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Home , Cathaymyrus, Haikouella, Haikouichthys, Myllokunmingia, Yunnanozoon

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Chinese Science Bulletin 2003 Vol. 48 No. 8 725-735 Cover: The earliest-known and most primitive on the A paleontological perspective Earth--- fengjiaoa ， (upper) Zhongjianichthys rostratus of origin （ middle ）， ercaicunensis

(lower left and lower right). They were SHU Degan Early Life Institute & Department of Geology, Northwest products of the early Explosion, University, Xi’an, 710069, China; School of Earth

excavated from the famous Chengjiang Sciences and Resources, China University of Geosciences, Beijing, 100083, China Lagersttat, which was formed in the (e-mail:[email protected])

eastern about 530 millions of years ago. These ancestral vertebrates not only Abstract The Early Cambrian Haikouichthys and have been claimed to be related to contribute in an important developed primitive separate vertebral way to our understanding of vertebrate origin, but there have elements, but also possessed principal been heated debates about how exactly they are to be interpreted. New discoveries of numerous specimens of sensory organs, including a pair of large Haikouichthys not only confirm the identity of previously lateral eyes, nostril with nasal sacs, then described structures such as the dorsal and the ventral fins, and chevron-shaped myomeres, but also reveal many new had led to the transition from acraniates to important characteristics, including sensory organs of the head (true vertebrates). The (e.g. large eyes), and a prominent with differentiated vertebral elements. This “first ” appears, discoveries of these “naked” agnathans however, to retain primitive reproductive features of have pushed the earliest record of acraniates, suggesting that it is a stem-group craniates. A new order (Myllokunmingiida) and a new family vertebrates back into the deep time for (Myllokunmingiidae) are erected, and a new species, about 50 millions of years. South China, Zhongjianichthys rostratus (gen. et sp. nov.), is described herein. Over 1400 newly-discovered specimens of Haikouella therefore, is suggested as the oldest-known provide a wealth of anatomical information on this organism. birthplace of the whole vertebrates. It differs from in many organs and organ systems, including the skin, muscles, respiratory, circulatory and nervous systems. In contrast, its body-design resembles that of vetulicolians, and the presence of a “transitional” nervous system with both dorsal and ventral nerve cords suggests an affinity with living . On the basis of these and other recent findings of fossil , a five-step hypothesis for vertebrate origin is proposed, intended to bridge the long-standing gap between protostomes and vertebrates. Four of the five steps accord with established ideas current in modern evolutionary zoology. Evidence for the first step is obtainable only from fossils, and specifically from fossils found from South China, hence the crucial importance of S. China sites for our understanding of early vertebrate origins and evolution. Accordingly, South China is suggested as the oldest-known birthplace of the whole vertebrates.

Key words: Primitive vertebrate Haikouichthys ， non- Haikouella ， Early Cambrian, Chengjiang Lagerstatte, origin of vertebrates, deuterostomes evolution

DOI: 10.1360/03wd0026

For two centuries since the time of Lamarck, the kingdom has been recognized as being divided into two major groups-vertebrates and invertebrates. Studying their evolutionary relationships, i.e. to trace when, where and how early vertebrates originated from invertebrates, has been a core subject in evolutionary biology. There are two basic ways to investigate the origin of vertebrates. One is the indirect approach of modern zoology; the other is the direct approach of paleobiology.

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Various branches of zoology, including morphology, pology conflicts with the widely accepted zoological view, embryology, and molecular biology, have been used to particularly in inverting the relation of extract evolutionarily relevant information from living and urochordates［4-8］. The second problem, a major one,

, but the latter make up only a very small from paleontological perspective, is that the ages of nearly proportion of the total number of species produced by all branches of calcichordates are far younger than the evolution. Most of the transitional forms, that would tell period when they would have had diversity. Clearly, us most about important evolutionary events, are almost has two jobs to perform in relation to origin of certainly now extinct, and can be recovered only as vertebrates. The first is to try to find out the earliest and the fossils. most primitive vertebrate fossils. The second is to trace The earliest serious hypothesis for vertebrate origins back using those vertebrates as a starting point, and was the “developmental inversion” idea of the French discover the nature of their ancestors. early evolutionist G. Saint-Hillaire (1822). He observed Although various kinds of animals had been described

