Annals of Botany 106: 709 –733, 2010
doi:10.1093/aob/mcq177, available online at www.aob.oxfordjournals.org
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
Qin-Qin Li, Song-Dong Zhou, Xing-Jin He*, Yan Yu, Yu-Cheng Zhang and Xian-Qin Wei
School of Life Sciences, Sichuan University, Chengdu 610064, Sichuan, China
* For correspondence. E-mail xjhe@scu.edu.cn
Received: 18 March 2010 Returned for revision: 12 April 2010 Accepted: 21 July 2010
Key words: Allium, biogeography, classification, ITS, molecular phylogeny, rps16.
IN T RO DU C T IO N
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 ¼ 8, but
other numbers (x ¼ 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
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† 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.
710
Li et al. — Phylogeny and biogeography of Allium
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 ¼ 7, 8, 10, 11 (not
x ¼ 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.
M AT E R I A L S A N D M E T H O D S
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.
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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.)
Li et al. — Phylogeny and biogeography of Allium
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 8C for
5 min; 30 cycles of 94 8C for 45 s, 55 8C for 45 s and 72 8C
for 1 min; and 72 8C 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.
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 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.
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; Sanmartı́n et al., 2008), DIVA remains
popular because it provides rapid results, requires little prior
information, and gives results comparable with the modelbased 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 (Sanmartı́n, 2003)
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Sequence comparisons and phylogenetic analyses
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Li et al. — Phylogeny and biogeography of Allium
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Subgenera
Amerallium
Microscordum
Nectaroscordum
Outgroups
F I G . 1. 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.
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0·54/<50
Sections
A. sanbornii var.sanbornii
A. jepsonii
A. abramsii
A. diabolense
A. fimbriatum var. fimbriatum
A. howellii var. howellii
A.tuolumnense
A.fimbriatum var. purdyi
A. denticulatum
A. sharsmithiae
A. membranaceum
A. campanulatum
A. atrorubens var. cristatum
A. atrorubens var. atrorubens
A. shevockii
A. tribracteatum
A. yosemitense
A. obtusum
A. hoffmanii
A. cratericola
A. platycaule
Lophioprason
A. lemmonii
A. parvum
A. anceps
A. burlewii
A. punctum
A. falcifolium
A. siskiyouense
A. haematochiton
A. cernuum
A. stellatum
A. hickmanii
A. hyalinum
A. amplectens
A. unifolium
A. praecox
A. dichlamydeum
A. serra
A. crispum
A. peninsulare var. peninsulare
A. bolanderi var. bolanderi
Rhophetoprason
A. glandulosum
A. validum
Caulorhizideum
A. goodingii
A. brevistylum
A. drummondii
Amerallium
A. canadense var. canadense
A. zebdanense
A. subhirsutum
Molium
A. neapolitanum
A. roseum
A. chamaemoly
A. moly
Arctoprasum
A. ursinum
A. paradoxum
Briseis
A. triquetrum
Narkissoprason
A. insubricum
A. hookeri var. hookeri
A. hookeri var. muliense
A. omeiense
Bromatorrhiza
A. fasciculatum
A. macranthum
A. wallichii var. wallichii
A. wallichii var. platyphyllum
Microscordum
A. monanthum
A. siculum
Nectaroscordum
A. bulgaricum
Dichelostemma multiflorum
Dichelostemma congestum
Dichelostemma ida-maia
Dichelostemma volubile
Dichelostemma capitatum subsp. capitatum
Ipheion uniflorum
Tulbaghia fragrans
Nothoscordum bivalve
Nothoscordum gracile
Tulbaghia violacea
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Clade 2
Sections
Compactoprason
Subgenera
Kaloprason
Popovia
Acaule
Aroidea
Megaloprason
Compactoprason
Procerallium
Compactoprason
Regeloprason
Acmepetala
Brevicaule
Miniprason
Regeloprason
Brevicaule
Melanocrommyum
Megaloprason
Stellata
Regeloprason
Verticillata
Regeloprason
Acanthoprason
Melanocrommyum
Kaloprason
Pseudoprason
Regeloprason
Asteroprason
Regeloprason
Megaloprason
Acmopetala
Decipientia
Longibidentata
Porphyroprason
Vvedenskya
Porphyroprason
Vvedenskya
Anguinum
Anguinum
Caloscordum
Caloscordum
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A. bakhtiaricum
A. giganteum
A. macleanii
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A. winklerianum
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A. hissaricum
A. lipskyanum
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A. chodsha-bakirganicum
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A. schachimardanicum
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A. helicophyllum
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A. kujukense
A. oreophilum
A. ovalifolium var. ovalifolium
1·00
67
A. ovalifolium var. cordifolium
1·00/100
A. ovalifolium var. leuconeurum
A. nanodes
A. prattii
1·00/99
67
A.
microdictyon
1·00
1·00
A. listera
99
A.
victorialis
1·00/84
A. tricoccum
A.
tubiflorum
1·00/100
A. neriniflorum
F I G . 1. Continued
713
714
Li et al. — Phylogeny and biogeography of Allium
C
1·00/<50
1·00/<50
1·00/89
1·00/83
Clade 3
B
F I G . 1. Continued
A. flavoriens
A. maximowiczii
1·00/86
A. karelinii
A. ledebourianum
A. altyncolicum
1·00/100
A. oliganthum
A. schmitzii
A. schoenoprasum var. latiorifolium
0·53/<50
A. schoenoprasum var. schoenoprasum
A. vavilovii
0·98/76
1·00
A. cepa
85
57
A. asarense
0·99
A. roylei
0·64/<50
A. farctum
1·00/86
A. oschaninii
1·00/87
1·00/76
A. praemixtum
0·69
A. pskemense
<50
A. galanthum
A. cepiforme
0·90/66
1·00/96
A. fistulosum
A. altaicum
A. monadelphum
1·00/91
A. atrosanguineum var. atrosanguineum
1·00/100
A. semenovii
1·00/86
A. atrosanguineum var. fedschenkoanum
A. kurssanovii
1·00/95
1·00/91
A. elegans
1·00/100
A. caesium
0·73/<50
A. caeruleum
0·59/<50
A. schoenoprasoides
A. haneltii
0·65/<50
1·00/95
A. litvinovii
A. eremoprasum
0·90/<50
A. macrostemon
A. przewalskianum
1·00/96
A. eduardii
A. nutans
0·88/63
A. austrosibiricum
A. prostratum
1·00/80
A. spurium
A. spirale
A. stellerianum
1·00/78
A. senescens
A. rubens
A. tuvinicum
1·00/95
A. burjaticum
A. senescens var. minor
1·00/100
A. incensiodorum
A. lusitanicum
A. angulosum
A. azutavicum
1·00/61
A. tytthocephalum
A. flavescens
0·99/80
A. albidum
A. anisopodium
1·00/97
1·00/100
0·88/<50
A. tenuissimum
A. vodopjanovae subsp. vodopjanovae
A. vodopjanovae subsp. czemalense
1·00/100
A. bidentatum
A. subangulatum
1·00/100
1·00/85 1·00
A. polyrhizum
62
A. dentigerum
1·00/<50
A. mongolicum
1·00/100
A. subtilissimum
A. kingdonii
1·00/100
A. mairei
0·96/72
A. spicatum
A. cyathophorum
1·00/100
1·00/97
A. weschniakowii
A. gilgiticum
1·00/81
A. oreoprasum
1·00/99
A. ramosum
A. tuberosum
1·00/100
1·00/61
A. heldreichii
Sections
Flavovirens?
