suggests that subsequent dispersal events and speciation were rapid, and they eventually spread into Eurasia, extending into the Mediterranean and temperate north-eastern and subarctic regions of America (Hanelt et al., 1992).
These analyses imply that Allium may have originated in Asia or more exactly in eastern Asia and that various subgenera underwent different biogeographical pathways that involved different numbers of vicariant and dispersal events, and further studies should be carried out to test and verify this hypothesis. We also hope that it will be possible to sort clades into categories for comparison based directly on age estimates and to infer which palaeoclimatic or palaeogeographical events impacted on the dispersal and vicariance of Allium.
Taxonomic implications and intrageneric classification of Chinese Allium
Allium spp. have adapted to diverse habitats and display a remarkable polymorphism, which is the main reason for the widely recognized difficulties in taxonomy and classification of Allium. Moreover, the traditional infrageneric classifications are based on some homoplasious characters (Fritsch and Friesen, 2002). Both these factors make it difficult to select natural evolutionary lineages using easily discernible characteristics. Today, biologists are adopting a system of classification based on phylogenetics, which reflects the evolutionary processes that have shaped life, including Allium spp.
The division of the included species in clades (Figs 1 and and2)2) is for the most part in accordance with the accepted taxonomic division based on traditional taxonomy or the new classification of Friesen et al. (2006). However, our phylogenetic analysis (Figs 1C and 2) provides some new findings. Both ITS and combined analyses strongly support placing A. przewalskianum in section Eduardii, and their close similarities in morphology (Xu, 1980) also indicate a close relationship. In both ITS and combined analyses, A. flavovirens forms an isolated branch, which provides evidence that it deserves sectional rank. Nevertheless, the circumscription of the new section and the identification of diagnostic characters are premature and further morphological and molecular studies are required.
Our taxon sample covers roughly 70 % of the known Allium spp. in China assembled to represent almost all taxonomic groups. Based on previous morphological studies and molecular data and our own results, we propose a synopsis (Appendix 3) which divides Chinese Allium into 13 subgenera and 34 sections (containing all the species recorded in Allium in Flora of China plus A. spicatum). The subgenera are listed according to their position in the phylogenetic tree (Figs 1 and and2),2), and a list of species is given for every section and subgenus. We believe this to be helpful because this is the first intrageneric classification treatment of Allium in China since the Flora of China for Allium was published. Unfortunately, we did not obtain ITS or rps16 sequences of some species and we were not able to conduct phylogenetic analysis on all the described taxa in China. We could only deduce the true position of these species from morphological characteristics and geographical distribution; in the appendices below, species for which the systematic position needs to be further tested and verified are marked with question marks.
SUPPLEMENTARY DATA
ACKNOWLEDGEMENTS
We thank the handling editor and the three reviewers for their comments and suggestions on the manuscript. We thank Jie-Mei Xu for comments on a previous draft of the manuscript and Zhen-Xin Fan for helpful suggestions. We also thank Chang-Bao Wang, Cheng-Yang Liao, Yun-Dong Gao, Xiang-Guang Ma and Li-Hua Zhao for interesting discussions and valuable help during field trips. This work was supported by the Doctoral Fund of the Ministry of Education of China (20090181110064), the Basic Research Program from the Ministry of Science and Technology of China (2007FY110100), the Research Fund for the Large-scale Scientific Facilities of the Chinese Academy of Sciences (2009-LSF-GBOWS-01), and grants from the National Natural Science Foundation of China (31070166).
APPENDIX 1
New accessions of Allium and outgroups from which ITS and rps16 intron sequences were obtained, with corresponding voucher information and GenBank reference numbers. A dash indicates the region was not sampled. The information is listed as follows: taxon — ITS, rps16 intron; voucher information.
