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Origin of the Rapa endemic genus Apostates: Revisiting major disjunctions and evolutionary conservatism in the Bahia alliance (Compositae: Bahieae)

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Abstract Molecular phylogenetic analyses of nuclear and chloroplast DNA sequences indicate that the rediscovered Apostates, known only from Rapa in the Austral Islands of southeastern Polynesia, represents an example of extreme long-distance dispersal (> 6500 km) from southwestern North America and one of at least four disjunctions of comparable magnitude in the primarily New World Bahia alliance (tribe Bahieae). Each of the disjunctions appears to have resulted from north-to-south dispersal since the mid-Miocene; three are associated with such marked morphological and ecological change that some of the southern taxa (including Apostates) have been treated in distinct genera of uncertain relationship. Phyllotaxy within the Bahia alliance, however, evidently has been even more conservative evolutionarily than reflected by previous taxonomies, with alternate-leaved and opposite-leaved clades in Bahia sensu Ellison each encompassing representatives of other genera that share the same leaf arrangements. A revised taxonomic treatment of the Bahia alliance is proposed to recognize morphologically distinctive, monophyletic genera, including the critically endangered Apostates.
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Baldwin & Wood • Systematics and biogeography of the Bahia alliance
106 4 Version of Record
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65 (5) • October 2016: 1064 1080
 
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   
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      
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         
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     
   
    
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   
   
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    


 
 
    

   
    


Apostates
Pacifigeron
and Metatrophis                 

  
 Miocalles 

Origin of the Rapa endemic genus Apostates: Revisiting major
disjunctions and evolutionary conservatism in the Bahia alliance
(Compositae: Bahieae)
Bruce G. Baldwin & Kenneth R. Wood
1 Jepson Herbarium and Department of Integrative Biology, University of California, Berkeley, California 94720, U.S.A.
2 National Tropical Botanical Garden, Kalaheo, Hawaii 96741, U.S.A.
 Bruce G. Baldwin, bbaldwin@berkeley.edu
ORCID 
DOI  655
Abstract
Apostates
         
 
 Bahia    

 Apostates
Bahia                                                
Bahia                 
   Bahia
Apostates
Keywords
 

Supplementary Material



Baldwin & Wood • Systematics and biogeography of the Bahia alliance
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
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Corokia
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 
 

    



          

Apostates
   
A.M. Stokes 186
  
Olearia  O. rapae
   Olearia
       
O. rapaeOlearia
O. rapaeOlearia
  O. rapae 
 Apostates
 
  
   
Apostates

 
    
Apostates




Apostates 

     Apostates on a


 

           

  ndhFtrnK 
rpl16 psbAtrnH Apostates
      

Apostates      
   

Apostates
Apostates
Fig. .Apostates rapae(lef t), 
(right).
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Fig. .BahiaA, Bahia neomexicana (= Picradeniopsis multif lora
B, Bahia absinthifolia (= Picradeniopsis absinthifoliaC, Bahia
ambrosioidesD,Apostates rapaeE, Apostates rapae  
F, Hymenothrix wrightiiG, Amauriopsis dissecta (= Hymenothrix dissecta
H, Palafoxia arida
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MATERIALS AND METHODS
Taxon sampling. —
  

Apostates rapae col
Wood &
  
Bahia  Bahia 
  
Bahia



Apostates
The families and genera of vascular plants
   
AchyropappusAmauriopsis  ApostatesBahia
  Cephalobembix   Picradeniopsis
Florestina Holoschkuhria
Hymenothrix  Nothoschkuhria Palafoxia
 PlatyschkuhriaSchkuhria
   Chaetymenia
   
  Bahia 
Picradeniopsis 
B. pringlei
B. neomexicana      
in Schkuhria   S. multiflora   
Amauriopsis Bahia 
A. janakosana
Achyropappus 
A. depauperatus 
ApostatesHoloschkuhriaNothoschkuhria
and Platy schkuhriaHymenothrix
H. greenmanii      
Schkuhria
S. greenmaniiHymenothrix greenmanii
Florestina
 Palafoxia    



DNA extraction and sequencing. —

   




    

     


      
     
     
   
     


         
   
ndhFndhF-ycf1 inter
 
   trnK intron and 5 
matK
rpl16     
psbAtrnH   


 

