2008-12-15 - Proceedings of the Royal Society B

Electronic Supplement:
In this Supplement we briefly review the remainder of the Chengjiang
deuterostomes. In comparison to the vetulicolians and yunnanozoans for the most part the
imterpretations of the other deuterostomes are somewhat less controversial.
A) First to the ambulacrarians. Perhaps surprisingly no bona-fide echinoderms are
known, although the appearance of this group certainly pre-dates the Chengjiang
Fossil-Lagerstätte. The vetulicystids, however, have been interpreted a pre-echinoderms
(Shu et al. 2004; Shu 2008), and intriguingly have again a bipartite body with a tail
(apparently segmented) and a globose anterior bearing at least three openings
(Supplementary Figure. 2a,b). These openings were interpreted as anterior mouth and
posterior anus, the latter flanked by a gill. These conclusions were treated with some
scepticism by Smith (2004; also Swalla & Smith 2008). Thus, he queried the identification
of the mouth, speculating it might be concealed at the anterior. Such is possible, but in the
available material we see no conclusive evidence. So too Smith considered alternative
possibilities for the functions of the various openings, noting that the identified gill may
have served for a respiratory exchange rather than being a gill in the deuterostome sense.
These discussions recall, of course, the protracted debate as to the correct interpretation of
the various orifices found in the pre-radial echinoderms, and in this context it is worth
emphasizing the remarkable diversity of the gill openings found in one group alone, the
stylophorans (e.g. Jefferies 1986; Dominguez et al. 2002). Swalla & Smith (2008)
commented that fossils of Vetulicystis “lack stereom and do not show a single echinoderm
synapomorphy, so it is not clear why these were placed in the Ambulacraria” (p. 1560).
This is certainly a valid point, but it goes to the heart of the question of how we might
identify the transformations that lead to a given body-plan. Presumably at some point in
the stem-group lineage of echinoderms the diagnostic calcitic stereom was acquired, just
as subsequently other diagnostic characters, such as the water-vascular system and
penta-radial symmetry, were acquired. Whilst provisional we would suggest that the
vetulicystid group could well be ancestral to all these important additions. In his
commentary Smith (2004) also mentioned the possibility that Phlogites (Supplementary
Figure 3a-c) “might even be a hemichordate or part of the common ancestral lineage of
echinoderms and hemichordates” (p. 412), a point that was cautiously endorsed in a
subsequent paper (Swalla & Smith 2008). Further work on this possibility is in progress
with Jean-Bernard Caron.
B) Second the chordates. So far as they are concerned the record of a possible
cephalochordate is restricted to Cathaymyrus (Shu et al. 1996b). The proposal by Chen
and Li (1997) that it is a crushed specimen of Yunnanozoon seems difficult to reconcile
with any yunnanozoan specimen, whatever its orientation (see also Smith et al. 2001, p.
74). Neither Cathaymyrus nor Pikaia from the Burgess Shale seem, however, to have a
particular similarity to amphioxus. The story of the urochordates is more complicated. The
report by Chen et al. (2003) of a tunicate (Shankouclava) has been widely accepted (e.g.
Smith 2004, Swalla & Smith 2008), but we suggest here that this may need
reconsideration for two reasons. First, because of the taphonomic circumstances
associated with the Chengjiang Fossil-Lagerstätte, which entails rapid burial by storm
activity followed by early diagenesis, the tentacles of various taxa may be obscured in
consolidated areas of sediment, and so require careful excavation. More specifically, a
re-examination by some of us of the eight specimens originally included in Shankouclava
(Chen et al. 2003) suggests that at least four of the specimens have remains of
tentacle-like structures (unfortunately the relevant region is cropped in the illustrations of
Chen et al. (2003)). Strong evidence in support of this view stems from the discovery of
a shankouclavid (from the same locality and horizon at Shankou village) that has an
almost identical main body, but in addition bears unequivocal distal tentacles (Figure 2g).
For these reasons we suggest Shankouclava is unlikely to be a tunicate (see also Shu 2008,
p. 231). An alternative proposal, that looks to Cheungkongella (Shu et al. 2001a), has met
with some scepticism and this taxon has been regarded as a junior synonym of Phlogites
(e.g. Chen et al. 2003). Whilst the single specimen of Cheungkungella (Supplementary
Figure 3d) has a similar anatomy to Phlogites (Supplementary Figure 3a-c) in terms of the
stalk and body, they differ fundamentally in the upper regions. Thus the former taxon
appears to have no trace of the multiple branching tentacles that are characteristic of
Phlogites. In addition the structure interpreted as an oral siphon (Shu et al. 2001a) is
quadrate and so does not have the rounded shape seen in the inter-tentacular lobes of
Phlogites (Caron et al. submitted and here Supplementary Figure 3a,b).