Subgenera
Schoenoprasum
Cepa
Cepa
Annuloprason
Oreiprason
Polyprason
Caerulea
Pallasia
Brevidentia
Caerulea
Kopetdagia
Allium
Allium
Eduardia
Rhizirideum
Rhizirideum
Tenuissima
Caespitosoprason
Oreiprason
Coleoblastus
Milula
Cyathophora
Annuloprason
Polyprason
Cyathophora
Cepa
Austromontana
Butomissa
Butomissa
Allium
Allium
Downloaded from http://aob.oxfordjournals.org/ by guest on June 20, 2013
1·00/<50
C-2
Li et al. — Phylogeny and biogeography of Allium
D C-2
C-1
F I G . 1. Continued
Sections
Rhizirideum
Scorodon
Subgenera
Rhizirideum
Polyprason
Reticulatobulbosa
Reticulatobulbosa
Campanulata
Nigrimontana
Scabriscapum
Oreiprason
Polyprason
Pallasia
Allium
Campanulata
Oreiprason
Scorodon
Reticulatobulbosa
Mediasia
Avulsea
Oreiprason
Allium
Falcatifolia
Polyprason
Polyprason
Allium
Brevidentia
Costulatae
Allium
Crystallina
Avulsea
Minuta
Brevispatha
Codonoprasum
Brevispatha
Kopetdagia
Pallasia
Condensatum
Sacculiferum
Sikkimensia
Cepa
Reticulatobulbosa
Oreiprason
Daghestanica
Polyprason
Downloaded from http://aob.oxfordjournals.org/ by guest on June 20, 2013
A. togashii
A. moschatum
A. leucocephalum
0·99/51
A. rupestristepposum
0·84/<50
A. clathratum
A. splendens
1·00/72
A. malyschevii
A. chamarense
A. ubsicola
1·00/100 0·66/<50
A. strictum
0·63
A. lineare
<50
A. montibaicalense
A. flavidum
A. sordidflorum
1·00/82
1·00/71
A. xiphopetalum
1·00/81
A. drepanophyllum
1·00/100
A. minorense
0·96
70
A. kuramense
76
0·91 0·99
A. jodanthum
63 0·64/<50
A. tenuicaule
A. drobovii
0·91/56
0·53/<50
A. oreoprasoides
1·00/100
A. sulphureum
1·00/100
1·00/100
A. trachyscordum
A. scabriscapum
A. saxatile
1·00/97
A. obliquum
1·00/99
1·00/<50
A. talassicun
1·00/96
A. petraeum
A. tanguticum
1·00/100
1·00/100
A. eusperma
0·87/<50
A. teretifolium
A. setifolium
1·00/<50
1·00/85
0·99/<50
A. pamiricum
1·00/<50
A. inaequale
A. turkestanicum
1·00/100
A. griffithianum
A. kaschianum
1·00/95
0·98/77
A. hymenorrhizum
A. carolinianwn
1·00/100
A. platyspathurn subsp. platyspathum
1·00/98
A. platyspathum subsp. amblyophyllum
A. ampeloprasum
1·00/100
1·00/68
A. porrum
0·76/<50
A. iranicum
A. sphaerocephalon
1·00/100 1·00/50
A. sativum
A. atroviolaceum
A. scorodoprasum
1·00/100
1·00/94
A. dregeanum
A. brevidens
0·60/71
0·60/58
A. filidens
1·00/88
A. filidentiforme
1·00/100
A. crystallinum
1·00/<50
A. umbilicatum
1·00/99
A. parvulum
A. margaritae
A. kunthianum
1·00/96
0·63/71
A. rupestre
0·51
< 50
1·00/100
A. paniculatum
A. melanantherum
100/79
1·00/92
A. flavum var. minus
0· 52 0·99/<50
A.
cupanii
< 50
A.
kopetdagense
1·00/94
A. pallasii
A. condensatum
A. chinense
1·00/100
1·00/100
A. thunbergii
0·96/<50
A. sacculiferum
A. yuanum
0·69/<50
0·54/<50
A. sikkimense
A. plurifoliatum var. zhegushanense
1·00/100
A. beesianum
0·76/<50
A. cyaneum
1·00/91
0·51/<50
A. plurifoliatum var. plurifoliatum
A. changduense
1·00/100
A. forrestii
A. ochroleucum subsp. ochroleucum
0·95/89
1·00/100
A. suaveolens
A. ochroleucum subsp. pseudosuaveolens
0·95/65
A. ericetorum
1·00/100
69
A. daghestanicum
1·00/90 0·99
A. maowenense
A. xichuanense
1·00/97
A. chrysanthum
1·00/50
A. rude
1·00/100
A. chrysocephalum
A. gunibicum
0·97/52
715
716
Li et al. — Phylogeny and biogeography of Allium
Sections
0·84/<50
Subgenera
Evolutionary lines
A. galanthum
A. cepa
1·00/91
0·63/<50
A. altaicum
0·85
A. cepiforme
64
0·50/<50
0·76/<50
1·00/93
1·00/100
Cepa
Cepa
A. fisiulosum
A. schoenoprasum var. schoenoprasum
Schoenoprasum
A. flavoriens
Flavovirens
A. chrysanthum
A. xichuanense
Daghestanica
Polyprason
A. condensatum
Condensatum
A. pallasii
Pallasia
Cepa
Allium
Sikkimensia
Reticulatobulbosa
A. chrysocephalum
1·00/79
1·00/<50
1·00/100
1·00/70
A. rude
A. plurifoliatum var. plurifoliatum
A. cyaneum
A. changduense
1·00/97
1·00/100
A. lineare
A. obliquum
0·97/<50
0·98/<50
1·00/96
1·00/100
Reticulatobulbosa
A. strictum
A. saxatile
A. hymenorrhizum
Oreiprason
Third
Polyprason
Falcatifolia
A. carolinianum
1·00/100
A. sativum
A. ampeloprasum
1·00/100
A. caeruleum
1·00/<50
1·00/100
1·00/80
1·00/84
Allium
A. subtilissimum
Caerulea
Oreiprason
A. mongolicum
Polyprason
Caespitosoprason
A. bidentatum
A. polyrhizum
0·59/<50
1·00/100
1·00/99
Allium
A. macrostemon
1·00/81
A. anisopodium
Tenuissima
Rhizirideum
A. tenuissimum
A. spirale
0·88/<50
1·00/100
Clade 3
A. nutans
Rhizirideum
A. senescens
1·00/88
1·00/93
A. przewalskianum
Eduardia
A. eduardii
0·98/91
1·00/100
1·00/100
A. mairei
Coleoblastus
A. cyathophorum
Cyathophora
A. tuberosum
A. ramosum
A. oreoprasum
1·00/99
1·00/87
1·00/100
1·00/78
A. ovalifolium var. cordifolium
A. ovalifolium var. leuconeurum
Anguinum
Anguinum
Caloscordum
Caloscordum
Bromatorrhiza
Amerallium
Second
A. nanodes
1·00/100
1·00/100
Butomissa
Austromontana
A. prattii
A. ovalifolium var. ovalifolium
1·00/100
Butomissa
Cyathophora
A. victorialis
A. listera
Clade 2
A. tubiflorum
0·81/<50
1·00/81
1·00/96
A. hookeri var. muliense
A. hookeri var. hookeri
1·00/73
A. fasciculatum
1·00/100
First
A. macranthum
0·96/82
Clade 1
A. omeiense
A. wallichii var. wallichii
A. wallichii var. platyphyllum
Nothoscordum gracile
Tulbaghia violacea
Outgroups
F I G . 2. 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.
