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Home , Cosmine, Dialipina, Ligulalepis, Onychodontiformes, Psarolepis, Sarcopterygii

Vol.24 No.2 2010 Paleoichthyology

The Origin and Diversification of Osteichthyans and Sarcopterygians: Rare Chinese Findings Advance Research on Key Issues of Evolution

YU Xiaobo1, 2 ZHU Min1* and ZHAO Wenjin1 1 Key Laboratory of Evolutionary Systematics of , Institute of 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 , 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, , gars, 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 , for paleontologists and evolutionary novel features, which set them apart (), their extinct relatives as biologists is to find out how the from jawless agnathans (lampreys, well as all land-dwelling diverse groups of organisms arose and their relatives). Within (, , , and and how they are related to each gnathostomes, four major groups ) (Fig.1). other, thereby reconstructing the developed: the bony osteichthyans The quest for their origins has and understanding the (including all bony 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 , scientists have puzzled over from common ancestors, they fall chondrichthyans (, rays and questions such as: When and how did

* To whom correspondence should be addressed at [email protected].

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(Zhu et al., 2009; Fig. 2). Guiyu (“ghost ”) 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 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 surface covering and by the shape of its cheek and operculo-gular . Computerized analysis of morphological characters places Guiyu as an osteichthyan in the 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). (Meemannia, 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 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, ).

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Late Silurian or earliest () sarcopterygians, including four stem sarcopterygians (Guiyu, Meemannia, Psarolepis and Achoania) and four forms near the base of major subgroups of sarcopterygians (, , 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 , 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 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 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--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 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-

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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 in China) is Yunnan, from Australia, and Psarolepis. an early occurring member (about and from the Canadian Meemannia (named in honor of 415 million years old) of the crown Arctic) have recently narrowed the Prof. Chang Meemann) is another sarcopterygian group (Fig. 3), and is morphological gap between different fossil fish from Yunnan that has one of the few osteichthyan fossils groups, they are mostly based on contributed significantly to the whose internal brain structures less complete materials and therefore understanding of sarcopterygian have been studied using 3-D are not as convincing as Guiyu in evolution (Zhu et al., 2006). reconstructions of serial grinding establishing the morphotype of Typical or crown sarcopterygians materials (Chang, 1982; Chang & Yu, early sarcopterygians and early are characterized by a special 1981). Kenichthys (named in honor osteichthyans. Guiyu provides a and now extinct tissue known as of Prof. Ken Campbell of Australia) classical textbook case showing . Lack of similar tissue in and Diabolepis (“devil ”) are how scientific hypotheses can be living vertebrates and the previous respectively the earliest members of tested through new discoveries. lack of rudimentary forms of this the lineages leading to all tetrapods Before the discovery of Guiyu, tissue presented a major obstacle and leading to modern-day lungfishes the restoration of many features for scientists to understand its mode (Chang & Yu, 1984; Chang & of Psarolepis (“speckled scale”) of origin and its function. Typical Zhu, 1993). Both Kenichthys and was sometimes regarded as weak cosmine is found only in certain Diabolepis played a critical role inferences because of the isolated and extinct sarcopterygians and consists in illuminating how tetrapods and disparate of fossil materials. of a pore-canal network embedded in lungfishes may have acquired their The near-complete restoration of mineralized dentine units and enamel. internal nostrils (or choana) as Guiyu (pending the discovery and Like its mosaic morphological novel evolutionary features (Zhu description of complete Psarolepis features, Meemannia reveals & Ahlberg, 2004). Internal nostrils specimen) provides the best possible previously unknown histological serve a vitally important function for authentication for most reconstructed features intermediate between the all air-breathing (including features of Psarolepis (Yu, 1998; typical cosmine tissue (found in later humans), and its origin has puzzled Zhu & Schultze, 1997; Zhu et al., sarcopterygians) and the ganoine-like paleontologists since the beginning of 1999). Together with Psarolepis, tissues (found in actinopterygians the 20th century. Styloichthys (“pillar Meemannia and other forms, Guiyu and some acanthodians). Meemannia fish”) shows what the common makes it possible to interpret suggests a stepwise mode of origin ancestor of modern-day lungfishes features found in early members of for cosmine and lends support to the and tetrapods may have looked like both lineages (actinopterygians and biological interpretation of the pore- and helps to explain the sequence sarcopterygians) in the common canal network as a vascular system in which the lineage and framework of deep osteichthyan supporting mineral deposition and the lineage acquired their phylogeny. Guiyu shows that the early resorption. Because of their sequential respective characters (Zhu & Yu, sarcopterygians and actinopterygians position on the early sectors of the 2002). Achoania (“without choana or retain widespread primitive sarcopterygian family tree, the cluster internal nostrils”) is closely related osteichthyan and gnathostome formed by Meemannia, Guiyu, to Psarolepis and suggests that early features, such as the cheek and Psarolepis, Achoania and Styloichthys or stem sarcopterygians may have operculo-gular pattern and the (Fig. 3) provides scientists with had an eyestalk as found in sharks anterodorsal process of the scale. unprecedented record of character and rays (chondrichthyans) and Lastly, Guiyu provides changes that helps to explain how extinct placoderms (Zhu et al., 2001). paleontologists with a new research sarcopterygians arose and eventually Last but not least, Qingmenodus agenda to focus more research developed into the two later lineages, represents one of the earliest resources and efforts on finding one leading to lungfishes, and the known onychodonts (a subgroup pre-Devonian osteichthyan fossils. other leading to tetrapods, including of sarcopterygians distantly related Guiyu (and Psarolepis) suggest that humans. to coelacanths) and helps to show early osteichthyans might carry In addition, these and other how this ancient fish may have had median fin spine and spine-bearing significant Chinese fossil fishes the same feeding mechanism as the pectoral girdles previously thought from Yunnan have become the famous modern day living fossil

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Latimeria (Lu & Zhu, 2010). The research on the Xiaoxiang group sarcopterygians (Zhao & The paleobiological roles of these Vertebrate Fauna will significantly Zhu, 2010). Given the exquisitely fossil fish findings cannot be fully improve our understandings of early preserved fossils with fine-scaled understood without detailed study of diversification of gnathostomes, stratigraphic control, study on the the associated faunas as a whole. Two especially when the morphological Xitun Vertebrate Fauna promises to significant vertebrate faunas have repertoire of acanthodians and the yield productive results regarding been established: the Late Silurian various primitive placoderms can the rapid diversification events Xiaoxiang fauna and the Early be fully deciphered and analyzed in responsible for the appearance of Devonian Xitun fauna. In addition to light of the new paradigm regarding crown-group sarcopterygians. All this Guiyu, Psarolepis and other (mostly the origin of osteichthyans from will provide a necessary framework microscopic or incomplete) remains non-osteichthyan groups. The Early to generate new hypotheses of osteichthyans, the Xiaoxiang Devonian Xitun Vertebrate Fauna is regarding the paleoenvironmental Vertebrate Fauna includes galeaspid characterized by the radiation and and paleogeographic aspects of this agnathans, acanthodians, and rich diversity of typical or crown- exciting chapter in the distant history diversified primitive placoderms. group placoderms and crown- of vertebrate evolution.

Main references

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