1
Electronic supplementary material
Yusa et al. Adaptive evolution of sexual systems in pedunculate barnacles.
Table S1. Sexual systems (H = hermaphroditism; A = androdioecy; D = dioecy),
proportions of solitary individuals and sources of ecological data and 18S rDNA
sequences in pedunculate barnacles used
Suborder
Family
Genus
Species
Iblomorpha
Iblomorpha
Lepadomorpha
Lepadomorpha
Lepadomorpha
Lepadomorpha
Lepadomorpha
Lepadomorpha
Lepadomorpha
Lepadomorpha
Heteralepadomorpha
Heteralepadomorpha
Heteralepadomorpha
Heteralepadomorpha
Heteralepadomorpha
Heteralepadomorpha
Iblidae
Iblidae
Lepadidae
Lepadidae
Lepadidae
Lepadidae
Lepadidae
Lepadidae
Lepadidae
Lepadidae
Koleolepadidae
Koleolepadidae
Heteralepadidae
Heteralepadidae
Heteralepadidae
Heteralepadidae
Ibla
Ibla
Conchoderma
Conchoderma
Conchoderma
Lepas
Lepas
Lepas
Lepas
Lepas
Koleolepas
Koleolepas
Paralepas
Paralepas
Heteralepas
Paralepas
cumingi
quadrivalvis
auritum
virgatum
hunteri
anatifera
anserifera
australis
testudinata
pectinata
Heteralepadomorpha Heteralepadidae Heteralepas
U89493
AY520655
EU082401
AB551725
AB551724
L26516
EU082404
EU082405
EU082406
EU082403
AB551735
AB551734
AB551733
AF057561
AB551732
EU082399
Reference
for
sequence
1
4
5
this study
this study
7
5
5
5
5
this study
this study
this study
13
this study
5
AB551731
this study
AB551726
AB551729
AB551728
AB551727
EU082407
AB551730
L26518
EU082412
AB551723
EU082389
AB551719
AB551722
EU082388
this study
this study
this study
this study
5
this study
7
5
this study
5
this study
this study
25
this study
Sexual Proportion
Accession
Reference
system solitary
no.
D
A
H
H
H
H
H
H
H
H
sp.
D
avis
A
xenophorae A
palinuri
H
quadrata
H
dannevigi
H
0.59
1.00
0.00
0.01
0.17
0.00
0.02
0.00
0.00
0.00
1.00
0.20
0.25
0.25
0.01
1.00
japonica
H
0.00
this study
2, 3
this study
6
6
this study
this study
8
9
this study
this study
10
this study
11, 12
this study
3
14, 15; this
study
this study
16
17
this study
9
this study
this study
18
19, 20
19
20, 21
22
23
Lepadomorpha
Lepadomorpha
Lepadomorpha
Lepadomorpha
Lepadomorpha
Lepadomorpha
Lepadomorpha
Lepadomorpha
Scalpellomorpha
Scalpellomorpha
Scalpellomorpha
Scalpellomorpha
Scalpellomorpha
Poecilasmatidae
Poecilasmatidae
Poecilasmatidae
Poecilasmatidae
Poecilasmatidae
Poecilasmatidae
Poecilasmatidae
Oxynaspidae
Scalpellidae
Scalpellidae
Scalpellidae
Scalpellidae
Scalpellidae
Megalasma
Poecilasma
Octolasmis
Octolasmis
Octolasmis
Temnaspis
Octolasmis
Oxynaspis
Trianguloscalpellum
Trianguloscalpellum
Arcoscalpellum
Scalpellum
Scalpellum
striatum
kaempferi
warwickii
angulata
cor
amygdalum
lowei
celata
balanoides
regium
sociabile
stearnsii
scalpellum
A
H
A
H
H
H
H
H
H
D
H
D
A
1.00
0.00
0.22
0.00
0.00
0.00
0.00
0.00
0.20
1.00
0.03
0.69
0.20
Scalpellomorpha
Scalpellidae
Arcoscalpellum
sp.