Downloaded from http://aob.oxfordjournals.org/ by guest on June 20, 2013
0·85/55
A. forrestii
Li et al. — Phylogeny and biogeography of Allium
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.
R E S U LT S
Molecular datasets
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 ¼ 1.00, BS ¼ 100 %).
Three major clades were found within Allium: the first major
clade (PP ¼ 1.00, BS ¼ 82 %) comprising subgenera
Nectaroscordum (Lindl.) Asch. & Graebn. (x ¼ 9), Amerallium
(x ¼ 7, 8, 9, 10, 11) and Microscordum (Maxim.) N.Friesen
(x ¼ 8); the second major clade (PP ¼ 1.00, BS ¼ 67 %) comprising subgenera Caloscordum, Anguinum, Vvedenskya,
Porphyroprason and Melanocrommyum (all x ¼ 8); and the
third major clade (PP ¼ 1.00, BS ¼ 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 ¼ 8). For
dataset 2, the ILD test conducted on the combined data matrix
of common ITS and rps16 accessions was significant (ILD probability value ¼ 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 ¼ 1.00, BS ¼ 100 %). Three major clades
were detected in this tree: the first major clade (PP ¼ 1.00,
BS ¼ 100 %) containing taxa from subgenera Amerallium, the
second major clade (PP ¼ 1.00, BS ¼ 78 %) with species from
subgenera Caloscordum and Anguinum, and the third major
clade (PP ¼ 1.00, BS ¼ 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 ¼ 1.00,
BS ¼ 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 ¼ 1.00, BS ¼ 75 %). The New World Amerallium clade
(Fig. 1A, PP ¼ 1.00, BS ¼ 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 ¼ 1.00, BS ¼ 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 ¼ 1.00, BS ¼ 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 ¼ 1.00, BS ¼ 84 %). In the Himalayas and southwest 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 ¼
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,
Downloaded from http://aob.oxfordjournals.org/ by guest on June 20, 2013
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 parsimonyinformative. 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 parsimonyinformative. 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 %.
717
718
Li et al. — Phylogeny and biogeography of Allium
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 ¼ 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).
D IS C US S IO N
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
Downloaded from http://aob.oxfordjournals.org/ by guest on June 20, 2013
A. fasciculatum, A. hookeri var. hookeri and A. hookeri var.
muliense (Fig. 2, PP ¼ 1.00, BS ¼ 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 ¼
1.00, BS ¼ 99 %). In one sister group, species from Eurasia
(A. listera, A. microdictyon and A. victorialis) form a trichotomy (Fig. 1B, PP ¼ 1.00, BS ¼ 99 %) and this trichotomy
is sister to the north-eastern North American species
A. tricoccum (Fig. 1B, PP ¼ 1.00, BS ¼ 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 ¼ 1.00, BS ¼ 100 %; Fig. 2, PP ¼ 1.00, BS ¼
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 ¼ 1.00, BS ¼ 79 %).
Splits within the third major clade are complex. In the
Butomissa clade, section Butomissa is sister to section
Austromontana (Fig. 1C, PP ¼ 1.00, BS ¼ 99 %; Fig. 2,
PP ¼ 1.00, BS ¼ 100 %). Noteworthy here is that
A. heldreichii from subgenus Allium section Allium is sister
to A. tuberosum (Fig. 1C, PP ¼ 1.00, BS ¼ 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 ¼ 0.96, BS ¼ 72 %). However, unexpected relationships were recovered for A. cyathophorum and
A. weschniakowii from subgenus Cepa section Annuloprason
T.V.Egorova (Fig. 1C, PP ¼ 1.00, BS ¼ 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 ¼ 0.88, BS , 50 %). Section Caespitosoprason is sister to
the clade consisting of sections Tenuissima and Rhizirideum
(Fig. 1C, PP ¼ 0.88, BS , 50 %; Fig. 2, PP ¼ 0.59, BS ,
50 %). Species from section Rhizirideum form polytomies
(Fig. 1C, PP ¼ 1.00, BS ¼ 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 ¼ 1.00, BS ¼ 100
%; Fig. 2, PP ¼ 1.00, BS ¼ 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 ¼ 1.00, BS , 50 %; Fig. 2, PP ¼
Li et al. — Phylogeny and biogeography of Allium
A
B
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Old World Amerallium
Mediterranean Region
Eastern Asia
2
9
F I G . 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.