   



   

    

   

Analyses of phylogeny, biogeography, and morphological
character evolution. —


         

 

   
    


 




Bahia pedata   





matKndhFrbcL    
 

Amauriopsis dissectaBahia
absinthifoliaChaetymenia peduncularis 
Florestina pedata Palafoxia arida       
 Peucephyllum schottii
Dimeresia howellii  Chaenactis
douglasii   C. santolinoides
Baldwin & Wood • Systematics and biogeography of the Bahia alliance
1068 Version of Record
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65 (5) • October 2016: 1064 1080

Bahia
    Bahia al
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  
   
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      
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    
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 
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    
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Schkuhria
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    
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    
   

    

     
  
Barnedesia
Dasyphyllum


      



    





   

  
  
     
  
         
     
        
 

Bahia     
 


Bahia

     
  



 
Bahia    


RESULTS
Phylogenetic resolution, congruence, and incongruence.
Bahia

   


Baldwin & Wood • Systematics and biogeography of the Bahia alliance
Version of Record
TAX ON
65 (5) • October 2016: 1064 1080
     

  Amauriopsis Hymenothrix  Platy-
schkuhria

    
  
Bahia
matKndhFrbcL 

Bahia 

   
   
Schkuhria 
 S. degenericaNothoschkuhria
C. pedunculata B978
S. wislizeni B974
S. schkuhrioides nx3/cPOP-150
S. wrightii K19020
S. pinnata nx2/cx3
Ac. anthemoides K15420
Ac. queretarensis S8344
B. ambrosioides C4574
Ho. tetramera nx2/cC3654
N. degenerica B7991
Apostates rapae x2
B. woodhousei nx2/cH8652
B. absinthifolia x2
B. oppositifolia H3153
B. neomexicana nx3/cH23490
B. bigelovii nx3/cP6384ind2
B. xylopoda nx3/cN28852
N32946
(B. schaffneri nHB6388/c-)
F. platyphylla K15532
F. tripteris B970
Pa. arida B784
Pa. texana B969
Pl. integrifolia nx2/cx1
Am. autumnalis x2
Am. biternata x2
Am. glandulosa A326
Hy. loomisii / wrightii
Hy. wislizeni x2
Am. dissecta x2
Am. dissecta I122
Hy. palmeri x2
(Am. pedata n-/cS438)
Chaetymenia (outgroup) Chaetymenia (outgroup)
Schkuhria
Schkuhria
Achyropappus
Achyropappus
Bahia Bahia
Holoschkuhria Holoschkuhria
Nothoschkuhria Nothoschkuhria
Apostates Apostates
Picradeniopsis
Picradeniopsis
Florestina
Florestina
Palafoxia
Palafoxia
Platyschkuhria
Platyschkuhria
Hymenothrix
Hymenothrix
1.00/100
1.00/84
1.00/100
1.00/100
1.00/67
1.00/95
1.00/98
1.00/99
1.00/100
1.00/100 1.00/100
1.00/100
1.00/100
0.97/80
1.00/100
1.00/100
1.00/100
1.00/99
1.00/100
1.00/100
1.00
1.00
1.00/87
1.00/100
0.99/95
1.00/100
1.00/100
1.00/95
1.00/99
1.00/100
1.00/100
1.00/92
0.99/90
1.00
1/100
0.98/93
1.00/98
1.00/96 1.00/100
1.00/100
1.00/100
1.00/98 1.00/100
1.00/100
1.00/99
97
100
97
1
1
2
2
3
3
4
4
a
b
c
a
b
c
1.00/100
Fig. .                (lef t) (right) Bahia       



 Ac AchyropappusAm Amauriopsis B. Bahia C.ChaetymeniaF. Florestina Ho. HoloschkuhriaHy.
Hymenothrix NNothoschkuhria Pa. Palafoxia Pl. PlatyschkuhriaS.Schkuhria.      

