Vol.24 No.2 2010 Paleoichthyology The Origin and Diversification of Osteichthyans and Sarcopterygians: Rare Chinese Fossil Findings Advance Research on Key Issues of Evolution YU Xiaobo1, 2 ZHU Min1* and ZHAO Wenjin1 1 Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthropology (IVPP), CAS, Beijing 100044, China 2 Department of Biological Sciences, Kean University, Union, New Jersey 07083, USA iving organisms represent into a hierarchical (or “set-within- chimaeras) with 970 living species, only 1% of all the biota that set”) pattern of groupings on the and the long-extinct placoderms and Lhas ever existed on earth. family tree, with members of each acanthodians. Within osteichthyans, All organisms, living or extinct, new group united by a common the actinopterygian lineage (with are related to each other by sharing ancestor and characterized by novel 26,981 living species) includes common ancestors at different levels, biological features. For instance, sturgeons, gars, teleosts and their like twigs and branches connected within vertebrates, gnathostomes (or relatives, while the sarcopterygian to each other at different nodes on jawed vertebrates) arose as a new lineage (with 26,742 living species) the great tree of life. One major task group when they acquired jaws as includes lungfishes, coelacanths for paleontologists and evolutionary novel features, which set them apart (Latimeria), their extinct relatives as biologists is to find out how the from jawless agnathans (lampreys, well as all land-dwelling tetrapods diverse groups of organisms arose hagfishes and their relatives). Within (amphibians, reptiles, birds, and and how they are related to each gnathostomes, four major groups mammals) (Fig.1). other, thereby reconstructing the developed: the bony osteichthyans The quest for their origins has history of life and understanding the (including all bony fishes and land- fascinated the human mind since pattern and process of evolution. dwelling tetrapods) with 53,633 the dawn of history. For many As organisms evolve and diverge living species, the cartilaginous years, scientists have puzzled over from common ancestors, they fall chondrichthyans (sharks, rays and questions such as: When and how did * To whom correspondence should be addressed at [email protected]. Bulletin of the Chinese Academy of Sciences 71 古脊椎专题.indd 71 2010-6-30 11:44:25 BCAS Vol.24 No.2 2010 (Zhu et al., 2009; Fig. 2). Guiyu (“ghost fish”) gets its name because of its ghostly or bazaar combination of morphological characters. Within gnathostomes, Guiyu sides with osteichthyans by bearing derived macromeric scales, yet it resembles non-osteichthyan chondrichthyans, placoderms and acanthodians by having a primitive pectoral girdle and median fin spine. Within osteichthyans, Guiyu sides with sarcopterygians by having a two part braincase with a movable joint in the middle (plus other cranial features), yet it resembles early actinopterygians by having ornamented ganoine surface covering and by the shape of its cheek and operculo-gular bones. Computerized analysis of morphological characters places Guiyu as an osteichthyan in the basal segment of the sarcopterygian Fig. 1 The family tree and geological time range of major vertebrate groups. Numbers of lineage (Zhu et al., 2009; Fig.3). living species (in brackets) indicate the relative abundance and diversity of the four living Three other fossil fishes from groups (Nelson, 2006). Yunnan (Meemannia, Psarolepis and gnathostomes arise? What would the common ancestor of all osteichthyans look like? How do osteichthyans relate to chondrichthyans, placoderms and acanthodians? How did osteichthyans diverge into the actinopterygian and sarcopterygian lineages? When and where did sarcopterygians arise and diverge? How did some sarcopterygian fishes eventually give rise to land-dwelling tetrapods, which include humans? These and related questions not only lie at the center of evolutionary research but also have broad implications for science in general. Because of recent fossil fish findings from China, the global study on these key areas of vertebrate evolution has made significant progress and is now at the threshold of an exciting breakthrough in the near future. The most significant fossil fish finding from China is Guiyu, the oldest near-complete gnathostome Fig. 2 Reconstruction of “ghost fish” Guiyu as it may have lived in the Silurian waters 419 million years ago. Guiyu represents the earliest near-complete fossil gnathostome and fossil found from the 419-Myr-old fossil osteichthyan record. muddy limestone in eastern Yunnan Picture courtesy of Brian Choo (Victoria Museum, Australia). 