Downloaded from http://aob.oxfordjournals.org/ by guest on June 20, 2013
5
A. sanbornii var. sanbornii
A. jepsonii
A. abramsii
A. diabolense
A. fimbriatum var. fimbriatum
A. howellii var. howellii
A. denticulatum
A. fimbriatum var. purdyi
A. tuolumnense
A. sharsmithiae
A. campanulatum
A. membranaceum
A. atrorubens var. atrorubens
A. atrorubens var. cristatum
A. shevockii
A. obtusum
A. yosemitense
A. tribracteatum
A. hoffmanii
A. cratericola
A. platycaule
A. lemmonii
A. parvum
A. anceps
A. burlewii
A. falcifolium
A. siskiyouense
A. punctum
A. haematochiton
A. stellatum
A. cernuum
A. hyalinum
A. hickmanii
A. amplectens
A. unifolium
A. praecox
A. dichlamydeum
A. serra
A. peninsulare var. peninsulare
A. crispum
A. bolanderi var. bolanderi
A. canadense var. canadense
A. drummondii
A. brevistylum
A. goodingii
A. glandulosum
A. validum
A. zebdanense
A. subhirsutum
A. neapolitanum
A. roseum
A. chamaemoly
A. moly
A. ursinum
A. paradoxum
A. triquetrum
A. insubricum
A. hookeri var. hookeri
A. hookeri var. muliense
A. omeiense
A. fasciculatum
A. macranthum
A wallichii var. wallichii
A. wallichii var. plalyphyllum
A. monanthum Microscordum
A. bulgaricum Nectaroscordum
A. siculum
New World Amerallium
North America
10
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Li et al. — Phylogeny and biogeography of Allium
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A. stipitatum
A. altissimum
A. hirtifolium
A. rosenorum
A. jesdianum subsp. angustitepalum
A. jesdianum subsp. jesdianum
A. hollandicum
A. bakhtiaricum
A. macleanii
A. winklerianum
A. hissaricum
A. giganteum
A. Iipskyanum
A. chodsha-bakirganicum
A. komarowii
A. protensum
A. alexeianum
A. nevskianum
A. majus
A. caspium subsp. baissunense
A. caspium subsp. caspium
A. bucharicum
A. gypsaceum
A. hexaceras
A. trautvetterianum
A. sarawschanicum
A. aroides
A. arkitense
A. alaicum
A. aflatunense
A. backhousianum
A. dodecadontum
A. schachimardanicum
A. chitralicum
A. schugnanicum
A. rosenbachianum subsp. rosenbachianum
A. darwasicum
A. insufficiens
A. rosenbachianum subsp. kwakense
A. tashkenticum
A severtzovioides
A. sewerzowii
A. costatovaginatum
A. saposhnikovii
A. dasyphyllum
A. vvedenskyanum
A. motor
A. sergii
A. karataviense
A. taeniopetalum subsp. taeniopetalum
A. taeniopetalum subsp. turokulovii
A. isakulii subsp. balkhanicum
A. isakulii subsp. subkopetdagense
A. verticillatum
A. cupuliferum subsp. cupuliferum
A. cristophii
A. ellisii
A. helicophyllum
A. kuhsorkhense
A. elburzense
A. pseudobodeanum
A. assadii
A. brachyscapum
A. regelii
A. suworowii
A. shelkovnikovii
A. materculae
A. akaka
A. breviscapum
A. derderianum
A. pseudowinklerianum
A. cardiostemon
A. rothii
A. noëanum
A. minutiflorum
A. nigrum
A. atropurpureum
A. orientate
A. cyrilli
A. aschersonianum
A. schubertii
A. koelzii
A. zergericum
A. viridulum
A. chelotum
A. tulipifolium
A. robustum
A. decipiens
A. fetisowii
A. kujukense
A. oreophilum
A. nanodes
A. ovalifolium var. ovalifolium
A. prattii
A. ovalifolium var. leuconeurum
A. ovalifolium var. cordifolium
A. listera
A. microdictyon
A. victorialis
A. tricoccum
A. neriniflorum
A. tubiflorum
Melanocrommyum
Porphyroprason
Vvedenskya
Anguinum
Caloscordum
F I G . 4. 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.
Downloaded from http://aob.oxfordjournals.org/ by guest on June 20, 2013
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Li et al. — Phylogeny and biogeography of Allium
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
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 ¼ 9 implies a long and separate phylogenetic
history of this subgenus (Stearn, 1955, 1978; Mathew and
Baytop, 1984; Fritsch, 1992b; 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 ¼ 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 ¼ 7 strongly support its
separate status, although x ¼ 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), threelobed 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,
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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.
721
722
Li et al. — Phylogeny and biogeography of Allium
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 sectionspecific 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
Downloaded from http://aob.oxfordjournals.org/ by guest on June 20, 2013
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 northeastern 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 ¼ 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,
Li et al. — Phylogeny and biogeography of Allium
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 (Sanmartı́n, 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
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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.
723
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Li et al. — Phylogeny and biogeography of Allium
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
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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.
Li et al. — Phylogeny and biogeography of Allium
S U P P L E M E N TARY D ATA
Supplementary data are available online at www.aob.
oxfordjournals.org and consist of a phylogenetic tree resulting
from a Bayesian analysis of a subset of ITS matrix (Fig. S1)
and a phylogenetic tree resulting from a Bayesian analysis of
the rps16 matrix (Fig. S2), both including 60 taxa focusing
on the Chinese Allium.
ACK N OW L E DG E M E N T S
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).
L I T E R AT U R E CI T E D
APG III. 2009. An update of the Angiosperm Phylogeny Group classification
for the orders and families of flowering plants: APG III. Botanical
Journal of the Linnean Society 161: 105–121.
Barker FK, Lutzoni FM. 2002. The utility of the Incongruence Length
Difference test. Systematic Biology 51: 625– 637.
Baldwin BG. 1992. Phylogenetic utility of the internal transcribed spacers of
nuclear ribosomal DNA in plants: an example from the Compositae.
Molecular Phylogenetics and Evolution 1: 3– 16.
Baldwin BG, Sanderson MJ, Wojciechowski JM, Campbell CS, Donoghue
MJ. 1995. The ITS region of nuclear ribosomal DNA: a valuable source
of evidence on angiosperm phylogeny. Annals of the Missouri Botanical
Garden 82: 247–277.
Blattner FR. 2004. Phylogenetic analysis of Hordeum (Poaceae) as inferred
by nuclear rDNA ITS sequences. Molecular Phylogenetics and
Evolution 33: 289–299.
Blattner FR, Friesen N. 2006. Relationship between Chinese chive (Allium
tuberosum) and its putative progenitor A. ramosum as assessed by
random amplified polymorphic DNA (RAPD). In: Zeder MA, Bradley
DG, Emshwiller E, Smith BD. eds. Documenting domestication: new
genetic and archaeological paradigms. Berkeley, CA: California
University Press, 134– 142.
Brullo S, Pavone P, Salmeri S. 1991. Allium kollmannianum, a new species
from Israel. Flora Mediterranea 1: 15–20.
Burbrink FT, Lawson R. 2007. How and when did Old World rat snakes disperse into the New World? Molecular Phylogenetics and Evolution 43:
173–189.
Calviño CI, Martı́nez SG, Downie SR. 2008. The evolutionary history of
Eryngium (Apiaceae, Saniculoideae): rapid radiations, long distance dispersals, and hybridizations. Molecular Phylogenetics and Evolution 46:
1129– 1150.
Chase MW, Reveal JL, Fay MF. 2009. A subfamilial classification for the
expanded asparagalean families Amaryllidaceae, Asparagaceae and
Xanthorrhoeaceae. Botanical Journal of the Linnean Society 161:
132–136.
Cheremushkina VA. 1992. Evolution of life forms of species in subgenus
Rhizirideum (Koch) Wendelbo, genus Allium L. In: Hanelt P, Hammer
K, Knüpffer H. eds. The genus Allium: taxonomic problems and
genetic resources. Proceedings of an international symposium held at
Gatersleben, Germany, 11–13 June 1991. Institut für Pflanzengenetik
und Kulturpflanzenforschung, Gatersleben, Germany, 27– 34.
Dahlgren RMT, Clifford HT, Yeo PF. 1985. The families of the monocotyledons: structure, evolution, and taxonomy. Berlin: Springer.