Baldwin & Wood • Systematics and biogeography of the Bahia alliance
 Version of Record
TAX ON
65 (5) • October 2016: 1064 1080
degenericaS. multiflora (= Bahia
neomexicanaAchyropappus  Bahia am-
brosioides HoloschkuhriaApostates
Bahia
B. neomexicanaNothoschkuhriaAmauriopsis
FlorestinaHymeno-
thrix  Palafoxia   
Platyschkuhria
      
   Flores-
tinaPalafoxia (c) AmauriopsisHymenothrix 
PlatyschkuhriaBahia
B. neomexicana   
 Bahia
absinthifolia   B. oppositifolia
   B. bigelovii    B. neomexi-
canaB. schaffneri
B. xylopoda  Schkuhria


S. pinnata 
S. wrightii
can S. wislizeni S. schkuhrioides   
      


BahiaB. neomexi-
canaApostatesAmauriopsis dissecta
Hymenothrix palmeri
   

  
  Achyropappus Bahia ambrosi-
oides Holoschkuhria 
B. ambrosioidesHoloschkuhria
AchyropappusB. ambrosioides
Fig. .Bahia

  Bahia
4
AcAchyropappusAmAmauriopsis B. BahiaC.Chaetymenia
F. Florestina Ho. HoloschkuhriaHy. Hymenothrix N.Nothoschkuhria Pa. Palafoxia Pl. Platyschkuhria S.Schkuhria. 
                                       

051 01 52 02 53 0
Apostates rapae (2)
B. xylopoda (2)
Pl. integrifolia B938(cl1)
Ac. anthemoides K15420
B. neomexicana F5658
S. wrightii K19020
B. absinthifolia S10714
B. schaffneri HB6388
Hy. loomisii/wrightii (1/1)
B. woodhousei (2)
Pa. arida B784
F. tripteris B970
C. peduncularis B978
Ho. tetramera C3654
Am. biternata VD93-789
Ho. tetramera O90733
B. absinthifolia B967
Pl. integrifolia B938(cl2)
Hy. palmeri RG97-1158
S. pinnata C103-03
B. bigelovii P6384(2 ind)
Am. biternata D1037
S. schkuhrioides (3)
Hy. palmeri S2722
N. degenerica B7991
Ac. queretarensis S8344
Am. autumnalis V7972
Pa. texana B969
Am. autumnalis V6604
B. oppositifolia H3153
B. neomexicana (2)
B. ambrosioides C4574
Am. dissecta (2)
F. platyphylla K15532
S. pinnata C111-07
Hy. wislizeni SJB s.n.
B. bigelovii P6384(1 ind)
S. wislizeni B974
Am. dissecta I122
Am. glandulosa A326
B. xylopoda GP1452
Hy. wislizeni C1517
Alternate leaves
Alternate leaves
(Opposite leaves)
1/100
1/100
1/100
0.98/93
1/100
1/100 1/99
1/100
*1/97
1/100
1/100
1/87
0.99/95
1/100
1/100
1/95
1/100
1/99
*1/92
1/100
-/71
0.99/90
*1/98
1/96
0.89/-
1/100
1/98
1/100
1/100
-/53
1/99
-/-
0.93/66
1/100
1/100
1/100
-/-
-/-
South America
North America
Rapa
Biogeography
(clade color):
:
Head type
(taxon label color):
Radiate heads
Discoid heads
Ma
1/96
Baldwin & Wood • Systematics and biogeography of the Bahia alliance
Version of Record
TAX ON
65 (5) • October 2016: 1064 1080
Florestina Palafoxia      Amauriopsis
HymenopappusPlatyschkuhria
Florestina Palafoxia
Palafoxia AmauriopsisHymenothrixPlatyschkuhria
Bahia bigeloviiB. neomexicana
B. xylopodaB. bigelovii
B. xylopodaB. schaffneri
B. neomexicanaB. bigelovii
B. neomexicanaB. xylopoda
Biogeographic model tests and estimates. —

     Bahia   
    
     



 


   


Morphological evolution. —

     

  
AmauriopsisHymenothrixPlatyschkuhria and once on
Nothoschkuhria 
  
Palafoxia


   Bahia alliance

   
  
Palafoxia
DISCUSSION
Apostates belongs t o the Bahia alliance. —
Apos-
tates         
Apostates
      

        

 
Apostates
 Apostates  
Bahia
 
     Schkuhria
Bahia      
Bahia Apostates 


Bahia       
 B. neomexicana  Notho schkuhria
  Bahia 
BahiaB. ambrosioides  
Achyropappus
 Holoschkuhria    
  Bahia
BahiaAmauriopsis
FlorestinaHymenothrix
PalafoxiaPlatyschkuhria
Apostates represents long-distance dispersal from North
America. — Apostates


Hypericophyllum   Apos-
tates


Apostates
  Apostates
 


   
Apostates   
 

ApostatesBahia alliance cannot
 

Tubulifloridites lilliei  



Other major disjunctions in the Bahia alliance. —
 
 Apostates   
Tab le . 