that the central neural system and the heart are located in from the Early Cambrian period (i.e. the Cambrian the dorsal and ventral sides respectively of vertebrates, Explosion) by 1995, they were exclusively protostomes ［11-16］ while the reverse is true of arthropods and annelids. Based with the exception of a few echinoderms. . Recently, on this fact, he postulated that the appearance of with the investigation of the Chengjiang fauna, a large

vertebrates might have resulted from inversion of the number of deuterostomes have been found, including embryo of arthropods or annelids. Although this idea was examples of urochordates, cephalochordates and initially refuted by G. Cuvier (1830), and really suffers -related animals, which are all transitional ［17-23］ ［24， from some major weaknesses, it has been recently revived forms ancestral to vertebrates , their extinct relatives by modern developmental biologists because of some 25］, as well as real vertebrates［26-28］. Based on this material, supporting molecular data. More widely accepted is the a new hypothesis of “five step” evolutionary origin for conventional phylogenetic tree of animals with, at its vertebrates is proposed here. base, a relatively short “trunk” of diploblastic animals, from which a larger “crown” of the triploblastic animals

arises. This, in turn, is separated into two major divisions: 1 Newly identified characters of Haikouichthys and their protostomes and deuterostomes. It is hard to imagine that evolutionary implications the vertebrates and arthropods, which lie on the tops of protostome and deuterostome branches respectively,

might be closely related, though there are a remarkable number of molecular similarities between them. But it is Among the 33 living phyla of animals, only the phylum Chordata includes both vertebrates and generally held in evolutionary biology that the vertebrates invertebrates. The phylum encompasses three subphyla: the could not have arisen from any of the higher groups of protostomes. Instead, they must be rooted in a series of Urochordata with a notochord limited to the posterior lower deuterostomes. section only; the Cephalochordata with the notochord One of the most influential hypothesis dealing with extending along the whole of the longitudinal axis (also named as Acraniata, due to the absence of clearly vertebrate origins from within the deuterostomes is the Garstang-Berrill-Romer theory of the paedomorphosis. recognizable head structures); and the Vertebrata with a ［1-3］ . After a long debate, by the 1980s a phylogenetic backbone and cranium of cartilage or (also called relationships of Craniata). The first two groups are referred to as lower chordates or protochordates, while the vertebrates are the (echinoderms+(hemichordates+(urochordates+(cephaloch ordates+vertebrates)))) as shown in was widely accepted higher chordates. In molecular terms, the lower chordates, ［ ］ (Schaeffer 1987) 4 . Since then, molecular and together with all their invertebrates, are distinguished by developmental data have reinforced the link between having a single Hox gene cluster only, while the vertebrates have multiple clusters［29］. With the increasing complexity of echinoderms and hemichordates, which make a natural the genome, both the Hox gene and other developmentally group, leading to a lineage with four branches rather than five［5-8］. However, for this hypothesis, there are still two important control genes, vertebrates have made enormous major problems to be solved: (1) does it conform to the advances morphologically. historical reality as seen in the fossil record, and (2) what The transition from acraniates to craniates involves a series of innovations in embryonic development and is the nature of the most basal deuterostomes, i.e. more primitive than the branch echinoderms + hemichordates? morphology, three of which are as follows: (1) the

More specifically, this review will examine whether fossil appearance of neural crest has led to formation of many material from the Chengjiang deposits answers one or important new structures such as the dorsal fin and gill skeleton［29］；(2) vertebral elements evolved so as to make both of these questions. The calcichordate theory of vertebrate origin is so far the longitudinal supporting axis stronger and more flexible;

the only one which is established primarily on the basis of (3) cephalization accompanied with development of fossil data.［9，10］. It suffers two major difficulties and is a sensory organs produced a functionally important ［5］ structures. The discovery of the early Cambrian “naked” “distinctly minority view” . One problem is that its to- Myllokunmingia and Haikouichthys has pushed the Chinese Science Bulletin 2003 Vol. 48 No. 8 April 2003 726