Allium: A. altaicum Pall. —GQ181094, GU566637; Burqin, Xinjiang, China; He X-J & Zhang X-L 97643. A. anisopodium Ledeb. —GQ181095, GU566650; Zhongwei, Ningxia, China; He X-J et al. 97834. A. bidentatum Fisch. ex Prokh. & Ikonn.-Gal. —GQ181096, GU566655; Ximeng, Nei Mongol, China; He X-J et al. 97813. A. caeruleum Pall. —GQ181064, GU566645; Yumin, Xinjiang, China; He X-J & Zhang X-L 97609. A. carolinianum DC. —GQ181097, GU566627; Wulumuqi, Xinjiang, China; He X-J & Zhang X-L 97656. A. cepiforme G.Don—GU566611, GU566635; Chengdu Botanical Garden, China; Li Q-Q 09011511. A. changduense J.M.Xu—GQ181065, GU566631; Changdu, Tibet, China; Zhang Y-C B19. A. chrysanthum Regel—GQ181066, GU566639; Huzhu, Xining, China; Xu J-M 97–5–663. A. chrysocephalum Regel—GU566612, GU566640; Qinhai Lake, Qinhai, China; Ma X-G 09080401. A. condensatum Turcz. —GQ181098, GU566643; Daqing Mountain, Nei Mongol, China; He X-J & Zhang X-L 97827. A. cyanum Regel—GQ181099, GU566632; Queer Mountain, Sichuan, China; Zhang Y-C B25. A. cyathophorum Bureau & Franch.—GQ181093, GU566659; Zhongdian, Yunnan, China; Xu J-M 93–17. A. eduardii Stearn ex Airy Shaw—GQ181100, GU566657; Daqing Mountain, Nei Mongol, China; He X-J et al. 97829. A. eusperma Airy Shaw—GQ181067, –; Batang, Sichuan, China; Zhang Y-C B03. A. fasciculatum Rendle—GQ181068, GU566674; Dazi, Xizang, China; Tu Y-L et al. 94-9. A. fistulosum L. — –, GU566638; Chengdu Botanical Garden, China; Li Q-Q 091201. A. flavovirens Regel—GQ181069, GU566634; Bayanhoti, Nei Mongol, China; He X-J et al. 97830. A. forrestii Diels—GQ181070, GU566633; Queer Mountain, Sichuan, China; Zhang Y-C B24. A. galanthum Kar. & Kir.—GQ181101, GU566636; Altai, Xinjiang, China; He X-J & Zhang X-L 97631. A. hookeri Thwaites var. hookeri— –, GU566672; Lijiang, Yunnan, China; Li Q-Q 09072702. A. hookeri var. muliense Airy Shaw—GQ181071, GU566671; Zhongdian, Yunnan, China; Xu J-M 93 –25. A. hymenorrhizum Ledeb.—GQ181102, GU566626; Burqin, Xinjiang, China; He X-J & Zhang X-L 97641. A. lineare L.—GQ181103, GU566629; Wulumuqi, Xinjiang, China; He X-J & Zhang X-L 97606. A. listera Stearn—GQ181063, GU566668; Dongfeng, Jilin, China; Tuliguer 91001. A. macranthum Baker—GQ181072, GU566675; Zhongdian, Yunnan, China; Xu J-M 93–23. A.macrostemon Bunge—GU566613, GU566646; Wenchuan, Sichuan, China; Li Q-Q 09060601. A. mairei H.Lévl. —GU566614, GU566658; Lijiang, Yunnan, China; Ma X-G 09102407. A. maowenense J. M.Xu—GQ181073, –; Wenchuan, Sichuan, China; Yu H 97836. A. mongolicum Regel—GQ181074, GU566649; Saihan, Nei Mongol, China; He X-J et al 97802. A. nanodes Airy Shaw—GU566615, GU566666; Daocheng, Sichuan, China; Li Q-Q 09080101. A. nutans L.—GQ181075, GU566652; Burqin, Xinjiang, China; He X-J & Zhang X-L 97635. A. obliquum L. —GQ181104, –; Tacheng, Xinjiang, China; He X-J & Zhang X-L 97604. A. omeiense Z.Y.Zhu—GQ181076,GU566673; Emei Mountain, Sichuan, China; Xu J-M 91-01. A. oreoprasum Schrenk—GQ181105, GU566660; Tuoli, Xinjiang, China; He X-J & Zhang X-L 97619. A. ovalifolium Hand.-Mazz. var. ovalifolium—GQ181084, GU566663; Kangding, Sichuan, China; Li Q-Q 2008081202. A. ovalifolium var. cordifolium (J. M. Xu) J.M.Xu—GQ181085, GU566664; Xiaojin, Sichuan, China; Li Q-Q 2008081703. A.ovalifolium var. leuconeurum (J.M.Xu) J.M.Xu—GU566616, GU566665; Lixian, Sichuan, China; Li Q-Q 09060901. A. pallasii Murr. —GQ181077, GU566644; Emin, Xinjiang, China; He X-J & Zhang X-L 97603. A. petraeum Kar. & Kir. —GQ181106, –; Yumin, Xinjiang, China; He X-J & Zhang X-L 97610. A. platyspathum Schrenk—GQ181078, –; Wulumuqi, Xinjiang, China; He X-J & Zhang X-L 97628. A. plurifolium Rendle var. plurifoliatum—GU566617, GU566625; Taibai Mountain, Shanxi, China; Li Q-Q 09080807. A. plurifoliatum var. zhegushanense J.M.Xu—GQ181086, –; Maerkang, Sichuan, China; Li Q-Q 2008081905. A. polyrhizum Turcz. ex Regel—GQ181107, GU566648; Saihan, Nei Mongol, China; He X-J et al. 97804. A. prattii C.H.Wright ex Hemsley—GQ181087, GU566667; Xiaojin, Sichuan, China; Li Q-Q 2008081603. A. przewalskianum Regel—GU566618, GU566656; Lintan, Ganshu, China; Wei X-Q 09072802. A. ramosum L. —GQ181079, GU566661; Daqing Mountain, Nei Mongol, China; He X-J et al. 97812. A. rude J.M.Xu—GQ181080, GU566641; Xiaojin, Sichuan, China; Li Q-Q 2008081701. A. saxatile M.Bieb. —GQ181108, GU566625; Wulumuqi, Xinjiang, China; He X-J & Zhang X-L 97626. A. senescens L. —GU566619, GU566653; Manzhouli, Nei Mongol, China; Wang C-B 09062. A. sikkimense Baker—GQ181088, –; Maerkang, Sichuan, China; Li Q-Q 2008082001. A. spirale Willd. —GU566620, GU566654; Helingeer, Nei Mongol, China; Li Q-Q 20080903. A. strictum Schrad. —GU566621, GU566628; Tuoli, Xinjiang, China; He X-J & Zhang X-L 97636. A. subtilissimum Ledeb. —GQ181081, GU566647; Wulumuqi, Xinjiang, China; He X-J & Zhang X-L 97650. A. tanguticum Regel—GQ181089, –; Zuodao, Qinhai, China; Feng T et al. 20080701. A. tenuissimum L. — GQ181090, GU566651; Helingeer, Nei Mongol, China; Li Q-Q 20080902. A. tuberosum Rottler ex Spreng. — –, GU566662; Foping, Shanxi, China; Li Q-Q2008092501. A. tubiflorum Rendle—GU566622, GU566670; Hua Mountain, Shanxi, China; Liao C-Y C072804. A. victorialis L. —GQ181082, GU566669; Dunhua, Jilin, China; Tuliguer 91002. A. wallichii Kunth var. wallichii—GQ181091, GU566676; Kangding, Sichuan, China; Li Q-Q 2008081203. A. wallichii var. platyphyllum (Diels) J.M.Xu—GU566624, GU566677; Lijiang, Yunnan, China; Li Q-Q 09072503. A. xichuanense J.M.Xu—GQ181083, GU566642; Queer Mountain, Sichuan, China; Zhang Y-C B29. A. yuanum F.T.Wang & Tang —GQ181092, –; Maerkang, Sichuan, China; Li Q-Q 2008082003.