  L     
    
    
    
    
    
    
    
    
Baldwin & Wood • Systematics and biogeography of the Bahia alliance
Version of Record
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65 (5) • October 2016: 1064 1080
   Bahia Apostates 
Bahia

     
  Apostates and
HoloschkuhriaBahia




Apostates

Bahia
   
    
           
Apostates
  Holoschkuhria
     

Nothoschkuhria   
Bahia neomexicana 
Bahia ambrosioidesHoloschkuhria 

   



Bahia ambrosioides and Holoschkuhria   


   
Bahia ambrosioides


     
Holoschkuhria (H. tetramera


Bahia

 


B. ambrosioidesAchyropap-
pus
Achyropappus
B. ambrosioidesHoloschkuhria
  
in B. neomexicana (= Schkuhria multiflora


  




Schkuhria
        
  

Bahia al
Nothoschkuhria
   
Bahia
B. neomexicana and Apostates  
     

Comparable biogeographic patterns in the southern Poly-
nesian flora. —
  

Apostates  

  


Fitchia
Oparanthus

Narvalina Selleophytum

Petrobium


      

FitchiaOparanthus   




       
     
  Bahia  Plantago

P. rapensis P. rupicola   
   
P. macrocarpa


     

   
   
 
     
 Metrosideros
   Pittosporum


Plantago  
  Nesoluma


Baldwin & Wood • Systematics and biogeography of the Bahia alliance
Version of Record
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65 (5) • October 2016: 1064 1080
  Melicope
 
2014) and Santalum



Intrinsic and extrinsic dispersal factors. —
  Apos-
tates     
Bahia


 
     

 
    
     
 Bahia  
 Amauriopsis (= Bahia 
        

Apostates

 



   
    

Apostates
    
 
 
   


      
  Phyllanthus

 Epicephala 

Evolutionary conservatism in the Bahia alliance? —

Bahia


      

acter in Bahia
Amauriopsis

 
         Ba-
hia    
Amauriopsis (= Bahia
  Hymenothrix and
Platy schkuhria    Bahia
B. neomexicana (= Schkuhria mul-
tifloraApostates

Bahia


Nothoschkuhria     Amauri-
opsisHymenothrixPlatyschkuhria
   
  
  
Bahia

     Bahia
Apostates   
 Hymenothrix Palafoxia 
AchyropappusAmauriopsisPlatyschkuhria
Schkuhria.
Amauriopsis
 
Bahia 
Achyropappus and Platyschkuhria   
BahiaB. neo-
mexicana  Bahia
Schkuhria S. multiflora


Schkuhria
Taxonomic treatment. —

Bahia
  Florestina and
Palafoxia        
    
 
Platyschkuhria

AmauriopsisHymenothrixNotho-
schkuhriaSchkuhria degenerica  

Schkuhria 
Amauriopsis (= Bahia
 Hymenothrix  
  
   
  Amauriopsis and Hymenothrix    
Bahia alliance

 

Hymenothrix
   Bahia   Apostates
BahiaPic-
radeniopsisNothoschkuhriaAchyropappusB. am-
brosioidesHoloschkuhria

Hymenothrix
Baldwin & Wood • Systematics and biogeography of the Bahia alliance
 Version of Record
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65 (5) • October 2016: 1064 1080
 
Bahia (B. ambrosioides

Apostates
     
Picradeniopsis
Cephalobembixx B. bigeloviiB. neo-
mexicanaB. pringlei
B. xylopoda B. schaffneriB. xylopoda
Picradeniopsis x B. absinthifoliaB. oppositi-
foliaB. woodhousei
to Apostates      
B. woodhousei  
 B. absinthifolia B. oppositifolia 
B. woodhouseiPicradeniop-
sisP. oppositi foliaBahia oppositi-
folia) and P. woodhouseiBahia woodhousei)
x
Achyropappus
ApostatesBahia
Holoschkuhria
Key to genera of the Bahia alliance
  2
  4
 