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earliest vertebrate record back by roughly 50 millions stomes［34，35］，and from early Paleozoic “ostracoderms” ［ ］ ［ ］ years, so these are really the first fish we know of 30 . 36 . This means that a new taxon may be needed for However, there was only a single specimen of each them. My proposal is for a new order species respectively when first reported. As a result, Myllokunmingiida and a new family only very limited anatomic information was available. Myllokunmingiidae. The definition for the former is: In particular, because the data on the vertebral elements naked agnathans with both well-developed dorsal and and sensory organs were lacking, it was difficult to ventral fins, complex myomeres, primitive gill arches, judge the exact evolutionary position of these species31］. well-developed sensory organs in the head and The Early Life Institute of Northwest University has separated cartilaginous vertebral elements, but with recently found hundreds of new and well-preserved multiple repeated gonards. The definition for the new samples of Haikouichthys, which have provided much family is: those myllokunmingiids with a fusiform body, needed details, including information on principal and a pair of large eyes within the dorso-anterior lobe. sensory organs in the head and vertebrae . . The new 2 A Newly discovered early Cambrian vertebrate specimens provide much more reliable evidence Along with Haikouichthys, from the same horizon

regarding the origins of important organs in the or slightly higher beds, five other specimens of different earliest-known fish［28］. fish species were obtained. They were largely preserved The lowest living vertebrates are the agnathan, i.e. on the top of small-scale of graded beds, suggesting that and . The former has a strong, thick they were probably the victims of catastrophic ocean notochord lacking vertebral elements. The latter has storms. The new species, Zhongjianichthys rostratus, small vertebral elements (arcualia) on the dorsal side of has an almost eel-like body. The eyes are located behind the notochord. From our material, Haikouichthys the antero-dorsal lobe, in contrast to the situation in appears to have separated metameric cartilaginous Myllokunmingiidae, so it is temporarily assigned to an vertebral elements as well. Additionally, the primitive uncertain family. vertebrae have bifid or arched structures on their dorsal Phylum Chordata and ventral sides, which could represent the precursors Subphylum Vertebrata to the later dorsal and ventral arches respectively. Thus, Class in this respect, Haikouichthys is more like a Order Myllokunmingiida (order nov.)

well-developed vertebrate than living agnathans. Family uncertain However, what is most interesting is that Haikouichthys Zhongjianichthys gen. nov. has a remarkable combination of characters in its head, Zhongjianichthys rostratus gen. et sp. nov. （ ） including a pair of very large lateral eyes, a single Figs.1 and 2-1---5 median nostril with a pair of nasal capsules behind it, Etymology. Generic name to honor Zhongjian and a pair of possible otic capsules. This suggests the Yang, who is recognized as one of the founder of brain itself must have been reasonably well developed vertebrate paleontology in China; the specific name as it is in craniates. On the other hand, an orbit (eye refers to the rarity of the samples. socket) is lacking, nor has a cartilaginous skull been Holotype. ELI-0001601（23）. Together with identified. In this respect, Haikouichthys is less other four specimens ELI-0001602-05, all are deposited advanced than the living cyclostomes. In addition, what in the Early Life Institute, Northwest University, Xi’an, may show its real primitiveness is that Haikouichthys, China. unlike any living vertebrate, bears multiple, repeated Stratigraphy and locality. Qiongzhusi

gonads, which, among living forms, is seen only in Formation, middle of Yu’anshan Member (Eoredlichia acraniates. This could indicate that the evolution of Zone), Lower Cambrian. Specimens collected from reproductive organs has logged that of non-reproductive Jianshan, about 2 km east of Ercai village, Haikou, near organs. Dianchi lake, Kunming, Yunnan. Cladistic analysis of both the lower fossil fishes Diagnosis. Body small in size, elongate and and living agnathans has reconfirmed that eel-like in shape, without clear boundary between head Haikouichthys is really among the most primitive and trunk. The dorsal of the head extends forward into a ［ 28 ］ vertebrates . It is interesting, however, that the rostral lobe. Along the anterior edge of this lobe there is cartilaginous gill arches of Haikouichthys are much a pair of arcuate plates, between which is the median simpler than the complex branchial basket in lampreys, nostril. Behind the anterior lobe are situated a pair of but similar to gills in gnathostomes in number, location eyes, between or slightly anterior to which is a pair of and structure, especially with respect to the lower units, tiny nasal sacs. The skin is naked. No trace of zigzag known as the ceratobranchials and hypobranchials. This myomeres is recognizable. There are at least five pairs

interesting feature might suggest that Haikouichthys be of simple gill arches in the antero-ventral region. ［32，33］ related with the early origin of gnathostomes . Description and comparison: Altogether five samples In summary, these primitive naked vertebrates, available, the body relatively small in size, elongated Haikouichthys and Myllokunmingia, are quite different morphologically from the living and fossil cyclo- and ell-like, rather than fusiform in shape, consist Chinese Science Bulletin 2003 Vol. 48 No. 8 April 2003 727