The presence of definitive craniates in the Chengjiang Fossil-Lagerstätte, which are of
course the earliest records of fish (Supplementary Figure 4), is perhaps the one area that
has met with a general consensus (at least to the first approximation) (Janvier 1999,
Valentine 2004, Halanych 2004, Dawkins 2004, Benton 2005, Prothero 2007). Three taxa
are identified: Myllokunmingia fengjiaoa (Supplementary Figure 4k) (Shu et al. 1999a),
Haikouichthys ercaicunensis (Supplementary Figure 4a-j) (Shu et al. 1999a, 2003; Hou et
al. 2002; Zhang & Hou 2004), and Zhongjianichthys rostratus (Supplementary Figure 4l,n)
(Shu 2003). The features that are visible make a telling contrast with the craniate
interpretation of yunnanozoans, with unequivocal myomeres (except in the anguilliform
Zhongjianichthys) which contra Hou et al. (2002) are W-shaped and not V-shaped
(Supplementary Figure 4e; see also Zhang & Hou 2004), paired eyes and a nasal sac
(Supplementary Figure 4a-d) (except in Myllokunmingia), and a prominent brachial basket
(Supplementary Figure 4f) in Haikouichthys (Shu et al. 2003b, Shu 2003). In the last
genus a notochord with equally-spaced vertebral elements has also been identified
(Supplementary Figure 4f-j; Shu et al. 2003), but it is notable that in this fish material the
notochord is more often indistinct, if not absent. Myllokunmingia (Supplementary Figure
4k) is only known from a single, albeit well-preserved specimen (Shu et al. 1999a).
Although it has been regarded as synonymous with Haikouichthys (Hou et al. 2002), we
suggest (see also Conway Morris 2006, Shu 2006) that this is unlikely for the following
reasons. Thus, the two taxa have different body proportions (Myllokunmingia is less
slender; e.g. Shu et al. 2003b, Fig. 1j, l), in Haikouichthys alone are dorsal fin rays evident
(curiously these are anteriorly inclined; note the earlier suggestion that these rays are
artefacts (Hou et al. 2002) cannot be supported (see also Zhang & Hou 2004)), and most
importantly in Myllokunmingia an absence of a branchial basket (along with a more
ventral position of the gills) is in contrast to the situation in Haikouichthys. Moreover,
Haikouichthys has as many as eight gill pouches, while Myllokunmingia has at most six.
Despite the co-existence of a notochord and vertebral elements it is striking how these
taxa, the most primitive of agnathans, differ from the extant cyclostomes. They provide an
important reminder that invaluable as the latter are for molecular insights attempts to
extrapolate the ecology and morphology of these living forms to the deep past can be
Benton, M.J. 2005 Vertebrate palaeontology (Third edition). Oxford, UK: Blackwell.
Chen, J-Y., Huang, D-Y., Peng, Q-Q., Chi, H-M., Wang, X-Q. & Feng, M. 2003 The first
tunicate from the early Cambrian of South China. Proc. Natl. Acad. Sci. USA 100,
Chen, J-Y. & Li, C-W. 1997 Early Cambrian chordate from Chengjiang, China. Bull. Natl
Mus. Natural Sci. Taiwan 10, 257-273.
Conway Morris, S. 2006 Darwin’s dilemma: the realities of the Cambrian ‘explosion’.
Phil. Trans. R. Soc B 361, 1069-1083.
Dawkins, R. 2004. The ancestor’s tale - A pilgrimage to the dawn of life. London, UK:
Weidenfeld & Nicolson.
Dominguez, P., Jacobson, A.G. & Jefferies, R.P.S. 2002 Paired gill slits in a fossil with a
calcite skeleton. Nature 417, 841-844.
Hou, X-G., Aldridge, R.J., Siveter, D.J., Siveter, D.J. & Feng, X-H. 2002 New evidence
on the anatomy and phylogeny of the earliest vertebrates. Proc. R. Soc. B 269,
Janvier, P. 1999 Catching the first fish. Nature 402, 21-22.
Jefferies, R.P.S. 1986 The ancestry of the vertebrates. London, UK: British Museum
(Natural History) and Cambridge University Press.
Prothero, D.R. 2007 Evolution: What the fossils say and why it matters. New York, NY:
Columbia University Press
Shu, D-G. 2003 A paleontological perspective of vertebrate origin. Chinese Sci. Bull 48,
Shu, D. 2006 Preliminary study on phylogeny of Chengjiang deuterostomes. In
Origination, radiations and biodiversity changes - Evidences from the Chinese fossil
record. (J. Rong, Z. Fang, Z. Zhou, R. Zhang, X. Wang, X. Yuan, eds), pp. 109-124
(in Chinese) and 841-844 (English summary). Beijing: Science Press
Shu, D. 2008 Cambrian explosion: Birth of tree of animals. Gondwana Res. 14, 219-240.
Shu, D-G., Chen, L., Han, J. & Zhang, X-L. 2001a An early Cambrian tunicate from China.
Nature 411, 472-473.
