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Sub-Paratethyan origin and Middle to Late Miocene principal diversification of the Lactucinae (Cichorieae, Compositae) inferred from molecular phylogenetics, divergence-dating and biogeographic analysis

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The Lactucinae or Lactuca alliance include approximately 200 species distributed across the Northern Hemisphere and Africa. They were not recognised as a separate lineage until the late 20th century and their circumscription is still not fully settled. The generic classification of no other group of the Cichorieae has faced as many controversies as the Lactuca alliance and competing taxonomies coexist. This paper provides the first molecular phylogeny of the subtribe on a global scale as a major step towards its revised systematics. The sampling includes almost 60% of the species-level diversity and spans all species groups. Two datasets were created, one including the nrDNA ITS region, the other five concatenated non-coding plastid DNA loci. Maximum parsimony, maximum likelihood and Bayesian inference were used to produce a robust phylogenetic backbone. The diversification and expansion of the Lactucinae in a geohistorical context was reconstructed by estimating the age of their lineages using relaxed molecular clock dating and by inferring the ancestral areas using Bayesian binary analysis. The redelimited monophyletic Lactucinae are composed of seven lineages that also include Prenanthes, which is confirmed to have a single species, P. purpurea. The positions of two further lineages shift between Lactucinae and Crepidinae in the nuclear and plastid DNA phylogenies. Incongruence between the phylogenies suggests events of ancient reticulation or incomplete lineage sorting in the formation of these latter two lineages and in two of the seven other Lactucinae lineages. The phyloge- netic results show a dilemma for Lactucinae systematics: most generic concepts proposed to date are highly artificial but the resolved phylogenetic lineages do not constitute practicable taxonomic entities with our current knowledge. Diversification of the subtribe is inferred to have taken place since the Middle Miocene. Biogeographic analysis proposes that the clade originated in the mountains of the landmass mediating between the European and Asian continents and delimited in the south by the Tethys Sea and in the north by the Paratethys Sea. Several independent migrations have occurred into various parts of Asia, Europe, tropical Africa and North America.
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66 (3) • June 2017: 675703 Kilian & al. • Diversification of the Lactucinae (Compositae)
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INTRODUCTION
 


     Lactuca
sativa   Cichorium endivia Cichorium
intybus         Lactuca L. and
Sub-Paratethyan origin and Middle to Late Miocene principal
diversification of the Lactucinae (Compositae: Cichorieae)
inferred from molecular phylogenetics, divergence-dating and
biogeographic analysis
Norbert Kilian,1* Alexander Sennikov,2 Ze-Huan Wang,3 Birgit Gemeinholzer4 & Jian-Wen Zhang3
1 Botanic Garden and Botanical Museum Berlin, Freie Universität Berlin, Königin-Luise-Str. 6–8, 14195 Berlin, Germany
2 Botanical Museum, Finnish Museum of Natural History, P.O. Box 7, 00014 University of Helsinki, Finland; and Herbarium,
Komarov Botanical Institute of Russian Academy of Sciences, Prof. Popov str. 2, 197376 St. Petersburg, Russia
3 Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences,
Kunming 650201, Yunnan, People’s Republic of China
4 AG Spezielle Botanik, Justus-Liebig-Universität Giessen, Heinrich-Buff-Ring 38, 35392 Giessen, Germany
 
 Norbert Kilian, n.kilian@bgbm.org
ORCID 
DOI 
Abstract
Lactuca 
  
 Lactuca


           
    


Prenanthes 
   P. purpurea
   




  


Keywords
Lactuca 
Supplementary Material


Cichorium
    

    




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66 (3) • June 2017: 675703Kilian & al. • Diversification of the Lactucinae (Compositae)
Lactuca


 Lactuca 
  
 

Lactuca



LactucaSonchus L. and
HieraciumCrepis

 

    







  





 
 

 

 



  


  
Faberia 



Faberia   



   
 Lactuca alliance.
 Lactuca
 

 
Cicerbita 

   Cicerbita

 


 






      


  
  


CicerbitaLactucaMelanoserisNotoseris
and Paraprenanthes 
Prenanthes pur-
purea L. and Faberia 


Prenanthes purpurea

  


  
  



 




     




  
Lactuca


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66 (3) • June 2017: 675703 Kilian & al. • Diversification of the Lactucinae (Compositae)
   
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 
  


  

 

Prenanthes purpurea 

   




MATERIALS AND METHODS
Plant material and sampling. —

 




 

   
     
   



1


116




   


Scorzonera
hispanica  

  



DNA isolation, amplification and sequencing. —

  




petB-petD
petD 

psbA-trnH 
trnL()-trnF

rpl32-trnL
()
 
rps16-trnQ()

       
      
  




Sequence alignment and coding of length mutational
events. —
petDpetD  petB-petD
         
   
  
 Version of Record
TAX ON
66 (3) • June 2017: 675703Kilian & al. • Diversification of the Lactucinae (Compositae)

Lactuca sativa
& al. (2007).
      