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ing of the head and the trunk regions, but without clear longer than that of Haikouichthys. Perhaps more boundary between the two divisions. From the lateral view, importantly, its eyes lie behind the anterior lobe rather the dorsal part of the head extends forward into a than within the lobe as the latter case. Second,

blunt, beak-like projection, termed the antero-dorsal lobe. Zhongjianichthys has thicker skin than It is separated from the rest of the head by a slight Haikouichthys.Third, Zhongjianichthys has an elongated constriction. Along the anterior edge of this lobe there is a eel-like body shape with less-evident development of pair of arcuate plate-like structures, between which is there the dorsal and ventral fins. This is quite unlike that a notch, which is interpreted as a median nostril. Behind fusiform body-design of the two other known early the anterior lobe are situated a pair of oval and distinctly Cambrian fishes. dark stains, which, like corresponding structures in Discussion. Compared with Haikouichthys, the new Haikouichthys, most probably represent eyes. Between or genus and species has several advanced characters and slightly anterior to the large eyes is a median structure, specialized features. Among the former are: (1) The

possibly paired and preserved in a similar way to the eye comparatively posterior location of the eyes. stains. This is rather similar to the case in Haikouichthys Anteriorly-positioned eyes in Haikouichthys and other and is likewise interpreted as part of the olfactory organ, “naked” fossil agnathans such as Jamoytius, are possibly nasal sacs. An alternative interpretation, considered primitive［28,35］. So the posteriorly located

although less-likely, is that these structures represent the eyes (behind the anterior lobe) of Zhongjianichthys may pineal/parapineal complex. The skin was apparently naked, represent an advanced character. (2) The absence of without any scales or external plates, but it was in life myotome impressions. In the both Haikouichthys and presumably relatively thick, as no trace of myomeres Myllokunmingia, the muscle blocks are clearly seen, beneath the skin is recognizable. There are at least five which indicates that the epidermis is thin and probably, pairs of simple gill arches in the antero-ventral region. made of a single layer of cells, as in living amphioxus. The present species is similar to Haikouichthys In the present species, the myomeres are hardly ercaicunensis in several respects, including the presence of recognizable, which indicates that its epidermis, as in a pair of large eyes, a single nostril with possible nasal sacs living lower craniates (lamprey and hagfish), was

behind it, the arcuate plates anterior to the antero-dorsal thicker, consisting of multiple layers of cells. A lobe, and a set of simple gill arches. However, specialized feature of Zhongjianichthys is its elongated Zhongjianichthys in at least three respects differs from eel-shaped body and the reduced fins, suggesting a Haikouichthys. First, its anterior-dorsal lobe is much limited swimming ability and perhaps an epi-faunal

mode of life that included intermittent burrowing.

Fig.1. Camera-lucida drawing of Zhongjianichthys rostratus gen. et sp. nov. Chinese Science Bulletin 2003 Vol. 48 No. 8 April 2003 728

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Figure 2: (a)-(e) Zhongjianichthys rara gen. et sp. nov.; (f)-(k) Haikouichthys ercaicunensis, (f),(g),(i) showing details in head. Except (e),(g),(i)

from dorso/ventral view， the others are from lateral view；(h),(j)(k) showing anatomy of the anterior body

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Figure 3: (a).Myllokunmingia fengjiaoa; (b). Xidazoon stephanus; (c) Didazoon haoae; (d). Vetulicola cuneata; (e) Vetulicola rectangulata; (f) Cheungkongella ancestralis; (g) diadexus (h) Haikouella lanceolata; (i)-(k) Haikouella jianshanensisI;. (l) lividum; (m). A possible soft-bodied cystoid-like animal (echinoderm). Chinese Science Bulletin 2003 Vol. 48 No. 8 April 2003 730