Outgroups: Nothoscordum gracile (Aiton) Stearn— –, GU566678; Kunming Botanical Garden, China; Liao C-Y et al. 091117. Tulbaghia violacea Harv.—GU566623, GU566679; Chengdu Botanical Garden, China; Li Q-Q et al. 091110.
APPENDIX 2
Previously published ITS and rps16 accessions obtained from GenBank
ITS accessions of Allium and outgroups obtained from GenBank. 1,Dubouzet and Shinoda (1998); 2,Dubouzet and Shinoda (1999); 3,Friesen et al. (2000); 4,Ricroch et al. (2005); 5,Friesen et al. (2006); 6,Gurushidze et al. (2007); 7,Gurushidze et al. (2008); 8,Nguyen et al. (2008); 9,Sinitsyna and Friesen (2008).
Allium: A. abramsii (Ownbey & Aase) McNeal EU0961318; A. aflatunense B.Fedtsch. FM1772397; A. akaka S.G.Gmel. ex Schult. & Schult.f. FM1772427; A. alaicum Vved. FM1772507; A. albidum Fisch. ex Bieb. AJ4118925; A. alexeianum Regel FM1772477; A. altissimum Regel FM1772517; A. altyncolicum N.Friesen AJ4119395; A. ampeloprasum L. AY4275304; A. amplectens Torr. AF0550972; A. anceps Kellogg EU0961348; A. angulosum L. EU0961368; A. arkitense R.M.Fritsch FM1772567; A. aroides Popov & Vved. FM1772597; A. asarense R.M.Fritsch & Matin AM4183656; A. aschersonianum Barbey FM1772607; A. assadii Seisums FM1772617; A. atropurpureum Waldst. & Kit. FM1772627; A. atrorubens S.Watson var. atrorubens EU0961378; A. atrorubens var. cristatum (S.Watson) McNeal EU0961388, A. atrosanguineum Schrenk var. atrosanguineum AJ4118645; A. atrosanguineum var. fedschenkoanum (Regel) G.H.Zhu & Turland AJ4118445; A. atroviolaceum Boiss. AJ4118845; A. austrosibiricum N.Friesen AJ4118325; A. azutavicum Kotukhov AM9496009, A. backhousianum Regel FM1772647; A. bakhtiaricum Regel FM1772697; A. beesianum W.W.Sm. AJ4118605, A. bolanderi S.Watson var. bolanderi EU0961398; A. brachyscapum Vved. FM1772737; A. brevidens Vved. AJ4127215; A. breviscapum Stapf FM1772747; A. brevistylum S.Watson AJ4127635, A. bucharicum Regel FM1772757; A. bulgaricum (Janka) Prodan AJ4127475; A. burjaticum N.Friesen AM9496029; A. burlewii Davidson EU0961428; A. caesium Schrenk AJ4127315; A. campanulatum S.Watson EU0961438; A. canadense L. var. canadense EU0961458; A. cardiostemon Fisch. & C.A.Mey. FM1772777; A. caspium subsp. baissunense FM1772677; A. caspium (Pall.) M.Bieb. subsp. caspium FM1772807; A. cepa L. AM4183706; A. cernuum Roth AF0376221, A. chamaemoly L. AF0551092; A. chamarense M.M.Ivanova AJ4119575; A. chelotum Wendelbo FM1774647; A. chinense G.Don AJ4118485; A. chitralicum F.T.Wang & Tang FM1772837; A. chodsha-bakirganicum Gaffarov & Turak. FM1772857; A. christophii Trautv. FM1772727; A. clathratum Ledeb. AJ4118555; A. costatovaginatum Kamelin & Levichev FM1772867; A. cratericola Eastw. EU0961468; A. crispum Greene EU0961478; A. crystallinum Vved. AJ4127245; A. cupanii Raf. AJ4127375; A. cupuliferum Regel subsp. cupuliferum FM1772927; A. cyrilli Ten. FM1774627; A. daghestanicum Grossh. AJ4118505; A. darwasicum Regel FM1774527; A. dasyphyllum Vved. FM1773057; A. decipiens Fisch. ex Schult. & Schult.f. FM1773067; A. denticulatum (Ownbey & Aase ex Traub) McNeal EU0961498; A. dentigerum Prokh. AJ4119585; A. derderianum Regel FM1773087; A. diabolense (Ownbey & Aase) McNeal EU0961508; A. dichlamydeum Greene EU0961518; A. dodecadontum Vved. FM1774617; A. dregeanum Kunth AJ4119625; A. drepanophyllum Vved. AJ4118545; A. drobovii Vved. AJ4118955; A. drummondii Regel AJ4119085; A. elburzense Wendelbo FM1773117; A. elegans Drobow AJ4127305; A. ellisii Hook.f. FM1773847; A. eremoprasum Vved. AJ4127265; A. ericetorum Thore AJ3118675; A. falcifolium Hook. & Arn. EU0961538; A. farctum Wendelbo AM4921847; A. fetisowii