    











      
 petDpsbA-trnHtrnL

-trnF
rpl32-trnL and 5rps16-t rnQ 





 






  
 
  

Phylogenetic reconstruction. —  
.




    
      

 
  


  

    
 
 


  
    
 
   
 

 

   


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   




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66 (3) • June 2017: 675703 Kilian & al. • Diversification of the Lactucinae (Compositae)


 
  
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  
   

Prenanthes purpurea   





 


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
 




Divergence time estimation. —











 

     
Cichorium intybus
        


Scorzonera hispida 

 



   


   




    


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
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


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

    
 
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
Prenanthes purpurea
 
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
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




Biogeography and ancestral area estimation. —
 
      















 



  


 

 Version of Record
TAX ON
66 (3) • June 2017: 675703Kilian & al. • Diversification of the Lactucinae (Compositae)
RES U LTS
Phylogenetic analyses. —    





 

  

Nuclear ribosomal DNA phylogeny. —


  

 

Prenanthes abietina 


  

Prenanthes purpurea
  

  

 
Prenanthes purpurea
Lactuca triquetra 
   

Faberia
Cicerbita
Kovalevskiella
Cicerbita
Notoseris
Paraprenanthes
   Lactuca
 Melanoseris

Prenanthes
purpurea
72





Prenanthes
purpurea

e

 
Plastid DNA phylogeny. —
 



)
Prenanthes purpurea   




Prenanthes abietina
 Lactuca triquetraFaberia


Prenanthes purpureaCicerbita
 
Notoseris-
Paraprenanthes

KovalevskiellaCicerbita


Lactuca-Melanoseris 
 Notoseris-Paraprenanthes
Lactuca-Melanoseris 


Incongruences between nuclear and plastid DNA phylog-
eny.
  
  
  
 










Tab le . 
Prenanthes purpurea 
P. purpurea
e






e

1 
2 
3 
4 
   133.24
Version of Record
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66 (3) • June 2017: 675703 Kilian & al. • Diversification of the Lactucinae (Compositae)
Fig. A–C.




) 