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3 Reexamination of Haikouella trace of notochord［18,39］, and it is also not clearly present

Yunnanozoans are enigmatic animals from the early in the posterior section. Modern taphonomic experiments Cambrian, which are known only from South China. shows that the notochord persists after death and should Owing to their unique body-plan, they have been classified therefore be more easily preserved than other soft parts ［37］ as a separated class . The class at present comprises two of the body. Therefore, its absence in yunnanozoans is genera：Yunnanozoon and Haikouella. When it was first suggestive.［44］. We should note that, the gut is commonly reported, the taxonomic position of Yunnaozoon was seen in the specimens of Haikouella jianshanensis, but uncertain ［ 38 ］ . Subsequently, as its gill structure was no evidence exists for a separate structure identifiable as ［22］ understood, it was assigned to the chordates and then a notochord. Besides, as the supporting axis to the trunk, reassigned to hemichordates［18］. the notochord is thick, strong and rigid, which usually There have possibly been claims based on some prevents the body from being folded or bent as in deformed specimens that Haikouella had a tripartite brain, Cathaymyrus ［19］. The flexibility of the trunk and the eyes, teeth and even primitive vertebrae, and that it might tendency for it to be tightly folded is inconsistent with represent an early ［ 23 ］ . Recently, over 1400 the presence of a notochord［45］。

soft-bodied examples of Haikouella have been unearthed (3) The respiratory system of yunnanozoans, by the Early Life Institute of Northwest University (Xi’an) without an atrium, is unique in lower deuterostomes. from the Jianshan section, Haikou region, Kunming City, There are up to 6 pairs of external bipectinate gill arches, Yunnan. The animal is similar in most respects to the type which connect the dorsal and ventral units. These are species H. lanceolata，but is distinctly different from the fundamentally different from the internal gills in latter in poor preservation of its postero-dorsal segments chordates. possibly due to weak cuticulization. Moreover, the new (4) The circulatory system of yunnanozoans consists form is stratigraphically earlier than H. lanceolata. of a pair of dorsal and a pair of ventral blood vessels Accordingly, it has been assigned to a new species H. respectively, which have no counterpart in chordates［17］. jianshanensis［39］. Investigation of ca. 520 well-preserved (5) The anterior section of H. jianshanensis is often specimens of the larger collection (Fig3-9- -11)，together preserved, showing lateral aspect, with little or no with reexamination of the numerous available examples of breaking or deformation. In well-preserved examples no Haikouella lanceolata (Fig3- trace of brain, eyes, teeth or other vertebrate characters

8) and Yunnanozoon (Fig3-12)，have led to the following are recognized. One can see a dorsal nerve cord in some new conclusions: examples, but it never expands anteriorly to form a brain ［39］ (1) While yunnanozoans are fundamentally （ Fig3- 11） 。 different from chordates in many respects, they resemble (6) H. jianshanensis may have had both ventral and vetulicolians in terms of basic body-design［24,40,41］. Both dorsal nerve cords ［ 39 ］ . This feature occurs only in have a segmented body, divided into two major sections hemichordates among living organisms, and these are (anterior and posterior) with the anterior section in turn believed to be transitional forms between chordates and ［ 17 ］ separated by an expandable median zone into dorsal and non-chordates . Therefore, from the viewpoint of ventral parts（Fig 2）。 evolution, Haikouella, and most probably all (2) The dorsal segments in yunnanozoans are peculiar, yunnanozoans apparently, are evolutionarily closest to somewhat similar to those in arthropods and annelids, and hemichordates, although they are different fail to show any sign of v-shaped boundaries characteristic morphologically. An alternative position for of chordates ［ 42,43 ］ . In the anterior section of H. yunnanozoans would be as a sister group with

jianshanensis, probably of all yunnanozoans, there is no vetulicolians, owing to similarities in their body-plans （ compare c with d in Fig. 5）.