Dale W, McNeal JR, Jacobsen TD. 2002. Allium. In: Kiger E. ed. Flora of
North America, Vol. 26. Oxford: Oxford University Press, 244–275.
Davis PH. 1984. Flora of Turkey and the east Aegean islands, Vol. 8.
Edinburgh: Edinburgh University Press, 98– 211.
De Wilde-Duyfjes BEE. 1976. A revision of the genus Allium L. (Liliaceae)
in Africa. Belmontia 7: 75– 78.
Donoghue MJ, Bell CD, Li JH. 2001. Phylogenetic patterns in Northern
Hemisphere plant geography. International Journal of Plant Science
162: S41–S52.
Doyle JJ, Doyle JL. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry Bulletin, Botanical Society of
Aremenia 19: 11–15.
Druselmann S. 1992. Vergleichende Untersuchungen an Vertretern der
Alliaceae Agardh. 1. Morphologie der Keimpflanzen der Gattung
Allium L. Flora, Morphologie, Geobotanik, Oekophysiologie 186: 37– 52.
Dubouzet JG, Shinoda K. 1998. Phylogeny of Allium L. subgenus
Melanocrommyum (Webb et Berth.) Rouy based on DNA sequence analysis of the internal transcribed spacer region of nrDNA. Theoretical and
Applied Genetics 97: 541–549.
Dubouzet JG, Shinoda K. 1999. Relationships among Old and New World
Alliums according to ITS DNA sequence analysis. Theoretical and
Applied Genetics 98: 422–433.
Dubouzet JG, Shinoda K, Murata N. 1997. Phylogeny of Allium L. subgenus
Rhizirideum (G. Don ex Koch) Wendelbo according to dot blot
Downloaded from http://aob.oxfordjournals.org/ by guest on June 20, 2013
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 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 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.
725
726
Li et al. — Phylogeny and biogeography of Allium
Fritsch RM, Blattner FR, Gurushidze M. 2010. New classification of Allium
L. subg. Melanocrommyum (Webb & Berthel) Rouy (Alliaceae) based on
molecular and morphological characters. Phyton 49: 145–220.
Gregory M, Fritsch RM, Friesen N, Khassanov FO, McNeal DW. 1998.
Nomenclator alliorum: Allium names and synonyms – a world guide.
Kew: Royal Botanic Gardens, 83.
Guo ZT, Ruddiman W, Hao QZ, et al. 2002. Onset of Asian desertification
by 22Myr ago inferred from loess deposits in China. Nature 416:
159– 163.
Gurushidze M, Mashayekhi S, Blattner FR, Friesen N, Fritsch RM. 2007.
Phylogenetic relationships of wild and cultivated species of Allium
section Cepa inferred by nuclear rDNA ITS sequence analysis. Plant
Systematics and Evolution 269: 259–269.
Gurushidze M, Fritsch RM, Blattner FR. 2008. Phylogenetic analysis of
Allium subgen. Melanocrommyum infers cryptic species and demands a
new sectional classification. Molecular Phylogenetics and Evolution 49:
997– 1007.
Gurushidze M, Fritsch RM, Blattner FR. 2010. Species level phylogeny of
Allium subgenus Melanocrommyum – incomplete lineage sorting, hybridization and trnF gene duplication. Taxon 59: 829–840.
Hanelt P. 1990. Taxonomy, evolution and history. In: Rabinowitch HD,
Brewster JL. eds. Onions and allied crops, Vol. 1. Boca Raton, FL:
CRC Press, 1– 26.
Hanelt P. 1992. Ovule number and seed weight in the genus Allium L. In:
Hanelt P, Hammer K, Knüpffer H. eds. The genus Allium: taxonomic problems and genetic resources. Proceedings of an international symposium
held at Gatersleben, Germany, 11–13 June 1991. Institut für
Pflanzengenetik und Kulturpflanzenforschung, Gatersleben, Germany,
99–105.
Hanelt P, Fritsch RM. 1994. Notes on some infrageneric taxa in Allium L.
Kew Bulletin 49: 559–564.
Hanelt P, Fritsch RM, Kruse J, Maass H, Ohle H, Pistrick K. 1989. Allium
L. sect. Porphyroprason Ekberg—Merkmale und systematische Stellung.
Flora, Morphologie, Geobotanik, Oekophysiologie 182: 69–86.
Hanelt P, Schulze-Motel J, Fritsch RM, et al. 1992. Infrageneric grouping of
Allium—the Gatersleben approach. In: Hanelt P, Hammer K, Knú´pffer H.
eds. The genus Allium: taxonomic problems and genetic resources.
Proceedings of an international symposium held at Gatersleben,
Germany, 11–13 June 1991. Institut für Pflanzengenetik und
Kulturpflanzenforschung, Gatersleben, Germany, 107–123.
Harris AJ, Xiang QY. 2009. Estimating ancestral distributions of lineages
with uncertain sister groups: a statistical approach to dispersal-vicariance
analysis and a case using Aesculus L. (Sapindaceae) including fossils.
Journal of Systematics and Evolution 47: 349– 368.
He XJ. 1999. Studies on evolutionary biology of the genus Allium L. in China.
PhD thesis, Sichuan University, Chengdu.
He XJ, Ge S, Xu JM, Hong DY. 2000. Phylogeny of Chinese Allium
(Liliaceae) using PCR-RFLP analysis. Science in China (series C) 43:
454– 463.
Hirschegger P, Jakše J, Trontelj P, Bohanec B. 2010. Origins of Allium
ampeloprasum horticultural groups and a molecular phylogeny of the
section Allium (Allium: Alliaceae). Molecular Phylogenetics and
Evolution 54: 488– 497.
Hörandl E, Paun O, Johansson JT, et al. 2005. Phylogenetic relationships
and evolutionary traits in Ranunculus s. l. (Ranunculaceae) inferred
from ITS sequence analysis. Molecular Phylogenetics and Evolution
36: 305 –327.
Huang RF, Xu JM, Yu H. 1995. A study on karyotypes and their evolutionary
trends in Allium Sect. Bromatorrhiza Ekberg (Liliaceae). Cathaya 7:
133– 145.
Hultén F. 1933. Studies on the origin and distribution of the flora in the Kurile
Island. Botaniska Notiser 1930: 325–343.
Inda LA, Segarra-Moragues JG, Mú´ller J, Peterson PM, Catalán P. 2008.
Dated historical biogeography of the temperate Loliinae (Poaceae,
Pooideae) grasses in the northern and southern hemispheres. Molecular
Phylogenetics and Evolution 46: 932–957.
Ingram AL, Doyle JJ. 2003. The origin and evolution of Eragrostis tef
(Poaceae) and related polyploids: evidence from nuclear waxy and
plastid rps16. American Journal of Botany 90: 116– 122.
Janssen T, Bremer K. 2004. The age of major monocot groups inferred from
800 +rbcL sequences. Botanical Journal of the Linnean Society 146:
385– 398.