Prenanthes abietina
Prenanthes purpureaLactuca
triquetraFaberiaCicerbita
KovalevskiellaNotoseris
ParaprenanthesLactuca
Melanoseris.
A
C
0.71
57.8
1 / 99
98.9
1 / 75
62.8
Paraprenanthes oligolepis
LAC 022
1 / 100
99.9
0.94 / 69
92.1
99.4
1 / 97
93.7
1 / 88
81.2
1 / 98
89.2
1 / 100
100
100
1 / 96
96.5
F
1 / 94
92.8
1 / 99
98.1
0.97 / 70
0.99 / 74
62.7
0.58
99.8
1 / 95
98.8
0.99 / 82
1 / 100
100
100
1 / 97
92.7
E
0.98 / 83
86.6
1 / 100
100
0.95
60.6
1 / 89
90.5
1 / 95
91.7
0.89
1 / 100
100
1 / 75
87.1
0.99 / 95
95.8
1 / 100
100
1 / 100
100
1
/
100
98.1
1 / 100
99.9
D
1
1 / 88
87.6
100
0.8 / 75
63
0.96 / 83
63.5
1 / 100
100
1 / 100
99.6
0.99 / 51
67.8
0.52
1 / 98
98.7
0.9
0.5
0.8
1 / 100
100
1 / 100
99.9
0.55 / 51
1 / 100
100
1 / 100
100
A
B
G
2
3
//
//
0.96
Notoseris henryi LAC 056
Notoseris henryi LAC 062
Notoseris macilenta LAC 064
Notoseris macilenta LAC 065
Notoseris macilenta LAC 143
Notoseris macilenta LAC 145
Notoseris khasiana LAC 066
Notoseris khasiana LAC 068
Notoseris triflora × khasiana LAC 151
Notoseris triflora LAC 059
Notoseris triflora LAC 061
Notoseris yakoensis LAC 054
Notoseris scandens LAC 052
Notoseris scandens LAC 147
Kovalevskiella rosea LAC 232
Kovalevskiella rosea LAC 233
Kovalevskiella kovalevskiana LAC 241
Kovalevskiella kovalevskiana LAC 207
Kovalevskiella zerawschanica LAC 270
Kovalevskiella zerawschanica LAC 239
Kovalevskiella zerawschanica LAC 238
Lactuca mira LAC 267
Chaetoseris roborowskii LAC 216
Chaetoseris roborowskii LAC 019
Chaetoseris roborowskii LAC 018
Chaetoseris roborowskii yellow LAC 222
Stenoseris auriculiformis LAC 016
Stenoseris auriculiformis LAC 017
Lactuca alaica LAC 268
Cicerbita azurea LAC 014
Cicerbita azurea LAC 015
Cephalorrhynchus microcephalus LAC 326
Cephalorrhynchus hispidus LAC 011
Cephalorrhynchus kirpicznikovii LAC 235
Cephalorrhynchus hispidus LAC 240
Cephalorrhynchus hispidus LAC 275
Cephalorrhynchus cypricus LAC 215
Cephalorrhynchus subplumosus LAC 226
Cephalorrhynchus hispidus LAC 214
Mycelis muralis LAC 138
Mycelis muralis LAC 139
Mycelis muralis LAC 274
Cicerbita petiolata LAC 271
Cicerbita petiolata LAC 136
Cicerbita pancicii LAC 272
Cicerbita pancicii LAC 273
Cicerbita alpina LAC 133
Cicerbita alpina LAC 012
Cicerbita alpina LAC 137
Faberia sinensis LAC 006
Faberia faberi LAC 010
Faberia nanchuanensis LAC 005
Lactuca triquetra LAC 278
Lactuca triquetra LAC 277
Lactuca triquetra LAC 276
Lactuca triquetra LAC 285
Lactuca triquetra LAC 286
Prenanthes purpurea HQ161931
Prenanthes purpurea LAC 141
Prenanthes purpurea LAC 142
Prenanthes purpurea LAC 013
Prenanthes abietina LAC 294
Leontodon tuberosus LAC 134
Hypochaeris radicata LAC 283
Hypochaeris maculata LAC 287
Hypochaeridinae
0.98 / 72
Hyoseridinae
Scorzonera hispanica LAC 296
Crepidinae
Soroseris erysimoides LAC 004
Soroseris glomerata LAC 297
LAC 300
Nabalus trifoliolatus LAC 288
Nabalus altissimus LAC 299
Nabalus sagittatus HQ161964
Dubyaea hispida LAC 298
Nabalus tatarinowii LAC 289
Sonchella dentata
Ixeris chinensis subsp. versicolor LAC 291
Crepis multicaulis LAC 003
Crepis sancta LAC 293
Lagoseriopsis popovii LAC 290
Youngia cineripappa LAC 292
Crepidiastrum tenuifolium LAC 295
Launaea sarmentosa
LAC 001
Reichardia dichotoma LAC 181