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Figure 5: Phylogenies of deuterostomes and origin of vertebrates: (a). after B. Schaeffer 1987; (b). after H. Gee 2001; (c) and (d) two alternative phylogenies of deuterostomes based on information from both modern zoology and the early Cambrian fossils. c, with more emphasis on the significance of nervous system in evolution; d, with more emphasis on the significance of the similarity of basic body-plans in evolution numerous protostomes have been reported from this period. 4 Deuterostomes from Chengjiang Lagerstatte and their This means direct evidence as to vertebrate origins in the implications regarding origin of vertebrates form of fossils, remains a problem. In principle, finding the ancestors of vertebrates among There is one hypothesis, the calcichordate theory that the lower deuterostomes should be far more difficult than does depend on fossil evidence［9,10］. However, it has some finding the earliest-known vertebrates themselves. One difficulties. Perhaps, the newly discovered Chengjiang expects the former, as soft-bodied creatures, to be extremely fossils will fill existing gaps in the record, allowing us to difficult to preserve. In fact, except a few echinoderm construct a more complete sequence of transitional forms ［18-28］ records, no reliable deuterostomes have been recognized in between the protostomes and the vertebrates . This the early Cambrian and older strata , though sequence, in my view, should have at least five major

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branches as follows. the sister group made up of the echinoderms and ［ ］ (1)The vertebrate branch. The discoveries of hemichordates 5-8 , both of the latter have secondly lost Myllokunmingia and Haikouichthys, and perhaps also segmentation, and echinoderms further lost gill slits. A few Zhongjianichthys, have pushed the early history of primitive echinoderms have been reported from the early ［26,27,30］ ［51］ vertebrates back by ca. 50 millions of years . The Cambrian in the USA and elsewhere , but no reliable extensive recently-found material of Haikouichthys echinoderms have so far been recorded from Chengjiang. further confirms that this animal, with its serial gonads, Phlogites, with tri-radiate branched arms (tentacles) might, must represent one of the most primitive vertebrates［28］. however, be some sort of soft-bodied ancestor to ［52］ This gives us a base for the terminal branch of the echinoderms . In addition, there is a newly-discovered phylogeny. soft-skinned cystoid-like organism with both the incurrent (2) The branch. Morphology and and ex-current cones, that might be also among this developmental zoology show that the living group(Fig.3- 13). If we accept that the shift in the nerve cephalochordates (amphioxus) is the closest relative to cord from a ventral position in non-chordates to a dorsal lower agnathans (lampreys and hagfish)［17，46］. This idea one in chordates is significant in evaluating deuterostome

reconfirmed by strict cladistic analysis of deuterostomes evolution, yunnanozoans, which may have both, like (Schaeffer, 1987)［4］, and is further supported by living hemichordates, may represent the transitional link ［6，7］ molecular and neuro-anatomic data . The question （ Fig.5-(c)）. Likewise, pterobranchs and enteropneusts then is, of known acraniates, including living and fossil are closely related (actually they form two main branches forms, which one is closest to the ancestor of the in hemichordates), but they are fundamentally distinct vertebrates? Since the amphioxus has a notochord from each other morphologically. extending forward to anterior end, which may prevent (5) The vetulicolian or vetolicolian + yunnanozoon from the full development of a true brain skull, it is branch. Among living forms the clade of echinoderms + generally considered as a derived and specialized hemichordates represent the lowest deuterostomes. creature that could never be a direct ancestor of craniates. However, there were undoubtedly other more primitive , from the middle Cambrian , forms among deuterostomes in the distant past. bearing a pair of strange anterior tentacles, is also Segmentation and gill slits are thought to be the primitive believed to be specialized, and peripheral to the lineage characters in deuterostomes, and the former might have ［ ， ］ leading to the vertebrates 26 42 . The early Cambrian been present in their common ancestor with protostomes. cephalochordate-like animal Cathaymyrus （ possibly Gill slits, however, are accepted as major morphological ［5］ con-specific Zhongxiniscus, which was laterally innovation of deuterostomes . Therefore, the segmented preserved and would not be so different anatomically vetulicolians, which have gill slits, most probably from the dorso-ventrally preserved Cathaymyrus）might represent the earliest-known and the most primitive actually be closest to the precursor of vertebrates here, members in deuterostomes［24 ］. In fact, Xidazoon, the based on appearance, size, its dorsal fin, myomeres, lowest member of vetulicolians is present in the earliest ［19，47］ pharynx and closely-spaced gill slits （Fig.3- 7）. strata at Chengjiang. Its gill slits are simple and lack gill (3)The urochordate branch. Nearly all the results filaments, as expected of a structure designed to drain from morphology, development and molecular biology excess water from the pharynx.［24，25］. Vetulicola, younger point to the conclusion that cephalochordates are rooted than Xidazoon, has more complex gill slits, with fine ［ 5 ， 48 ， 49 ］ in the urochordates , regardless they might filaments, which may have functioned as respiratory represent a subphylum within the phylum Chordata［17］, or organs (Figure 3- 4,5). A newly discovered giant ［ ， ］ might be treated as a separated phylum 7 50 . To date, the vetulicolian from Chengjiang has very long delicate earliest-known urochordate recognized is the filaments in its gill slits, which is the most advanced Cheunggongella ancestralis from Chengjiang, which condition seen in this group （ Ai-lin Chen, personal ［20］ ） closely resembles the living tunicate Styela . This tends communication . Gill slits in vetulicolians are, however, to support, in some way, the traditional text book view rather different from those in calcichordates ［ 53 ］， (Garstang-Berrill)［1，2］，and the degraded lophophores on yunnanozoans, living hemichordates, and chordates as the top of incurrent-siphon of Cheunggongella would well ［17］. Vetulicolians therefore probably represent an early provide good support to this hypothesis(Fig.3-6). specialized side-branch of early deuterostomes. Though （4）The echinoderm + hemichordate branch. Exploring thrived in the early Cambrian, they appear to be a lineage the possible forebears of urochordates among that has left no modern representatives. In fact, they non-chordates is very tough indeed, as the morphological evidently disappeared after they first appeared in the fossil gap between chordates and non-chordates is obviously record. Perhaps competition from more advanced enormous. Nevertheless, it is widely accepted by modern chordates, including actively-swimming fishes, and