Regel FM1773167; A. filidens Regel AJ4127235; A. filidentiforme Vved. AJ4127225; A. fimbriatum S.Watson var. fimbriatum EU0961558; A. fimbriatum var. purdyi (Eastw.) McNeal EU0961568; A. fistulosum L. AM4183716; A. flavescens Besser AJ4118425; A. flavidum Ledeb. AJ4119565; A. flavum L. var. minus AJ4119265; A. giganteum Regel FM1773207; A. gilgiticum F.T.Wang & Tang AJ4127625; A. glandulosum Link & Otto AJ4127465; A. goodingii Ownbey AF0550952; A. griffithianum Boiss. AJ4118625; A. gunibicum Miscz. ex Grossh AM4183616; A. gypsaceum Popov & Vved. FM1773227; A. haematochiton S.Watson EU0961578; A. haneltii F.O.Khass. & R.M.Fritsch AJ4127255; A. heldreichii Boiss. AY4275394; A. helicophyllum Vved. FM1773247; A. hexaceras Vved. FM1773267; A. hickmanii Eastw. EU0961598; A. hirtifolium Boiss. AF0376121; A. hissaricum Vved. FM1773287; A. hoffmanii Ownbey EU0961608; A. hollandicum R.M.Fritsch FM1773337; A. hookeri Thwaites AJ4127405; A. howellii Eastw. var. howellii EU0961618; A. hyalinum Curran EU0961628; A. inaequale Janka AJ4127355; A. incensiodorum Radic AJ4118665; A. insubricum Boiss. & Reut. AJ2502913; A. insufficiens Vved. FM1773347; A. iranicum (Wendelbo) Wendelbo AJ4119615; A. isakulii subsp. balkhanicum R.M.Fritsch & F.O.Khass. FM1772717; A. isakulii subsp. subkopetdagense R.M.Fritsch & F.O.Khass. FM1774277; A. jepsonii (Ownbey & Aase) S.S.Denison & McNeal EU0961638; A. jesdianum subsp. angustitepalum (Wendelbo) F.O.Khass. & R.M.Fritsch FM1772537; A. jesdianum Boiss. & Buhse subsp. Jesdianum FM1773377; A. jodanthum AJ4119025; A. karataviense Regel FM1773417; A. karelinii Poljakov AJ4118765; A. kaschianum Regel AJ4127545; A. kingdonii Stearn AJ2502865; A. koelzii (Wendelbo) Perss. & Wendelbo FM1773137, A. komarovianum Vved. AJ4127605, A. komarowii Lipsky FM1773427; A. kopetdagense Vved. AJ4119505; A. kuhsorkhense R.M.Fritsch & Joharchi FM1773867; A. kujukense Vved. AJ4119475; A. kunthianum Vved. AJ4127345; A. kuramense F.O.Khass. & N.V.Friesen AJ4118685; A. kurssanovii Popov AJ3118695; A.ledebourianum Schult. & Schult.f. AJ4119255; A. lemmonii S.Watson EU0961648; A. leucocephalum Turcz. ex Ledeb. AJ4127575; A. lipskyanum Vved. FM1773487; A. litvinovii Drobow ex Vved. AJ4127275; A. lusitanicum Lam. AJ4118315; A. macleanii Baker FM1773517; A. majus Vved. FM1773557; A. malyschevii N.Friesen AJ4127585; A. margaritae B.Fedtsch. AJ4127325; A. materculae Bordz. FM1773567; A. maximowiczii Regel AJ4118775; A. melanantherum Pancic AJ4127395; A. membranaceum Ownbey ex Traub EU0961658; A. microdictyon Prokh. AJ4118595; A. minorense ined. AJ4127485; A. minutiflorum Regel FM1774467; A. moly L. AF0551082; A. monadelphum Turcz. ex Kar. et Kir. AJ4119555; A. monanthum Maxim. AJ4127455; A. montibaicalense N.Friesen AJ4118385; A. moschatum L. AJ4118725; A. motor Kamelin & Levichev FM1773647; A. neapolitanum Cirillo AF0551042; A. neriniflorum (Herb.) G.Don AJ4119205; A. nevskianum Vved. FM1773657; A. nigrum L. FM1773687; A. noëanum Reut. ex Regel FM1773747; A. obtusum Lemmon EU0961668; A. ochroleucum Waldst. et Kit. subsp. ochroleucum AJ4127555; A. ochroleucum subsp. pseudosuaveolens Zahar. AJ4118635; A. oliganthum Kar. & Kir. AJ4118355; A. oreophilum C.A.Mey. AF0376201; A. oreoprasoides Vved. AJ4118965; A. orientale Boiss. FM1773777; A. oschaninii O.Fedtsch. AM4183766; A. pamiricum Wendelbo AJ4127365; A. paniculatum L. AJ4119495; A. paradoxum (M.Bieb.) G.Don AJ4127415; A. parvulum Vved. AJ4127205; A. parvum Kellogg EU0961698; A. peninsulare Lemmon ex Greene var. peninsulare EU0961708; A. platycaule S.Watson EU0961718; A. platyspathum