Shu, D-G. et al. 2003b Head and backbone of the Early Cambrian vertebrate
Haikouichthys. Nature 421, 526-529.
Shu, D., Conway Morris, S. & Zhang, X-L. 1996b A Pikaia-like chordate from the Lower
Cambrian of China. Nature 384, 156-157.
Shu, D-G., Conway Morris, S., Han, J., Zhang, Z-F. & Liu, J.N. 2004 Ancestral
echinoderms from the Chengjiang deposits of China. Nature 430, 422-427.
Shu, D-G., Luo, H-L., Conway Morris, S., Zhang, X-L., Hu, S-X., Chen, L., Han, J., Zhu,
M., Li, Y. & Chen, L-Z. 1999a Lower Cambrian vertebrates from South China. Nature
402, 42-46.
Shu, D-G. & Conway Morris, S. 2003 Response to comment on “A new species of
yunnanozoan with implications for deuterostome evolution”. Science 300, 1372d.
Smith, A.B. 2004 Echinoderm roots. Nature 430, 411-412.
Smith, M.P., Sansom, I.J. & Cochrane, K.D. 2001 The Cambrian origin of vertebrates. In
Major events in early vertebrate evolution (P.E. Ahlberg, ed.), pp. 67-84. London and
New York: Taylor & Francis.
Swalla, B.J. & Smith, A.B. 2008 Deciphering deuterostome phylogeny: molecular,
morphological and palaeontological perspectives. Phil. Trans. R. Soc. B 363,
Valentine, J.W. 2004. On the origin of phyla. Chicago, IL: University of Chicago Press,
Zhang, X-G. & Hou, X-G. 2004 Evidence for a single median fin-fold and tail in the
Lower Cambrian vertebrate, Haikouichthys ercaicunensis. J. Evol. Biol. 17,
Supplement Figures:
Fig. 1 Vetulicola cuneata (a,b,d) and V. rectangulata (c); stem-group Deuterostomia.
Details of gill slits. a, ELI-0000216, detail of gill slit viewed from exterior; note internal
aperture (arrowed in blue) covered by filamentous structure,; b, ELI-0000212, detail of
gill slit viewed from interior; note putative inhalant aperture (arrowed in blue); c,
ELI-0000210, detail of two gill slits, with external apertures (arrowed in red) and
flanking rhomboidal lappets; d, ELI-0000215, gill slits of left (lower level, with external
aperture in red) and right (upper level) sides, in latter note connecting tube-like
structures and also internal apertures (arrowed in blue). All scale bars millimetric.
Abbreviation in this and Fig. 2: ELI, Early Life Institute, Northwest University, Xi’an,
Fig. 2 Vetulicystids (a,b) and yunnanozoans (c,d); ?stem-group Ambulacraria. a,b
ELI-Ech-04-001A, holotype of Vetulicystis catenata, with camera-lucida interpretation;
note in particular the three prominent openings; c,d, Yunnanozoon lividum
NWU93-1406A, although indifferently preserved this specimen shows clear evidence
for partial detachment of the gill-bearing anterior from the more dorsal segmented
section. All scale bars millimetric.
Fig. 3 Phlogites (a-c); a, ELI-Phl-001, top view, note branching tentacles and
inter-tentacular lobes; b, ELI-Phl-002, lateral view showing tentacles and lobes with
body containing gut and possible reproductive bodies; c, ELI-Phl-003, lateral view
with tentacles and body with prominent gut; d, ELI-0000195, Cheungkongella, upper
part of body; note absence of tentacles, but an oral siphonal structure unlike the
inter-tentacular lobes of Phlogites.
Fig. 4 The earliest fish Haikouichthys ercaicunensis (a-j), Myllokunmingia fengjiaoa (k)
and Zhongjianichthys rostratus (l-n). a-d (respectively specimens ELI-Fish-273, 30B,
204, and 287): dorsal views, showing paired eyes, nostril, possible otic capsules, brain
and/or spinal cord; e, ELI- Fish-107, mid- trunk, showing complex myomeres and
probable heart; f-j (respectively specimens ELI- Fish-12B, 229, 251, 467, 97B, and
402): lateral views of the anterior, showing notochord with equally-spaced vertebral
elements, eyes, dorsal fin, myomeres, and branchial arches. k, ELI-0000201, holotype,
showing distinctive differences with Haikouichthys, including six gill pouches. l-n,
(respectively specimens ELI-00001604, 1605,1601): m, dorsal views, l and n, lateral
view, showing paired eyes and distinct antero-dorsal lobe. Abbreviations: Ba,
branchial arches; B&Sc, possible brain and/or spinal cord; DF, Dorsal fin; H, Heart;
Lap; Left anterior plate, LE, Left eye; M, Myomeres; N, Nostril; N&V, notochord with
vertebral elements; ?Oc, possible otic capsules; Rap, Right anterior plate; RE, Right
eye; G1,G2,G3,G4,G5,G6, gill pouches 1 to 6.