zoologists that the common ancestors to all chordates predatory arthropods (e.g. anomalocarids, the so-called should have two essential characters, segmentation and “Cambrian dinosaurs”), extinguished them before the ［5］ pharyngeal slits . If this same ancestor also gave rise to close of the Cambrian. The earliest appearance of vetuli-

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colians suggests that segmentation in cephalochordates (5) It has been generally accepted that the and vertebrates may not be independently acquired reconstruction of life history would now chiefly character but rooted from the common ancestor of depend on the advancement in molecular biology ［54］ protostomes and deuterostoms. and new remarkable findings in paleontology . In summery, among the five-step phylogeny New results from molecular biology indicate that the inferred dates for the origin of vertebrates are proposed here on the basis of the fossil material from the ［55］ close to the age of the fossils described here . It earliest known radiation of deuterostomes, last four steps follows that South China’s deposits are of crucial are consistent with generally held ideas. However, the importance in attempts to understand the origin of first step, the appearance of the vetulicolians, is a new vertebrates, a major group of animals that includes idea dependent entirely on fossil evidence. Vetulicolians ourselves. have gill slits unique to deuterostomes on one hand, and segmentation, which may have been present in the latest Acknowledgements L. Chen, Y. Li, X-L. Zhang, common ancestor with protostomes on the other. J. Han, Z-F. Zhang, J-N. Liu, H-Q. Liu, H-X. Guo, Accordingly, this extinct group is proposed here as the Y-B. Ji, M-R. Cheng, J-P. Zhai are thanked for their assistance in both field work and lab work. I starting point for the evolutionary sequence leading to higher deuterostomes（Figure 5c）. There are still many am grateful to Mi-man Zhang for kind advice, and to S. Conway Morris, T. Lacalli, K. Yasui, S. gaps in this sequence, which hopefully will be filled as Turner, P. Janvier, J. Bergstroem, John Long and new fossil material is discovered. two anonymous referees for their comments and 5 Conclusion valuable suggestions, and my special thanks to S. Conway Morris, who has made his significant (1) Haikouichthys has three features that place it firmly contributions to our joint papers on early among the lower vertebrates: primitive vertebral deuterostomes. This work was supported by the elements, sensory organs in the head and structures National “973” Project (Grant No. G-2000077702) derived from the neural crest cells (e.g. dorsal fin, gills and the National Natural Science Foundation of and arches). On the other hand, it retains serial gonads, China (Grant No. 32070207). a primitive feature seen only in acraniates.

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