subsp. amblyophyllum (Kar. & Kir.) N.Friesen AJ4118755; A. platyspathum Schrenk subsp. platyspathum AJ4118785; A. porrum L. AY4275434; A. praecox Brandegee EU0961738; A. praemixtum Vved. AM4183796; A. prostratum Trevir. AM9496049; A. protensum Wendelbo FM1773807; A. pseudobodeanum R.M.Fritsch & Matin FM1773817; A. pseudowinklerianum R.M.Fritsch & F.O.Khass. FM1773877; A. pskemense B.Fedtsch. AM4183826; A. punctum L.F.Hend. EU0961748; A. regelii Trautv. FM1773897; A. robustum Kar. & Kir. FM1773917; A. rosenbachianum subsp. kwakense R.M.Fritsch FM1773457; A. rosenbachianum Regel subsp. rosenbachianum FM1773937; A. rosenorum R.M.Fritsch FM1773957; A. roseum L. AF0551052; A. rothii Zucc. FM1774007; A. roylei Stearn AM4921896; A. rubens Schrad. ex Willd. AM9496199; A. rupestre Steven AJ4127335; A. rupestristepposum N.Friesen AJ4118695; A. sanbornii Alph.Wood var. sanbornii EU0961778; A. saposhnikovii Nikitina FM1774057; A. sarawschanicum Regel FM1774067; A. sativum L. AF0376211; A. scabriscapum Boiss. AJ4118815; A. schachimardanicum Vved. FM1774107; A. schmitzii Cout. AJ4127615; A. schoenoprasoides Regel AJ4127285; A. schoenoprasum L. subsp. schoenoprasum AF0551122; A. schoenoprasum subsp. latiorifolium (Pau) Rivas Mart. AJ4118375; A. schubertii Zucc. FM1774117; A. schugnanicum Vved. FM1774127; A. scorodoprasum L. AJ4127135; A. semenovii Regel AJ4118975; A. sergii Vved. AJ4119365; A. serra McNeal & Ownbey EU0961788; A. setifolium Schrenk AJ4118985; A. severtzovioides R.M.Fritsch FM1774147; A. sewerzowii Regel FM1774037; A. sharsmithiae (Ownbey & Aase) McNeal EU0961798; A. shelkovnikovii Grossh. FM1774137; A. shevockii McNeal EU0961808; A. siculum Ucria AJ2502993; A. siskiyouense Munz & Keck ex Ownbey EU0961818; A. sordidiflorum Vved. AJ4118995; A. sphaerocephalon L. AJ4127175; A. spicatum (Prain) N.Friesen AJ2502853; A. splendens Willd. ex Schult. & Schult.f. AJ4119275; A. spurium G.Don AM9496359; A. stellatum Nutt. ex Ker Gawl. EU0961838; A. stellerianum Willd. subsp. splendens AJ4119635; A. stipitatum Regel AJ4119115; A. suaveolens Jacq. AJ4118745; A. subangulatum Regel AJ4118705; A. subhirsutum L. AF0551062; A. sulphureum Vved. AJ4127595; A. suworowii Regel FM1774307; A. taeniopetalum Popov & Vved. var. taeniopetalum FM1774337; A. taeniopetalum subsp. turakulovii R.M.Fritsch & F.O.Khass. FM1774437; A. talassicun Regel AJ4118655; A. tashkenticum F.O.Khass. & R.M.Fritsch FM1774347; A. tenuicaule Regel AJ4118875; A. teretifolium Regel AJ4118865; A. thunbergii G.Don AJ4118495; A. togashii H.Hara AJ4118435; A. trachyscordum Vved. AJ4118575; A. trautvetterianum Regel FM1774387; A. tribracteatum Torr. EU0961848; A. tricoccum Sol. AJ4119175; A. triquetrum L. AJ4127425; A. tuberosum Rottler ex Spreng. AJ4119145; A. tulipifolium Ledeb. FM1774427; A. tuolumnense (Ownbey & Aase) S.S.Denison & McNeal EU0961858; A. turkestanicum Regel AJ4119685; A. tuvinicum (N.Friesen) N.Friesen AM9496099; A. tytthocephalum Schult. & Schult.f. AM9496329; A. ubsicola Regel AJ4119605; A. umbilicatum Boiss. AJ4127195; A. unifolium Kellogg EU0961868; A. ursinum L. AJ4127445; A. validum S.Watson EU0961888; A. vavilovii Popov & Vved. AM4183836; A. verticillatum Regel FM1774477; A. viridulum Ledeb. FM1774497; A. vodopjanovae N.Friesen subsp. vodopjanovae AJ4118455; A. vodopjanovae subsp. czemalense N.Friesen AJ3118685; A. vvedenskyanum Pavlov FM1774517; A. weschniakowii Regel AJ4119465; A. winklerianum Regel FM1774557; A. xiphopetalum Aitch. et Baker AJ4118585; A. yosemitense Eastw. EU0961898; A. zebdanense Boiss. & Noë AY4275524; A. zergericum F.O.Khass. & R.M.Fritsch FM1774567.