A
0.80 this study
AB551720
Scalpellomorpha
Scalpellidae
Litoscalpellum
discoveryi
D
1.00 24, 25
EU489852
Scalpellomorpha
Scalpellidae
Arcoscalpellum
bouveti
D
1.00 24
EU489855
Scalpellomorpha
Scalpellomorpha
Scalpellomorpha
Scalpellomorpha
Scalpellomorpha
Scalpellomorpha
Scalpellomorpha
Scalpellomorpha
Scalpellomorpha
Scalpellomorpha
Scalpellomorpha
Scalpellomorpha
Scalpellomorpha
Scalpellomorpha
Calanticidae
Calanticidae
Calanticidae
Scalpellidae
Pollicipedidae
Amigdoscalpellum
Ornatoscalpellum
Neolepas
Neolepas
Leucolepas
Ashinkailepas
Vulcanolepas
Pollicipes
Pollicipes
Calantica
Calantica
Calantica
Smilium
Lithotrya
Capitulum
sp.
Scalpellidae
Eolepadidae
Eolepadidae
Eolepadidae
Eolepadidae
Eolepadidae
Pollicipedidae
Pollicipedidae
D
D
H
H
H
H
H
H
H
D
A
A
A
H
H
1.00
0.29
0.00
0.00
0.00
0.00
0.00
0.00
0.00
1.00
0.25
1.00
0.14
0.00
0.00
AB551718
AB551721
EU082391
EU082390
EU082392
EU082395
EU082394
AY520651
AY520650
AB551717
EU082384
L26513
EU082386
EU082382
AY520652
stroemii
zevinae
rapanuii
longa
seepiophila
osheai
polymerus
pollicipes
sp.
spinosa
villosa
peronii
valentiana
mitella
this study
this study
26
27
28
29
30
3
2, 9
this study
18
2, 3
2
2, 11
this study
Linse et al.
unpublished
Linse et al.
unpublished
this study
this study
5
5
5
5
5
4
4
this study
5
7
5
5
4
2
1. Mizrahi, L., Achituv, Y., Katcoff, D. J. & Perl-Treves, R. 1998 Phylogenetic position
of Ibla (Cirripedia: Thoracica) based on 18S rDNA sequence analysis. J. Crust. Biol.
18, 363-368.
2. Darwin, C. 1851 A monograph on the sub-class Cirripedia. I. The Lepadidae.
London: Ray Society.
3. Broch, H. 1922 Paper from Dr. Th. Mortensen’s Pacific Expedition 1914–16. X.
Studies on Pacific cirripeds. Vedensk Heddel Dansk Naturleist, Foren Kobenhavn 73,
215-358.
4. Pérez-Losada, M., Høeg, J.T. & Crandall, K. A. 2004 Unraveling the evolutionary
radiation of the Thoracican barnacles using molecular and morphological evidence:
A comparison of several divergence time estimation approaches. Syst. Biol. 53, 244264. (doi: 10.1080/10635150490423458)
5. Pérez-Losada, M., Harp, M., Høeg, J. T., Achituv, Y., Jones, D., Watanabe, H. &
Crandall, K. A. 2008 The tempo and mode of barnacle evolution. Mol. Phylogenet.
Evol. 46, 328-346. (doi: 10.1016/j.ympev.2007.10.004)
6. Yamato, S., Yusa, Y. & Tanase, H. 1996 Distribution of two species of Conchoderma
(Cirripedia: Thoracica) over the body of a sea snake, Laticauda semifasciata
(Reinwardt), from the Kii Peninsula, southwestern Japan. Publ. Seto Mar. Biol. Lab.
37, 337-343.
7. Spears, T., Abele, L. G. & Applegate, M. A. 1994 Phylogenetic study of cirripedes
and selected relatives (Thecostraca) based on 18S rDNA sequence analysis. J. Crust.
Biol. 14, 641-656.
8. Utinomi, H. 1968 Pelagic, shelf and shallow-water Cirripedia from the IndoWestpacific. Videnskabelige Meddelelser Fra Dansk Naturhistorisk Forening 131,
161-186.