 Version of Record
TAX ON
66 (3) • June 2017: 675703Kilian & al. • Diversification of the Lactucinae (Compositae)
0.98 / 57
0.81 / 61
51.7
100
Lactuca paradoxa
LAC 198
1 / 96
89.7
0.99 / 70
66.2
1 / 85
52.4
0.98 / 82
55.5
1 / 95
68.2
0.8 / 75
67.9
1 / 99
100
0.81 / 88
84.4
100
1 / 100
100
100
1 / 100
100
99.9
0.79 / 67
53
1 / 100
99.3
1 / 100
100
100
0.56
100
1 / 99
99.6
1 / 99
97.8
0.98 / 72
68.9
1 / 100
100
0.95 / 72
63.4
0.94 / 65
63.5
0.92 / 70
52.7
99.9
1 / 88
94.1
1 / 98
99.4
0.7 / 84
62.5
100
1 / 97
95.1
1 / 100
100
1 / 100
100
0.96 / 81
1 / 100
100
0.51 / 78
1 / 87
86.8
1 / 100
99.9
1
100
1 / 100
100
1 / 100
99.3
99.6
1 / 98
94.8
1 / 97
88.9
1 / 84
88.4
1 / 95
92.1
1 / 98
98.1
1 / 98
97.8
1 / 99
99.6
1 / 99
98.5
0.61 / 98
0.99
77.2
0.54 / 82
0.98 / 98
82.1
1 / 100
100
99.9
1 / 99
0.91 / 87
1
Notoseris henryi
LAC 056
H
4
I
I1
I2
I3
I3a
I3b
I3c
I3d
I4
I5
I6
I7
I8
I9
B
Lactuca tuberosa
yellow LAC 178
Lactuca tuberosa LAC 179
Lactuca tuberosa LAC 118
Lactuca tuberosa LAC 180
Lactuca dissecta LAC 116
Lactuca dolichophylla LAC 117
Lactuca inermis LAC 119
Lactuca inermis LAC 177
Lactuca inermis LAC 176
Lactuca tenerrima
LAC 171
Lactuca ludoviciana LAC 153
Lactuca canadensis HQ161956
Lactuca hirsuta HQ172901
Lactuca graminifolia LAC 155
Lactuca biennis HQ161959
Lactuca floridana LAC 154
Cicerbita plumieri LAC 149
Cicerbita plumieri LAC 186
Lactuca perennis LAC 113
Lactuca perennis LAC 334
Lactuca intricata LAC 183
Lactuca intricata LAC 182
Lactuca undulata LAC 115
Lactuca undulata LAC 114
Lactuca glauciifolia LAC 184
Cephalorrhynchus picridiformis LAC 185
Cicerbita racemosa LAC 187
Cicerbita racemosa LAC 188
Cicerbita macrophylla LAC 189
Cicerbita macrophylla LAC 190
Lactuca virosa LAC 146
Lactuca virosa LAC 246
Lactuca georgica LAC 164
Lactuca sativa LAC 130
Lactuca serriola LAC 144
Lactuca serriola LAC 247
Lactuca serriola LAC 163
Lactuca saligna LAC 148
Lactuca saligna LAC 281
Lactuca quercina LAC 165
Lactuca tetrantha LAC 167
Lactuca alpestris LAC 168
Lactuca viminea LAC 127
Lactuca acanthifolia LAC 162
Lactuca orientalis LAC 126
Lactuca tatarica LAC 166
Lactuca tatarica LAC 248
Lactuca sibirica LAC 128
Lactuca indica LAC 169
Lactuca indica LAC 170
Lactuca indica LAC 121
Lactuca formosana LAC 122
Lactuca raddeana LAC 124
Lactuca glareosa LAC 196
Lactuca glareosa LAC 195
Lactuca oyukludaghensis LAC 191
Lactuca variabilis LAC 192
Lactuca variabilis LAC 265
Cicerbita deltoidea LAC 194
Lactuca aurea LAC 193
Paraprenanthes yunnanensis LAC 044
Paraprenanthes yunnanensis LAC 490
Paraprenanthes yunnanensis LAC 491
Paraprenanthes meridionalis LAC 036
Paraprenanthes prenanthoides LAC 035
Paraprenanthes sororia LAC 037
Paraprenanthes sororia LAC 038
Paraprenanthes diversifolia LAC 041
Paraprenanthes wilsonii LAC 049
Paraprenanthes wilsonii LAC 051
Paraprenanthes melanantha LAC 046
Paraprenanthes melanantha LAC 047
Paraprenanthes parishii LAC 028
Paraprenanthes parishii LAC 029
Paraprenanthes triflora LAC 025
Paraprenanthes triflora LAC 152
Paraprenanthes triflora LAC 266
Paraprenanthes oligolepis LAC 020
Paraprenanthes oligolepis LAC 022
Version of Record
TAX ON
66 (3) • June 2017: 675703 Kilian & al. • Diversification of the Lactucinae (Compositae)
   Prenanthes abietina   
 