Outgroups: Dichelostemma capitatum (Benth.) Alph. Wood subsp. capitatum EU0961908; Dichelostemma congestum (Smith) Kunth EU0961918; Dichelostemma ida-maia (Alph.Wood) Greene EU0961928; Dichelostemma multiflorum (Benth.) A. Heller EU0961938; Dichelostemma volubile (Kellogg) A.Heller EU0961948; Ipheion uniflorum (Graham) Raf. AJ4127155; Nothoscordum gracile (Ait.) Stearn AJ4127165; Nothoscordum bivalve (L.) Britton AJ2503013; Tulbaghia fragrans Verdoorn AJ2503003.
rps16 accessions obtained from GenBank
10Umehara et al. (unpublished); 11,Ryzhova et al. (2009).
Allium: A. ampeloprasum FJ65370011; A. cepa L. AB29230010; A. obliquum FJ65367111; A. sativum FJ65368811; A. schoenoprasum FJ65370511.
APPENDIX 3
Taxonomic synopsis of the genus Allium L. in China
First evolutionary line
1. Subgenus Microscordum (Maxim.) N.Friesen.—Type: A. monanthum Maxim. (monotypic).
1.1. Section Microscordum Maxim.—Type: A. monanthum Maxim.
1.1.1. A. monanthum Maxim.
2. Subgenus Amerallium Traub.—Type: A. canadense L.
2.1. Section Bromatorrhiza Ekberg.
2.1.1. A. guanxianense J.M.Xu
2.1.2. A. xiangchengense J.M.Xu
2.1.3. A. hookeri Thwaites
2.1.3a. A. hookeri var. hookeri
2.1.3b. A. hookeri var. muliense Airy Shaw
2.1.4. A. omeiense Z.Y.Zhu
2.1.5. A. chienchuanense J.M.Xu
2.1.6. A. fasciculatum Rendle
2.1.7. A. wallichii Kunth
2.1.7a. A. wallichii var. wallichii
2.1.7b. A. wallichii var. platyphyllum (Diels) J.M.Xu
2.1.8. A. macranthum Baker
Second evolutionary line
3. Subgenus Caloscordum (Herb.) R.M.Fritsch.—Type: A. neriniflorum (Herbert) G.Don
3.1. Section Caloscordum (Herb.) Baker.—TYPE: A. neriniflorum (Herbert) G.Don
3.1.1. A. tubiflorum Rendle
3.1.2. A. inutile Makino
3.1.3. A. neriniflorum (Herbert) G.Don
4. Subgenus Anguinum (G.Don ex Koch) N.Friesen.—Type: A. victorialis L.
4.1. Section Anguinum G.Don ex Koch.—Type: A. victorialis L.
4.1.1. A. victorialis L.
4.1.2. A. listera Stearn
4.1.3. A. ovalifolium Hand.-Mazz.
4.1.3a. A. ovalifolium var. ovalifolium
4.1.3b. A. ovalifolium var. leuconeurum J.M.Xu
4.1.3c. A. ovalifolium var. cordifolium (J.M.Xu) J.M.Xu
4.1.4. A. funckiifolium Hand.-Mazz.
4.1.5. A. nanodes Airy Shaw
4.1.6. A. prattii C. H. Wright ex Hemsley
5. Subgenus Porphyroprason (Ekberg) R.M.Fritsch.—Type: A. oreophilum C.A.Mey. (monotypic).
5.1. Section Porphyroprason Ekberg.—TYPE: A. oreophilum C.A.Mey.
5.1.1. A. oreophilum C.A.Mey.
6. Subgenus Melanocrommyum (Webb & Berth.) Rouy.—Type: A. nigrum L.
6.1. Section Melanocrommyum Webb & Berth.—Type: A. nigrum L.
6.1.1. A. tulipifolium Ledeb.
6.1.2. A. roborowskianum Regel
6.1.3. A. robustum Kar. & Kir.
6.2. Section Acmopetala R. M. Fritsch.—Type: A. backhousianum Regel
6.2.1. A. fetisowii Regel
6.3. Section Regeloprason Wendelbo.—Type: A. regelii Trautv.
6.3.1. A. winklerianum Regel
Third evolutionary line
7. Subgenus Butomissa (Salisb.) N.Friesen.—Type: A. ramosum L.
7.1. Section Butomissa (Salisb.) Kamelin.—Type: A. ramosum L.
7.1.1. A. tuberosum Rottler ex Spreng.
7.1.2. A. ramosum L.
7.2. Section Austromontana N.Friesen.—Type: A. oreoprasum Schrenk
7.2.1. A. oreoprasum Schrenk
8. Subgenus Cyathophora (R.M.Fritsch) R.M.Fritsch.—Type: A. cyathophorum Bur. & Franch.