Downloaded from http://aob.oxfordjournals.org/ by guest on June 20, 2013
hybridization with randomly amplified DNA probes. Theoretical and
Applied Genetics 95: 1223–1228.
Farris JS, Källersjö M, Kluge AG, Bult C. 1994. Testing significance of
incongruence. Cladistics 10: 315–319.
Fay MF, Chase MW. 1996. Resurrection of Themidaceae for the Brodiaea
alliance, and recircumscription of Alliaceae, Amaryllidaceae and
Agapanthoideae. Taxon 45: 441– 451.
Fay MF, Rudall PJ, Sullivan S, et al. 2000. Phylogenetic studies of
Asparagales based on four plastid DNA loci. In: Wilson KL, Morrison
DA. eds. Monocots – systematics and evolution, Vol. 1. Melbourne:
CSIRO, 360– 371.
Friesen [“Frizen”] N. 1988. Lukovye Sibiri: sistematika, kariologija,
khorologija. Novosibirsk, Russia: Nauka–Sibirskoe Otd., 185.
Friesen N. 1992. Systematics of the Siberian polyploid complex in subgenus
Rhizirideum (Allium). In: Hanelt P, Hammer K, Knüpffer H. eds. The
genus Allium: taxonomic problems and genetic resources. Proceedings
of an international symposium held at Gatersleben, Germany, 11– 13
June 1991. Institut für Pflanzengenetik und Kulturpflanzenforschung,
Gatersleben, Germany, 55– 66.
Friesen N. 1995. The genus Allium L. in the flora of Mongolia. Feddes
Repertorium – Journal of Botanical Taxonomy and Geobotany 106:
1–2, 59–81.
Friesen N, Klaas M. 1998. Origin of some minor vegetatively propagated
Allium crops studied with RAPD and GISH. Genetic Resources and
Crop Evolution 45: 511– 523.
Friesen N [“Frizen NV”], Zuev VV, Aljanskaja NS. 1986. Krasivoluk nereidocvetnyj —Caloscordum neriniflorum Herbert. In: Sobolevskaja KA.
ed. Biologicheskie osobennosti rastenij sibiri, nuzhdajushhikhsja v
okhrane. Novosibirsk, Russia: Nauka–Sibirskoe Otd., 83– 92.
Friesen N, Pollner S, Bachmann K, Blattner FR. 1999. RAPDs and noncoding chloroplast DNA reveal a single origin of the cultivated Allium fistulosum from A. altaicum (Alliaceae). American Journal of Botany 86:
554–562.
Friesen N, Fritsch RM, Pollner S, Blattner FR. 2000. Molecular and morphological evidence for an origin of the aberrant genus Milula within
Himalayan species of Allium (Alliaceae). Molecular Phylogenetics and
Evolution 17: 209 –218.
Friesen N, Fritsch RM, Blattner FR. 2006. Phylogeny and new intrageneric
classification of Allium (Alliaceae) based on nuclear ribosomal DNA ITS
sequences. Aliso 22: 372–395.
Fritsch RM. 1988. Anatomische Untersuchungen an der Blattspreite bei
Allium L. (Alliaceae)—I. Arten mit einer einfachen Leitbündelreihe.
Flora, Morphologie, Geobotanik, Oekophysiologie 181: 83– 100.
Fritsch RM. 1990. Bericht über Sammelreisen in Tadzhikistan (1983–1988)
zum Studium von mittelasiatischen Vertretern der Gattung Allium I.
Kulturpflanze 38: 363– 385.
Fritsch RM. 1992a. Zur Wurzelanatomie in der Gattung Allium
L. (Alliaceae). Beiträge zur Biologie der Pflanzen 67: 129 –160.
Fritsch RM. 1992b. Septal nectaries in the genus Allium L. In: Hanelt P,
Hammer K, Knüpffer H. eds. The genus Allium: taxonomic problems
and genetic resources. Proceedings of an international symposium held
at Gatersleben, Germany, 11–13 June 1991. Institut für Pflanzengenetik
und Kulturpflanzenforschung, Gatersleben, Germany, 77–85.
Fritsch RM. 1993. Anatomische Merkmale des Blütenschaftes in der Gattung
Allium L. und ihre systematische Bedeutung. Botanische Jahrbücher für
Systematik 115: 97–131.
Fritsch RM. 2001. Taxonomy of the genus Allium: contribution from IPK
Gatersleben. Herbertia 56: 19– 50.
Fritsch RM. 2009. New Allium (Alliaceae) species from Tajikistan,
Kyrgyzstan, and Uzbekistan. Botanische Jahrbücher für Systematik
127: 459– 471.
Fritsch RM, Astanova SB. 1998. Uniform karyotypes in different sections of
Allium L. subgenus Melanocrommyum (Webb & Berth.) Rouy from
Central Asia. Feddes Repertorium – Journal of Botanical Taxonomy
and Geobotany 109: 539–549.
Fritsch RM, Friesen N. 2002. Evolution, domestication and taxonomy. In:
Rabinowitch HD, Currah L. eds. Allium crop science: recent advances.
Wallingford, UK: CABI Publishing, 5– 30.
Fritsch RM, Friesen N. 2009. Allium oreotadzhikorum and A. vallivanchense,
two new species of Allium subg. Polyprason (Alliaceae) from the Central
Asian republic Tajikistan. Feddes Repertorium – Journal of Botanical
Taxonomy and Geobotany 20: 321–331.
Li et al. — Phylogeny and biogeography of Allium
Mitsui Y, Chen ST, Zhou ZK, Peng CI, Deng YF, Setoguchi H. 2008.
Phylogeny and biogeography of the genus Ainsliaea (Asteraceae) in the
Sino-Japanese region based on nuclear rDNA and plastid DNA sequence
data. Annals of Botany 101: 111–124.
Nguyen NH, Driscoll HE, Specht CD. 2008. A molecular phylogeny of the
wild onions (Allium; Alliaceae) with a focus on the western North
American center of diversity. Molecular Phylogenetics and Evolution
47: 1157–1172.
Noda S, Kawano S. 1988. The biology of Allium monanthum (Liliaceae),
Vol. 1. Polyploid complex and variations in karyotype. Plant Species
Biology 3: 13– 26.
Nylander JAA. 2004. MrModeltest, version 2.2. Program distributed by the
author. Uppsala: Evolutionary Biology Centre, Uppsala University,
(http://www.abc.se/ ≏nylander/).
Nylander JAA, Olsson U, Alström P, Sanmartı́n I. 2008. Accounting for
phylogenetic uncertainty in biogeography: a Bayesian approach to dispersal–vicariance analysis of the thrushes (Aves: Turdus). Systematic
Biology 57: 257–268.
Ohri D, Fritsch RM, Hanelt P. 1998. Evolution of genome size in Allium
(Alliaceae). Plant Systematics and Evolution 210: 57– 86.
Oxelman B, Liden M, Berglund D. 1997. Chloroplast rpsl6 intron phylogeny
of the tribe Sileneae (Caryophyllaceae). Plant Systematics and Evolution
206: 393 –410.