Prenanthes purpurea


 Lactuca triquetra


  Lactuca

1 / 97
88.2
1 / 93
82
0.98 / 75
74.1
1 / 97
98.7
0.82 / 58
53.3
0.95 / 68
81.5
1 / 88
84
0.95 / 76
59.9
0.99 / 99
83.1
1
99.8
0.99 / 62
58.8
0.98 / 54
0.95 / 82
0.56 / 59
0.53 / 67
66.4
0.97 / 67
87.4
1 / 94
86.1
0.93 / 92
0.86 / 61
56.4
0.97
/
88
1 / 92
90.7
1 / 95
95.3
0.97 / 63
63.5
1 / 98
97.2
100
1 / 100
100
1 / 100
100
1 / 75
72.8
0.74 / 75
0.78 / 51
0.99 / 76
1 / 99
99.6
0.97 / 95
97.7
0.84 / 87
63.2
1 / 97
96.9
99.7
1 / 100
99.9
1 / 100
100
1 / 98
95.1
1 / 99
99.7
1 / 100
99.7
1 / 98
97
0.6 / 55
61.2
100
1 / 100
100
100
1 / 92
88.9
99.1
1 / 63
99.5
1 / 98
88.6
0.64 / 82
57.5
1 / 96
93.3
99.9
0.6 / 53
1 / 95
98.6
1
99.3
99.7
1 / 100
100
0.81 / 88
J
J1
J2
J2a
J2b
J2c
J2d
J2e
J2f
J2g
J3
C
Melanoseris graciliflora LAC 259
Melanoseris graciliflora LAC 250
Melanoseris graciliflora LAC 249
Melanoseris graciliflora LAC 112
Melanoseris tenuis LAC 237
Melanoseris tenuis LAC 107
Melanoseris tenuis LAC 106
Melanoseris atropurpurea LAC 101
Melanoseris atropurpurea LAC 099
Melanoseris likiangensis LAC 258
Melanoseris likiangensis LAC 098
Melanoseris macrantha LAC 075
Melanoseris monocephala LAC 231
Melanosris henryi LAC 280
Melanoseris violifolia LAC 076
Melanoseris violifolia LAC 077
Melanoseris violifolia LAC 254
Melanoseris macrorhiza LAC 253
Melanoseris macrorhiza LAC 073
Melanoseris macrorhiza LAC 074
Melanoseris lessertiana LAC 071
Prenanthes sumatrana LAC 279
Melanoseris aff. cyaneaLAC 257
Melanoseris cyanea LAC 089
Melanoseris cyanea LAC 084
Melanoseris cyanea LAC 080
Melanoseris aff. cyanea LAC 257
Melanoseris qinghaica LAC 078
Melanoseris decipiens LAC 256
Melanoseris brunoniana LAC 255
Melanoseris souliei
LAC 251
Melanoseris souliei LAC 252
Melanoseris souliei LAC 069
Melanoseris souliei LAC 070
Cephalorrhynchus brassicifolius LAC 225
Cephalorrhynchus brassicifolius LAC 227
Cephalorrhynchus brassicifolius LAC 218
Cephalorrhynchus polycladus LAC 219
Cephalorrhynchus polycladus LAC 282
Cephalorrhynchus polycladus LAC 213
Cephalorrhynchus takhtadzhianii LAC 234
Cephalorrhynchus soongoricus LAC 208
Cephalorrhynchus soongoricus LAC 211
Cephalorrhynchus soongoricus LAC 210
Cicerbita bourgaei LAC 260
Cicerbita bourgaei LAC 150
Cicerbita prenanthoides LAC 229
Cicerbita prenanthoides LAC 230
Lactuca rosularis LAC 199
Steptorhamphus pumilus LAC 261
Lactuca hazaranensis LAC 262
Melanoseris bracteata LAC 244
Melanoseris bracteata LAC 221
Melanoseris bracteata LAC 072
Cicerbita thianschanica LAC 263
Cicerbita thianschanica LAC 264
Cephalorrhynchus kossinskyi LAC 220
Cephalorrhynchus kossinskyi LAC 212
Cephalorrhynchus kossinskyi LAC 217
Cephalorrhynchus kossinskyi LAC 243
Steptorhamphus crassicaulis LAC 224
Steptorhamphus crassicaulis LAC 223
Steptorhamphus persicus LAC 284
Lactuca praecox T2 LAC 203
Lactuca praecox T3 LAC 204
Lactuca calophylla LAC 200
Lactuca schulzeana LAC 205
Lactuca ugandensis LAC 206
Lactuca setosa LAC 201
Lactuca lasiorhiza LAC 199
Lactuca praecox T1 LAC 202
Lactuca attenuata LAC 197
Lactuca paradoxa LAC 198
 Version of Record
TAX ON
66 (3) • June 2017: 675703Kilian & al. • Diversification of the Lactucinae (Compositae)
Fig. 2A– C. 
  