8.1. Section Cyathophora R.M.Fritsch.—Type: A. cyathophorum Bur. & Franch.
8.1.1. A. cyathophorum Bur. & Franch.
8.1.1a. A. cyathophorum var. cyathophorum
8.1.1b. A. cyathophorum var. farreri (Stearn) Stearn
8.1.2. A. trifurcatum (F.T.Wang & Tang) J.M.Xu?
8.2. Section Coleoblastus Ekberg.—Type: A. mairei H.Lévl.
8.2.1. A. mairei H.Lévl.
8.2.2. A. kingdonii Stearn
8.2.3. A. rhynchogynum Diels
8.3. Section Milula (Prain) N.Friesen.—Type: A. spicatum (Prain) N.Friesen.
8.3.1. A. spicatum (Prain) N.Friesen
9. Subgenus Rhizirideum (G.Don ex Koch) Wendelbo s.s. Type: A. senescens L.
9.1. Section Rhizirideum G.Don ex Koch s.s.—Type: A. senescens L.
9.1.1. A. prostratum Trevir.
9.1.2. A. rubens Schrad. ex Willd.
9.1.3. A. brevidentatum F.Z.Li
9.1.4. A. taishanense J.M.Xu
9.1.5. A. chiwui F.T.Wang & Tang
9.1.6. A. spurium G.Don
9.1.7. A. spirale Willd.
9.1.8. A. senescens L.
9.1.9. A. nutans L.
9.2. Section Caespitosoprason N.Friesen.—Type: A. polyrrhizum Siev.
9.2.1. A. mongolicum Regel
9.2.2. A. yongdengense J.M.Xu?
9.2.3. A. subangulatum Regel
9.2.4. A. polyrhizum Turcz. ex Regel
9.2.5. A. bidentatum Fisch. ex Prokh. & Ikonn.-Gal.
9.2.6. A. dentigerum Prokh.
9.3. Section Rhizomatosa Egor.—Type: A. caespitosum Siev. ex Bong. & C.A.Mey.
9.3.1. A. caespitosum Siev. ex Bong. & C.A.Mey.
9.4. Section Tenuissima (Tzagolova) Hanelt.—Type: A. tenuissimum L.
9.4.1. A. tenuissimum L.
9.4.2. A. elegantulum Kitag.
9.4.3. A. anisopodium Ledeb.
9.4.3a. A. anisopodium var. anisopodium
9.4.3b. A. anisopodium var. zimmermannianum (Gilg) F.T.Wang & Tang
9.5. Section Eduardia N. Friesen.—Type: A. eduardii Stearn ex Airy Shaw
9.5.1. A. eduardii Stearn ex Airy Shaw
9.5.2. A. przewalskianum Regel
9.5.3. A. siphonanthum J.M.Xu?
10. Subgenus Allium.—Type: A. sativum L.
10.1. Section Allium L. —Type: A. sativum L.
10.1.1. A. porrum L.
10.1.2. A. sativum L.
10.1.3. A. macrostemon Bunge
10.2. Section Caerulea (Omelcz.) F.O.Khassanov.—Type: A. caeruleum Pall.
10.2.1. A. caeruleum Pall.
10.2.2. A. caesium Schrenk
10.2.3. A. sairamense Regel?
10.2.4. A. jacquemontii Kunth?
10.2.5. A. juldusicola Regel?
10.3. Section Pallasia (Tzagolova.) F.O.Khassanov, R.M.Fritsch & N.Friesen.—Type: A. pallasii Murr.
10.3.1. A. delicatulum Siev. ex Schult. & Schult.f.
10.3.2. A. eusperma Airy Shaw
10.3.3. A. pallasii Murr.
10.3.4. A. glomeratum Prokh.?
10.3.5. A. schoenoprasoides Regel
10.3.6. A. songpanicum J.M.Xu?
10.3.7. A. tanguticum Regel
10.4. Section Eremoprasum (Kamelin) F.O.Khassanov, R.M.Fritsch & N.Friesen.—Type: A. sabulosum Steven ex Bunge
10.4.1. A. sabulosum Steven ex Bunge
11. Subgenus Cepa (Mill.) Radić.—Type: A. cepa L.
11.1. Section Cepa (Mill.) Prokh.—Type: A. cepa L.
11.1.1. A. altaicum Pall.
11.1.2. A. fistulosum L.
11.1.3. A. cepa L.
11.1.3a. A. cepa var. cepa
11.1.3b. A. cepa var. proliferum (Moench) Regel
11.1.3c. A. cepa var. aggregatum G.Don
11.1.4. A. cepiforme G.Don
11.1.5. A. galanthum Kar. & Kir.
11.2. Section Annuloprason T.V.Egorova.—Type: A. fedschenkoanum Regel.
11.2.1. A. semenovii Regel
11.2.2. A. atrosanguineum Schrenk
11.2.2a. A. atrosanguineum var. atrosanguineum
11.2.2b. A. atrosanguineum var. fedschenkoanum (Regel) G.Zhu & Turland
