http://www.paper.edu.cn Chinese Science Bulletin 2003 Vol. 48 No. 8 725-735 Cover: The earliest-known and most primitive vertebrates on the A paleontological perspective Earth---Myllokunmingia fengjiaoa ， (upper) Zhongjianichthys rostratus of vertebrate origin （ middle ）， Haikouichthys ercaicunensis (lower left and lower right). They were SHU Degan Early Life Institute & Department of Geology, Northwest products of the early Cambrian 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 Yunnan about 530 millions of years ago. These ancestral vertebrates not only Abstract The Early Cambrian Haikouichthys and Haikouella 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 craniates (true vertebrates). The (e.g. large eyes), and a prominent notochord with differentiated vertebral elements. This “first fish” 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. It differs from chordates in many organs and organ systems, birthplace of the whole vertebrates. 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 hemichordates. On the basis of these and other recent findings of fossil deuterostomes, 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-chordate Haikouella ， Early Cambrian, Chengjiang Lagerstatte, origin of vertebrates, deuterostomes evolution DOI: 10.1360/03wd0026 For two centuries since the time of Lamarck, the animal 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. Chinese Science Bulletin 2003 Vol. 48 No. 8 April 2003 725 中国科技论文在线 http://www.paper.edu.cn 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 cephalochordates extract evolutionarily relevant information from living and urochordates［4-8］. The second problem, a major one, animals, 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 paleontology 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 deuterostome 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 hemichordate-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 bone (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