Pastor J, Valdes B. 1985. Bulb structure in some species of Allium (Liliaceae)
of Iberian Peninsula. Annales Musei Goulandris 7: 249– 261.
Pistrick K. 1992. Phenological variability in the genus Allium L. In: Hanelt P,
Hammer K, Knüpffer H. eds. The genus Allium: taxonomic problems and
genetic resources. Proceedings of an international symposium held at
Gatersleben, Germany, June 11– 13, 1991. Institut für Pflanzengenetik
und Kulturpflanzenforschung, Gatersleben, Germany, 243– 249.
Ree RH, Smith SA. 2008. Maximum likelihood inference of geographic range
evolution by dispersal, local extinction, and cladogenesis. Systematic
Biology 57: 4– 14.
Ree RH, Moore BR, Webb CO, Donoghue MJ. 2005. A likelihood framework for inferring the evolution of geographic range of phylogenetic
trees. Evolution 59: 2299– 2311.
Reeves G, Chase MV, Goldblatt P, et al. 2001. Molecular systematics of
Iridaceae: evidence from four plastid DNA regions. American Journal
of Botany 88: 2074–2087.
Regel E. 1875. Alliorum adhuc cognitorum monographia. Acta Horti
Petropolitani 3: 1 –266.
Regel E. 1887. Allii species Asiae Centralis in Asia Media a Turcomania
desertisque Araliensibus et Caspicis usque ad Mongolian crescentes.
Acta Horti Petropolitani 10: 278–362.
Ryzhova NN, Kholda OA, Kochieva EZ. 2009. Structure characteristics of
the chloroplast rpS16 intron in Allium sativum and related Allium
species. Molecular Biology 43: 828–837.
Ricroch A, Yockteng R, Brown SC, Nadot S. 2005. Evolution of genome
size across some cultivated Allium species. Genome 48: 511–520.
Ronquist F. 1996. DIVA, version 1.1. Computer program and manual available
by anonymous FTP from Uppsala University (http://www.ebc.uu.se/
systzoo/research/diva/diva.html).
Ronquist F. 1997. Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology 46: 195– 203.
Ronquist F. 2001. DIVA, version 1.2. Computer program for MacOS and
Win32. Evolutionary Biology Centre, Uppsala University (http://www.
ebc.uu.se/systzoo/research/diva/diva.html).
Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.
Samoylov A, Klaas H, Hanelt P. 1995. Use of chloroplast polymorphisms for
the phylogenetic study of subgenera Amerallium and Bromatorrhiza
(genus Allium). Feddes Repertorium – Journal of Botanical Taxonomy
and Geobotany 106: 161–167.
Samoylov A, Friesen N, Pollner S, Hanelt P. 1999. Use of chloroplast polymorphisms for the phylogenetic study of Allium subgenera Amerallium
and Bromatorrhiza (Alliaceae) II. Feddes Repertorium – Journal of
Botanical Taxonomy and Geobotany 110: 103–109.
Sanmartı́n I. 2003. Dispersal vs. vicariance in the Mediterranean:
historical biogeography of the Palearctic Pachydeminae (Coleoptera,
Scarabaeoidea). Journal of Biogeography 30: 1883–1897.
Sanmartı́n I, Van Der Mark P, Ronquist F. 2008. Inferring dispersal: a
Bayesian approach to phylogeny-based island biogeography, with
Downloaded from http://aob.oxfordjournals.org/ by guest on June 20, 2013
Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ. 1998.
Multiple sequence alignment with Clustal X. Trends in Biochemical
Sciences 23: 403– 405.
Jing WC, Xu JM, Yang L. 1999. A study on cytotaxonomy of Sect.
Anguinum of Allium. Acta Phytotaxonomica Sinica 37: 20– 34.
Kamelin RV. 1973. Florogeneticheskij analiz estestvennoj flory gornoj
Srednej Azii. Leningrad: Nauka, 354.
Kamenetsky R. 1992. Morphological types and root systems as indicators of
evolutionary pathways in the genus Allium. In: Hanelt P, Hammer K,
Knüpffer H. eds. The genus Allium: taxonomic problems and genetic
resources. Proceedings of an international symposium held at
Gatersleben, Germany, 11–13 June 1991. Institut für Pflanzengenetik
und Kulturpflanzenforschung, Gatersleben, Germany, 129–135.
Kawano S, Nagai Y, Hayashi K. 2005. Life-history monographs of Japanese
plants. 3: Allium monanthum Maxim. (Alliaceae). Plant Species Biology
20: 155 –165.
Khassanov FO. 1997. Conspectus of the wild growing Allium species of
Middle Asia. In: Öztürk M, Secmen Ö, Görk G. eds. Plant life in
Southwest and Central Asia. Izmir, Turkey: Ege University Press,
141– 159.
Khassanov FO, Fritsch RM. 1994. New taxa in Allium L. subgen.
Melanocrommyum (Webb & Berth.) Rouy from Central Asia. Linzer
Biologische Beiträge 26: 965–990.
Klaas M, Friesen N. 2002. Molecular markers in Allium. In: Rabinowitch HD,
Currah L. eds. Allium crop science: recent advances. Wallingford, UK:
CABI Publishing, 159– 185.
Kovtonyuk NK, Barkalov VJu, Friesen N. 2009. Synopsis of the family
Alliaceae Borkh. (onions) of Asian parts of Russia. Turczaninowia 12:
31–39.
Kruse J. 1984. Rasterelektronenmikroskopische Untersuchungen an Samen
der Gattung Allium L. Kulturpflanze 32: 89– 101.
Kruse J. 1988. Rasterelektronenmikroskopische Untersuchungen an Samen
der Gattung Allium L. III. Kulturpflanze 36: 355–368.
Kruse J. 1992a. Growth form characters and their variation in Allium L. In:
Hanelt P, Hammer K, Knüpffer H. eds. The genus Allium: taxonomic problems and genetic resources. Proceedings of an international symposium
held at Gatersleben, Germany, 11–13 June 1991. Institut für
Pflanzengenetik und Kulturpflanzenforschung, Gatersleben, Germany,
173– 179.
Kruse J. 1992b. Variability of testa sculptures in the genus Allium L. In:
Hanelt P, Hammer K, Knüpffer H. eds. The genus Allium: taxonomic problems and genetic resources. Proceedings of an international symposium
held at Gatersleben, Germany, 11–13 June 1991. Institut fú´r
Pflanzengenetik und Kulturpflanzenforschung, Gatersleben, Germany,
181– 182.
Lindley J. 1836. Genus Nectaroscordum Lindl. Edwards’s Botanical Register
9: 1913.
Linnaeus C. 1753. Species plantarum, Vol. 1. Allium. Stockholm: Laurentiis
Salvii [Facsimile edition, 1957– 1959, London: Ray Society], 294–302.
Linne von Berg G, Samoylov A, Klaas M, Hanelt P. 1996. Chloroplast DNA
restriction analysis and the infrageneric grouping of Allium (Alliaceae).