72 Bulletin of the Chinese Academy of Sciences 古脊椎专题.indd 72 2010-6-30 11:44:27 Vol.24 No.2 2010 Paleoichthyology Late Silurian or earliest Devonian (Lochkovian) sarcopterygians, including four stem sarcopterygians (Guiyu, Meemannia, Psarolepis and Achoania) and four forms near the base of major subgroups of sarcopterygians (Styloichthys, Diabolepis, Youngolepis and an unnamed onychodont). During the Late Silurian–Lochkovian periods (about 411–422 million years ago), the South China region was a separate continent adjacent to eastern Gondwana, and its vertebrate fauna as a whole was highly endemic to the region, indicating little or no exchange between this region and other areas before the Middle Devonian period (397 million years ago). It was in this isolated or semi-isolated environment that major events in early sarcopterygian evolution unfolded and Fig. 3 The family tree and geological time range of “ghost fish” Guiyu and other important early osteichthyans from China. Of the nine Late Silurian or earliest Devonian two subgroups developed, one giving (Lochkovian) sarcopterygians, eight (framed in red) come from South China, suggesting rise to living lungfishes while the other that this region was once a center of origin and diversification for early sarcopterygians. giving rise to all tetrapods, including humans (Fig. 3). Achoania) cluster with Guiyu as basal calibrated by using fossils as specific Third, Guiyu provides the most or stem sarcopterygians, but they historical time markers. Guiyu as complete morphological information come from younger ages and consist a basal member of sarcopterygians for establishing the morphotype (or of less complete materials when has an accurate dating based on the primitive morphological model) of compared with Guiyu. The earliest Silurian conodont zonation (419 early gnathostomes, osteichthyans geologic time of appearance, a near- million years old), and this indicates and sarcopterygians. Based on complete preservation of whole body that the minimal estimated time for the morphotype for each major structures, and a unique combination the actinopterygian–sarcopterygian group, paleontologists can generate of gnathostome vs non-gnathostome split must be at least 419 million hypotheses about the sequential characters as well as sarcopterygian years ago (instead of the previously order of morphological changes vs actinopterygian characters―all 416-million-year-old estimate based from the origin of a group to specific these make Guiyu highly significant on Psarolepis―another important evolutionary events in history, such for the global study on the origin early sarcopterygian fossil from as the branching of lineages or the of gnathostomes, the origin and Yunnan). With this new calibration, conquering of new environments by diversification of osteichthyans, the molecular clock is now more new groups. and the origin and diversification of accurate than before in gauging the Gnathostomes may have first sarcopterygians. time dimension for accumulated appeared in the Late Ordovician First, Guiyu provides critical molecular changes between different (more than 444 million years fossil record to calibrate the molecular living groups. ago), but non-osteichthyan groups clock regarding the divergence time Second, Guiyu (together with (chondrichthyans, placoderms between two major osteichthyan seven other early sarcopterygians from and acanthodians) left little or no lineages (i.e., actinopterygians and the Silurian and earliest Devonian complete fossil specimens before the sarcopterygians). While modern strata of southern China) establishes Early Devonian period. Similarly, biologists can determine the the paleobiogeographic importance previously known osteichthyan amount of molecular differences of ancient South China region as a fossils from the Late Silurian are separating different living groups, center of origin and diversification fragmentary and their lineage this information can serve as a useful for sarcopterygians. So far, Yunnan assignment is uncertain. Thus, molecular clock only when it is has yielded eight out of the nine Guiyu represents the earliest near- Bulletin of the Chinese Academy of Sciences 73 古脊椎专题.indd 73 2010-6-30 11:44:30 BCAS Vol.24 No.2 2010 complete gnathostome and the to exist only in non-osteichthyan “superstars” among paleontologists earliest near-complete osteichthyan groups. Consequently, many pre- for many other reasons. For instance, fossil known to science. Although Devonian spine-like materials can Youngolepis (named after late Prof. other important osteichthyan fossils now be reexamined (and possibly Young Chungchien, pioneer of (Meemannia and Psarolepis from reinterpreted) in the light of Guiyu vertebrate paleontology in China) is Yunnan, Ligulalepis from Australia, and Psarolepis. an early occurring