11.2.2c. A. atrosanguineum var. tibeticum (Regel) G.Zhu & Turland
11.2.3. A.weschniakowii Regel
11.3. Section Condensatum N. Friesen.—Type: A. condensatum Turcz.
11.3.1. A. longistylum Baker?
11.3.2. A. alabasicum Y.Z.Zhao?
11.3.3. A. condensatum Turcz.
11.4. Section Sacculiferum P.P.Gritz.—Type: A. sacculiferum Maxim.
11.4.1. A. grisellum J.M.Xu?
11.4.2. A. chinense G.Don
11.4.3. A. yanchiense J.M.Xu?
11.4.4. A. sacculiferum Maxim.
11.4.5. A. thunbergii G.Don
11.5. Section Schoenoprasum Dumort.—Type: A. schoenoprasum L.
11.5.1. A. schoenoprasum L.
11.5.1a. A. schoenoprasum var. schoenoprasum
11.5.1b. A. schoenoprasum var. scaberrimum Regel
11.5.2. A. oliganthum Kar. & Kir.
11.5.3. A. maximowiczii Regel
11.5.4. A. ledebourianum Schult. & Schult.f.
11.6. Section Flavovirens Q.Q.Li & X.J.He—Type: A. flavovirens Regel (monotypic).?
11.6.1. A. flavovirens Regel
12. Subgenus Reticulatobulbosa (Kamelin) N.Friesen.—Type: A. lineare L.
12.1. Section Reticulatobulbosa Kamelin s.s.—Type: A. lineare L.
12.1.1. A. humile Kunth?
12.1.2. A. lineare L.
12.1.3. A. schrenkii Regel?
12.1.4. A. amphibolum Ledeb.
12.1.5. A. strictum Schrad.
12.1.6. A. splendens Willd. ex Schult. & Schult.f.
12.1.7. A. maackii (Maxim.) Prokh. ex Kom.
12.1.8. A. clathratum Ledeb.
12.1.9. A. flavidum Ledeb.
12.1.10. A. leucocephalum Turcz. ex Ledeb.
12.2. Section Campanulata Kamelin.—Type: A. xiphopetalum Aitch.
12.2.1. A. teretifolium Regel
12.2.2. A. tekesicola Regel?
12.2.3. A. korolkowii Regel?
12.3. Section Sikkimensia (Traub) N.Friesen.—Type: A. sikkimense Baker.
12.3.1. A. forrestii Diels
12.3.2. A. changduense J.M.Xu
12.3.3. A. beesianum W.W.Smith
12.3.4. A. yuanum F.T.Wang & Tang
12.3.5. A. sikkimense Baker
12.3.6. A. cyaneum Regel
12.3.7. A. aciphyllum J.M.Xu
12.3.8. A. henryi C.H.Wright
12.3.9. A. heteronema F.T.Wang & Tang
12.3.10. A. paepalanthoides Airy Shaw
12.3.11. A. plurifoliatum Rendle
12.3.11a. A. plurifoliatum var. plurifoliatum
12.3.11b. A. plurifoliatum var. zhegushanense J.M.Xu
12.3.12. A. stenodon Nakai & Kitag.
13. Subgenus Polyprason Radić.—Type: A. moschatum L.
13.1. Section Oreiprason F.Herm.—Type: A. saxatile M.Bieb.
13.1.1. A. obliquum L.
13.1.2. A. saxatile M.Bieb.
13.1.3. A. petraeum Kar. & Kir.
13.1.4. A. tianschanicum Rupr.?
13.1.5. A. megalobulbon Regel?
13.1.6. A. pevtzovii Prokh.?
13.1.7. A. caricoides Regel?
13.1.8. A. kurssanovii Popov
13.1.9. A. setifolium Schrenk
13.1.10. A. subtilissimum Ledeb.
13.2. Section Falcatifolia N.Friesen.—Type: A. carolinianum DC.
13.2.1. A. hymenorhizum Ledeb.
13.2.1a. A. hymenorhizum var. hymenorhizum
13.2.1b. A. hymenorhizum var. dentatum J.M.Xu
13.2.2. A. kaschianum Regel
13.2.3. A. carolinianum DC
13.2.4. A. blandum Wall.?
13.2.5. A. phariense Rendle?
13.2.6. A. platyspathum Schrenk
13.2.6a. A. platyspathum subsp. platyspathum
13.2.6b. A. platyspathum subsp. amblyophyllum (Kar. & Kir.) N.Friesen
13.3. Section Daghestanica (Tscholok.) N.Friesen.—Type: A. daghestanicum Grossh.
13.3.1. A. rude J.M.Xu
13.3.2 A. chrysocephalum Regel
13.3.3. A. xichuanense J.M.Xu
13.3.4. A. chrysanthum Regel
13.3.5. A. maowenense J.M.Xu
13.3.6. A. herderianum Regel?
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