Prenanthes abietinaPrenanthes purpureaLactuca triquetraFaberiaCicerbitaKovalevskiellaNotoseris
ParaprenanthesLactucaMelanoseris.
3
0.53 / 52
0.92 / 74
53.1
1 / 96
95.8
1 / 100
100
1 / 100
99.9
74.1
Cicerbita azurea
LAC 015
Kovalevskiella kovalevskiana
LAC 207
1 / 100
99.6
1 / 100
95.7
1 / 92
83.1
1 / 74
89.6
0.98 / 88
63.7
1 / 92
93.2
0.99 / 69
1 / 99
87.1
0.99 / 68
57.6
0.96 / 67
67.5
1
/
100
99.6
1
/
100
99.7
1 / 100
100
1 / 100
100
1 / 99
100
1 / 100
100
1 / 100
99.9
0.97 / 70
63.5
1 / 100
100
1 / 92
98.1
1 / 100
100
0.98 / 83
80.1 1
/
100
99
1 / 80
63.6
1 / 100
98.7
1 / 94
71.6
Mycelis muralis
0.99 / 73
90.8
1 / 69
1 / 81
1
/
100
99.5
1 / 100
100
1 / 96
69.1
0.75
/
75
0.61 / 57
1 / 85
1 / 100
98.4
1 / 100
98.3
1 / 100
100
1 / 100
99.6
1 / 100
100
1 / 100
99.9
0.7 / 75
1 / 100
99.6
1 / 100
100
0.93 / 73
64
1 / 64
63.5
1 / 99
95.9
1 / 100
100
1 / 100
100
1 / 99
99.9
1 / 100
89.3
A
C
D
B
E
1
G/
H
2
3
1 / 62
63
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//
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//
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ANotoseris henryi LAC 056
Notoseris henryi LAC 062
Notoseris macilenta LAC 064
Notoseris macilenta LAC 065
Notoseris triflora LAC 059
Notoseris triflora LAC 061
Notoseris khasiana LAC 068
Notoseris khasiana LAC 066
Paraprenanthes meridionalis LAC 036
Paraprenanthes prenanthoides LAC 035
Paraprenanthes diversifolia LAC 041
Paraprenanthes wilsonii LAC 049
Paraprenanthes wilsonii LAC 051
Paraprenanthes yunnanensis LAC 044
Paraprenanthes yunnanensis NK172
Paraprenanthes sororia LAC 037
Paraprenanthes sororia LAC 038
Paraprenanthes melanantha LAC 046
Paraprenanthes melanantha LAC 047
Paraprenanthes parishii LAC 028
Paraprenanthes parishii LAC 030
Paraprenanthes oligolepis LAC 020
Paraprenanthes oligolepis LAC 022
Paraprenanthes triflora LAC 025
Paraprenanthes triflora LAC 266
Notoseris scandens LAC 147
Notoseris yakoensis LAC 054
Notoseris scandens LAC 052
Cephalorrhynchus kirpicznikovii LAC 235
Cephalorrhynchus microcephalus LAC 236
Cephalorrhynchus hispidus LAC 011
Cephalorrhynchus hispidus LAC 240
Cephalorrhynchus hispidus LAC 214
Cephalorrhynchus subplumosus
Cephalorrhynchus cypricus
LAC 274
LAC 226
LAC 215
Cicerbita alpina LAC 133
Cicerbita pancicii LAC 273
Cicerbita pancicii LAC 272
Cicerbita petiolata LAC 271
Cicerbita petiolata LAC 228
Prenanthes purpurea LAC 013
Prenanthes purpurea LAC 242
Nabalus trifoliolatus LAC 288
Nabalus tatarinowii LAC 289
Soroseris erysimoides LAC 004
Lagoseriopsis popovii LAC 290
Faberia sinensis LAC 006
Faberia faberi LAC 010
Faberia nanchuanensis LAC 005
Youngia cineripappa LAC 292
Crepidiastrum tenuifolium LAC 295
Ixeris chinensis subsp. versicolor LAC 291
Lactuca triquetra LAC 277
Lactuca triquetra LAC 276
Lactuca triquetra LAC 278
Lactuca triquetra LAC 285
Lactuca triquetra LAC 286
Prenanthes abietina LAC 294
Crepis multicaulis LAC 003
Crepis sancta LAC 293
Hypochaeris radicata LAC 283
Hypochaeris maculata LAC 287
Leontodon tuberosus LAC 002
Launaea sarmentosa LAC 001
Reichardia dichotoma LAC 181
Hypochaeridinae
Hyoseridinae
Scorzonera hispanica LAC 296
Crepidinae
Version of Record
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66 (3) • June 2017: 675703 Kilian & al. • Diversification of the Lactucinae (Compositae)
Melanoseris