Plant Systematics and Evolution 200: 253–261.
Maass HI. 1992. Electrophoretic study of storage proteins in the genus Allium
L. In: Hanelt P, Hammer K, Knüpffer H. eds. The genus Allium: taxonomic problems and genetic resources. Proceedings of an international
symposium held at Gatersleben, Germany, 11–13 June 1991. Institut
für Pflanzengenetik und Kulturpflanzenforschung, Gatersleben,
Germany, 183– 189.
Marazzi B, Endress PK, De Queiroz LP, Conti E. 2006. Phylogenetic
relationships within Senna (Leguminosae, Cassiinae) based on three
chloroplast DNA regions: patterns in the evolution of flora symmetry
and extrafloral nectarines. American Journal of Botany 93: 288– 303.
Mathew B. 1996. A review of Allium section Allium. Kew: Royal Botanic
Gardens, 176.
Mathew B, Baytop T. 1984. The bulbous plants of Turkey. London:
B. T. Batsford Ltd.
Mes THM, Friesen N, Fritsch RM, Klaas M, Bachmann K. 1997. Criteria
for sampling in Allium based on chloroplast DNA PCR-RFLPs.
Systematic Botany 22: 701 –712.
Mes THM, Fritsch RM, Pollner S, Bachmann K. 1999. Evolution of the
chloroplast genome and polymorphic ITS regions in Allium subgenus
Melanocrommyum. Genome 42: 237–247.
727
728
Li et al. — Phylogeny and biogeography of Allium
APP E ND IX 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
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special reference to the Canary Islands. Journal of Biogeography 35:
428–449.
Sinitsyna TA, Friesen N. 2008. Phylogeny of section Rhizirideum G.Don.f. ex
W.D.J.Koch of genus Allium L. on the base of molecular data. Problems
of botany of South Siberia and Mongolia. Barnaul: Azbuka Press,
323–326.
Stearn WT. 1955. Allium bulgaricum. Botanical Magazine. 170: plate 257
and text.
Stearn WT. 1978. European species of Allium and allied genera of Alliaceae:
a synonymic enumeration. Annales Musei Goulandris 4: 83– 198.
Stearn WT. 1980. Allium L. In: Tutin TG, Heywood VH, Burges NA, et al
eds. Flora Europaea, Vol. 5. Cambridge: Cambridge University Press,
49– 69.
Swofford DL. 2003. PAUP*: Phylogenetic Analysis Using Parsimony (*and
other methods), version 4.0b10. Sunderland, MA: Sinauer Associates.
Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular
Evolutionary Genetics Analysis (MEGA) software version 4.0.
Molecular Biology and Evolution 24: 1596– 1599.
Tiffney BH. 1985. The Eocene North Atlantic land bridge: its importance in
tertiary and modern phytogeography of the Northern Hemisphere.
Journal of the Arnold Arboretum 66: 243–273.
Traub HP. 1968. The subgenera, sections and subsections of Allium L. Plant
Life 24: 147–163.
Traub HP. 1972. Genus Allium L. — subgenera, sections and subsections.
Plant Life 28: 132–137.
Velazco PM, Patterson BD. 2008. Phylogenetics and biogeography of the
broad-nosed bats, genus Platyrrhinus (Chiroptera: Phyllostomidae).
Molecular Phylogenetics and Evolution 49: 479–459.
Vvedensky AI. 1935. Rod 267. Luk— Allium L. In: Komarov VL. ed. Flora
URSS, Vol. 4. Leningrad: Izd. Akad. Nauk SSSR, 112–280.
White TJ, Bruns TD, Lee SB, Taylor J. 1990. Amplification and direct
sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis
MA, Gelfand DH, Sninsky JJ. eds. PCR protocols: a guide to methods
and applications. New York: Academic Press, 315– 321.
Xiang QY, Thomas DT. 2008. Tracking character evolution and biogeographic history through time in Cornaceae—does choice of methods
matter? Journal of Systematics and Evolution 46: 349–374.
Xu JM. 1980. Allium L. In: Wang FZ, Tang J. eds. Flora Reipublicae
Popularis Sinicae, Vol. 14. Beijing: Science Press, 170– 272.
Xu JM, Kamelin RV. 2000. Allium L. In: Wu ZY, Raven PH. eds. Flora of
China, Vol. 24. Beijing: Science Press; St. Louis: Missouri Botanical
Garden Press, 165–202.
Xu JM, Yang L, He XJ. 1998. A study on karyotype differentiation of Allium
fasciculatum (Liliaceae). Acta Phytotaxonomica Sinica 36: 346– 352.
Yu Y, Harris AJ, He XJ. 2010. S-DIVA (statistical dispersal-vicariance
analysis): a tool for inferring biogeographic histories. Molecular
Phylogenetics and Evolution doi: 10.1016/j.ympev.2010.04.011.
Zhou SD, He XJ, Yu Y, Xu JM. 2007. Karyotype studies on twenty-one
populations of eight species in Allium section Rhiziridium. Acta
Phytotaxonomica Sinica 45: 207–216.
Li et al. — Phylogeny and biogeography of Allium
APPENDIX 2
Previously published ITS and rps16 accessions obtained from
GenBank
ITS accessions of Allium and outgroups obtained from
GenBank. 1Dubouzet and Shinoda (1998); 2Dubouzet and
Shinoda (1999); 3Friesen et al. (2000); 4Ricroch et al.
(2005); 5Friesen et al. (2006); 6Gurushidze et al. (2007);
7
Gurushidze et al. (2008); 8Nguyen et al. (2008); 9Sinitsyna
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;
5
A. austrosibiricum N.Friesen AJ411832 ; A. azutavicum
Kotukhov
AM9496009,
A.
backhousianum
Regel
7
FM177264 ;
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;
7
A. cardiostemon Fisch. & C.A.Mey. FM177277 ; A. caspium
subsp. baissunense FM1772677; A. caspium (Pall.) M.Bieb.
subsp. caspium FM1772807; A. cepa L. AM4183706;
A.
cernuum
Roth
AF0376221,
A.
chamaemoly
2
L. AF055109 ; 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;
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& 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.
729
730
Li et al. — Phylogeny and biogeography of Allium
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;
2
A. subhirsutum L. AF055106 ; 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;
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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,
7
A. komarowii Lipsky FM177342 ; 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;
8
A. lemmonii S.Watson EU096164 ; 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;
5
A. melanantherum Pancic AJ412739 ; 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;
5
A. neriniflorum (Herb.) G.Don AJ411920 ; 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;
Li et al. — Phylogeny and biogeography of Allium
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.
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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
10
Umehara et al. (unpublished); 11Ryzhova et al. (2009).
Allium: A. ampeloprasum FJ65370011; A. cepa
L. AB29230010; A. obliquum FJ65367111; A. sativum
FJ65368811; A. schoenoprasum FJ65370511.
731
732
Li et al. — Phylogeny and biogeography of Allium
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?
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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.
Li et al. — Phylogeny and biogeography of Allium
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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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?
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