9. Chan, B. K. K., Prabowo, R. E. & Lee, K-S. 2009 Crustacean fauna of Taiwan:
Barnacles, volume I – Cirripedia: Thoracica excluding the Pyrgomatidae and
Acastinae. Keelung, Taiwan: National Taiwan Ocean University.
10. Yusa, Y., Yamato, S. & Marumura, M. 2001 Ecology of a parasitic barnacle,
Koleolepas avis: relationship to the hosts, distribution, left-right asymmetry and
reproduction. J. Mar. Biol. Assoc. U. K. 81, 781-788. (doi:
10.1017/S0025315401004593)
11. Barnard, K. H. 1924 Contributions to the crustacean fauna of South Africa. 7.
Cirripedia. Annals South African Mus. 20, 1-103, 1 plate.
12. Newman, W. A. 1960 Five pedunculate cirripeds from the Western Pacific,
including two new forms. Crustaceana 1, 100-116.
3
13. Perl-Treves, L., Mizrahi, D. J., Katcoff, D. J. & Achituv, Y. 2000 Elucidation of the
phylogenetic relationships of three thecostracans, Verruca, Paralepas, and
Dendrogaster based on 18S rDNA sequences. J. Crust. Biol. 20, 385-392.
14. Hiro, F. 1933 Report on the Cirripedia collected by the surveying ships of the
Imperial Fisheries Experimental Station on the continental shelf bordering Japan.
Rec. Oceanogr. Works Japan 5, 11-84, 3 plates.
15. Hiro, F. 1938 Notes on the animals found on Macrocheira kaempferi de Haan. I.
Cirripeds, II. Molluscs. Annot. Zool. Japon 17, 465-476.
16. Williams, R. & Moyse, J. 1988 Occurrence, distribution, and orientation of
Poecilasma kaempferi Darwin (Cirripedia: Pedunculata) epizoic on Neolithodes
grimaldi Milne-Edwards and Bouvier (Decapoda: Anomura) in the northeast
Atlantic. J. Crust. Biol. 8, 177-186.
17. Yusa, Y., Takemura, M., Miyazaki, K., Watanabe, T. & Yamato, S. 2010 Dwarf
males of Octolasmis warwickii (Cirripedia: Thoracica): The first example of
coexistence of males and hermaphrodites in the suborder Lepadomorpha. Biol. Bull.
218, 259-265.
18. Foster, B. A. 1978 The marine fauna of New Zealand: Barnacles (Cirripedia:
Thoracica). Mem. N. Z. Oceanogr. Inst. 69, 1-160.
19. Hoek, P. P. C. 1883 Report on the Cirripedia collected by H.M.S. Challenger during
the years 1873-1876. In Report on the scientific results of the voyage of H.M.S.
Challenger during the years 1873-1876, zoology (eds. C. W. Thomson & J. Murray),
pp. 1-169, 13 plates. London: John Murray, London.
20. Nilsson-Cantell, C. A. 1931 Cirripeds from the Indian Ocean and Malay
Archipelargo in the British Museum (Nat. Hist.), London. Arkiv Zoologi 23A, 1-12.
21. Klepal, W. 1990 The fundamentals of insemination in cirripedes. Oceanogr. Mar.
Biol. Annu. Rev. 28, 353-379.
22. Nilsson-Cantell, C. A. 1934 Cirripeds from the Malay Archipelago in the Zoological
Museum of Amsterdam. Zoologische Mededeelingen 13, 31-33.
23. Gomez, E. D. 1975 Sex determination in Balanus (Conopea) galeatus (L.)
(Cirripedia Thoracica). Crustaceana 28, 105-107.
24. Nilsson-Cantell, C. A. 1939 Thoracic cirripedes collected in 1925–1936.‘Discovery’
Reports 18, 223-238.
25. Newman, W. A. & Ross, A. 1971 Antarctic Cirripedia. Washington: American
Geophysical Union.
26. Newman, W. A. 1979 A new scalpellid (Cirripedia); a Mesozoic relic living near an
abyssal hydrothermal spring. Trans. San Diego Soc. Nat. Hist. 19, 153-167.