 Nothoschkuhria
 


 
 Platyschkuhria
 

 Hymenothrix
   
         
 5
 


 6
          

 Florestina
 

 Palafoxia
 

 
 Schkuhria
  



 
 8
 
     

 
 Apostates


 
Holoschkuhria
    
 Achyropappus
 

 10
  
 Bahia
    
 Picradeniopsis
New combinations for the proposed taxonomic changes
Hymenothrix autumnaliscomb.
nov.Bahia autumnalis 
Amauriopsis autumnalis
        

M.C . Johnston & J. Crutchfield 5856
    

Hymenothrix biternata c omb . nov.
Bahia biternata
 Schkuhria biternata
 
Eriophyllum biternatum
Villanova biternata
Amaur -
iopsis biternata
 
C. Wright 1256 (GH


       

Hymenothrix dissecta  comb. nov.
Amauria? dissecta    
  Villanova chrysanthemoides

V. dissectaBahia
chrysanthemoides
 Bahia dissecta
      
Eriophyllum chrysanthemoides
Villanova dis-
secta  
Amauriopsis dissecta

Baldwin & Wood • Systematics and biogeography of the Bahia alliance
Version of Record
TAX ON
65 (5) • October 2016: 1064 1080
 
A. Fendler 537

= Bahia dissecta anisopappa
  
        
   I.L. Wiggins &
D. Demaree 4870 

      
Hymenothrix glandulopubescens  
comb. nov.Hymenopappus glandulopubescens
  
Waterfall
12576
  

= Bahia glandulosa
Hymenothrix glandulosa
Amauriopsis glan-
dulosa
2010 – Lectotype, designated here 
     
      
 E. Palmer 492





       
(E. Palmer 492
C.G. Pringle 308Bahia
glandulosa



   

Palmer 492
Hymenothrix janakosanacomb.
nov.Amauriopsis janakosana
    
                      
F. Chiang, T. Wendt & M.C. John-
ston 9665
Hymenothrix pedata   comb. nov.
Bahia pedata
  Schkuhria pedata   
Eriophyl-
lum pedatum  
Amauriopsis pedata

       
C. Wright 387 (GH

 

Picradeniopsis absinthifolia  comb.
nov. Bahia absinthifolia
Eriophyllum absinthifolium
      
Ha rt weg 128 


= Bahia dealbata
Bahia absinthifolia   deal
-
bata
  Picradeniopsis dealbata
   
Lecto type (designated here): 
Dr. Gregg s.n. (GH


  Hart weg 128 
    Bahia absinthifolia

     Hartweg 128 
B. de-
albata

   




Picradeniopsis bigelovii   com b. nov.
Bahia bigelovii 
Schkuhria bigelovii
      Eriophyllum
bigelovii   
 
 Bigelow s.n.          

Picradeniopsis multiflora
comb. nov.Schkuhria multiflora  
Achyropappus
schkuhrioides 
Achyropappus schkuhrioides
Bahia gil-
liesii
Bahia multiflora       

Gillies 147    

= Schkuhria neomexicana
Neo-MexicanaAm-
blyopappus neomexicanus
Baldwin & Wood • Systematics and biogeography of the Bahia alliance
 Version of Record
TAX ON
65 (5) • October 2016: 1064 1080
Bahia neomexicana
    
   Achyropappus neomexicanus    
Cephalobembix
neomexicana

  A. Fendler 458 (GH
    
      
= Schkuhria pusilla
 Rothia pusilla
Schkuhria multif lorapusilla  

d’Orbigny 1403
= Rothia intermedia
Lectotype (designated here):
O. Kuntze s.n.

= Schkuhria pusilla aristata 
Schkuhria multi-
flora   aristata    

R.E. Fries 812b


= Schkuhria pusilla   longipedicellata 
   longepedicellata 

 Bodenbender s.n. 

