The Origin and Diversification of Osteichthyans and Sarcopterygians: Rare Chinese Fossil Findings Advance Research on Key Issues of Evolution
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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
L
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
has 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 t h e d a w n o f h i s t o r y. F o r m a n y
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 zhumin@ivpp.ac.cn.
Bulletin of the Chinese Academy of Sciences 71
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
Fig. 2 Reconstruction of “ghost fish” Guiyu as it may have lived in the Silurian waters 419
oldest near-complete gnathostome
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
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
( a b o u t 4 11 – 4 2 2 m i l l i o n y e a r s
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
Fig. 3 The family tree and geological time range of “ghost fish” Guiyu and other
sarcopterygian evolution unfolded and
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 m a j o r
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 73BCAS 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 Yo u n g C h u n g c h i e n , p i o n e e r o f
(Meemannia and Psarolepis from reinterpreted) in the light of Guiyu vertebrate paleontology in China) is
Yunnan, Ligulalepis from Australia, and Psarolepis. an early occurring member (about
and Dialipina 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 cosmine. Lack of similar tissue in and Diabolepis (“devil scale”) 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 ( C h a n g & Yu , 1 9 8 4 ; C h a n g &
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 nature 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 animals (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 lungfish lineage and
framework of deep osteichthyan supporting mineral deposition and the tetrapod 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 bone 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
L a s t l y, G u i y u p r o v i d e s 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 f r o m Yu n n a n h a v e b e c o m e t h e famous modern day living fossil
74 Bulletin of the Chinese Academy of SciencesVol.24 No.2 2010 Paleoichthyology
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.
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