4
27. Jones, D. S. 1993 A New Neolepas (Cirripedia: Thoracica: Scalpellidae) from an
abyssal hydrothermal vent, southeast Pacific. Bull. Mar. Sci. 52, 937-948.
28. Tunnicliffe, V. & Southward, A. J. 2004 Growth and breeding of a primitive stalked
barnacle Leucolepas longa (Cirripedia: Scalpellomorpha: Eolepadidae:
Neolepadinae) inhabiting a volcanic seamount off Papua New Guinea. J. Mar. Biol.
Assoc. U. K. 84, 121-132. (doi: 10.1017/S0025315404008987h)
29. Yamaguchi, T., Newman, W. A. & Hashimoto, J. 2004 A cold seep barnacle
(Cirripedia: Neolepadinae) from Japan and the age of the vent/seep fauna. J. Mar.
Biol. Assoc. U. K. 84, 111-120. (doi: 10.1017/S0025315404008975h)
30. Buckeridge, J. S. 2000 Neolepas osheai sp. nov., a new deep-sea vent barnacle
(Cirripedia: Pedunculata) from the Brothers Caldera, south-west Pacific Ocean. New
Zealand. J. Mar. Fresh. Res. 34, 409-418. (doi: 10.1080/00288330.2000.9516944)
5
68
65
63
100
54
74
72
55
100
100
91
94
56
100
77
88
100
73
99
60
51
55
86
53
88
100 63
67
88
76
98
99
D Ibla cumingi
A Ibla quadrivalvis
D Trianguloscalpellum regium
H Arcoscalpellum sociabile
A Arcoscalpellum sp.
D Scalpellum stearnsii
A Scalpellum scalpellum
H Trianguloscalpellum balanoides
A Megalasma striatum
H Poecilasma kaempferi
A Octolasmis warwickii
H Octolasmis angulata
H Octolasmis cor
H Temnaspis amygdalum
H Octolasmis lowei
H Oxynaspis celata
H Conchoderma auritum
H Conchoderma virgatum
H Conchoderma hunteri
H Lepas pectinata
H Lepas anatifera
H Lepas anserifera
H Lepas australis
H Lepas testudinata
A Paralepas xenophorae
D Koleolepas sp.
A Koleolepas avis
H Paralepas palinuri
H Heteralepas quadrata
H Paralepas dannevigi
H Heteralepas japonica
D Ornatoscalpellum stroemii
D Amigdoscalpellum sp.
D Litoscalpellum discoveryi
D Arcoscalpellum beuveti
H Leucolepas longa
H Neolepas zevinae
H Neolepas rapanuii
H Ashinkailepas seepiophila
H Vulcanolepas osheai
H Lithotrya valentiana
H Capitulum mitella
H Pollicipes polymerus
H Pollicipes pollicipes
D Calantica sp.
A Smilium peronii
A Calantica spinosa
A Calantica villosa
Iblomorpha
Scalpellomorpha
Lepadomorpha
Heteralepadomorpha
Scalpellomorpha
Figure S1. Sexual system placed on the maximum likelihood phylogenetic tree of
pedunculate barnacles assuming the GTR+I+G model of evolution. Bootstrap
proportions (only values higher than 50%) are shown in the tree. Ibla cumingi and I.
quadrivalvis were used as outgroups. H: hermaphroditic, A: androdioecious (males +
hermaphrodites), D: dioecious (males + females).
6
q12 = 0
1. Hermaphroditism
(0, 0)
q13 = 43.7
q31 = 140.6
2. Gynodioecy
(0, 1)
q21 = 3.7
q24 = 657.6
q42 = 0
q34 = 409.9
3. Androdioecy
(1, 0)
q43 = 453.4
4. Dioecy
(1, 1)
Figure S2. Evolutionary transition rates between sexual systems in pedunculate
barnacles estimated by maximum likelihood. qij refers to the transition rate from the ith
to the jth sexual system, averaged over 100 randomly-resolved maximum likelihood
trees. In parentheses, the presence (1) or absence (0) of dwarf males (left) and of
females (right) is shown.