Rothia intermedia  


Picradeniopsis pringleicomb. nov.
Bahia pringlei

C.G. Pringle
6407       

        

   

   
 

      
      

Picradeniopsis schaffneri  comb.
nov.Bahia schaffneri

     C.G. Pringle
3028
Picradeniopsis schaffneriaristata 
co mb. nov. Bahia aristata
Bahia schaffneriaristata

  
 C.G. Pringle 5127 (GH barcode

Picradeniopsis xylopoda   com b. n ov.
Bahia xylopoda
   
  C.G. Pringle 6931

  

   
    



   
 
      
  

= Bahia ehrenbergii
Ehrenberg
362
Extreme endangerment of Apostates. — 
Apostates
rapae
     
     

       

 
A. rapae 
    
Myoporum rapense     Scaevola taccada  
tuamotuensis Eugenia reinwardtiana   
and Osteomeles anthyllidifolia 
Dianella intermedia punctata    Portulaca
lutea and Lycium sandwicense 
 Cyperus javanicus Chrysopogon
aciculatus Ischaemum stokesii 
Asplenium obtusatum  and Polystichum
rapense 
A. rapae
    
     
 
Psidium cattleianum Miscanthus florid-
ulus, Scirpus nodosus  Sporobolus
elongatus  and Eleusine indica 
  A. rapae  
Baldwin & Wood • Systematics and biogeography of the Bahia alliance
Version of Record
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65 (5) • October 2016: 1064 1080
   



   
A. rapae 

A. rapae

     
    
 
       
 



Apostates 



Apos-
tates

A. rapae 

   

     
 
ACKNOWLEDGMENTS
   
     Apostates
rapae      
    
      
     


            
   
                   
    


      

    
              
  
   
             


Appelhans, M.S., Wen, J, Wood, K.R., Allan G.J., Zimmer, E.A. &
Wagner, W.L.    
MelicopePlatydesma and Zanthoxylum
Bot. J. Linn. Soc. 
       
Baker, H.G. Evolution 21:

Baldwin, B.G.   Nothoschkuhria   
 Schkuhria degenerica  Phytoneuron

Baldwin, B.G. & Markos, S. 
 
Calycadenia   Molec. Phylogen. Evol.

Baldwin, B.G. & Wagner, W.L.   
Ann. Bot. (Oxford) 

Baldwin, B.G. & Wessa, B.L.  
 Amer. J.
Bot. 
Baldwin, B.G., Crawford, D.J., Francisco-Ortega, J., Kim, S.-C.,
Sang, T. & Stuessy, T.F. 

Molecular systematics
of plants. II. DNA sequencing      

Baldwin, B.G., Wessa, B.L. & Panero, J.L.   

Syst. Bot.
Barreda , V.D., Palazzesi, L ., Teller ia, M.C., Olivero, E .B., Raine, J.I .
& Forest, F.     
Proc. Natl. Acad. Sci. U.S.A.
          
Barreda, V.D., Palazzesi, L., Tellaría, M.C., Olivero, E.B., Raine,
J.I. & Forest F. 
Proc. Natl.
Acad. Sci. U.S.A.

Birch, J.L., Keeley, S.C. & Morden C.W. 
Astelia      
 Molec.
Phylogen. Evol.
    
Brown, F.B.H.  Flora of southeastern Polynesia. III. Dicot yle-
dons   

Carlquist, S.      
Evolution

Carlquist, S.   Island biology 

Cooke, C.M., Jr.



 

56
in:
    Report of the Director for 1934   
          
Crawford, D.J., Lowrey, T.K., Anderson, G.J., Barnardello, G.,
Santos- Guerra, A. & Stuessy, T.F.        


   Systematics, evolution, and biogeography of Composi-
tae
Cross, E.W., Quinn, C.J. & Wagstaff, S.J. 
OleariaPl. Syst. Evol.
 
Dierschke, T., Mandáková, T., Lysak, M.A. & Mummenhoff, K.

LITERATURE CITED
Baldwin & Wood • Systematics and biogeography of the Bahia alliance
 Version of Record
TAX ON
65 (5) • October 2016: 1064 1080
Lepidium
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Molec.
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 Proc. Natl.
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
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  Rhodora
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tonia 
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
Bahia   Amer. J. Bot.
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PhytoKeys
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