China - United States of America Collaborative Research: Critical Transitions in History of Life 1





China - United States of America Collaborative Research: Critical Transitions in History of Life
Zhe-Xi Luo: Carnegie Museum of Natural History, Pittsburgh, Samuel Bowring: Massachusetts Institute of Technology, Xiangdong Wang: Nanjing Institute of Geology & Palaeontology, : Nanjing Institute of Geology & Palaeontology, Douglas Erwin: Smithsonian Institution, Washington, D.C., Shuhai Xiao: Virginia Polytechnic Institute, James Clark: George Washington University, Washington, D.C., Xing Xu: Institute of Vertebrate Paleontology & Paleoanthropology, Beijing, Shuzhong Shen: Nanjing Institute of Geology & Palaeontology, Ke-Qin Gao: Peking University, Beijing, Xiaoming Wang: Natural History Museum of Los Angeles County, Qiang Ji: Chinese Academy of Geological Sciences, Beijing, Mark Norell: American Museum of Natural History
The history of earth and its diverse life are characterized by a number of critical transitions - episodes of profound biological and environmental evolution on global scales. These include the origins and early evolution of animals ca. 600 million years ago and their subsequent explosive diversification ca. 530 million years ago, the great biotic extinction and subsequent recovery at the Permian-Triassic transition, the Mesozoic origins of flowering plants and modern vertebrate lineages that dominate the modern terrestrial ecosystems, and the radiation of mammals in the early Cenozoic that eventually led to the rise of humans. Studying these transitions is crucial for understanding the relationships between biological evolution and changes in the physical environment. In this poster, we feature three of these intervals that have benefited from collaboration between U.S. and Chinese scientists during the past decade.
Accelerated research and exploration in paleontology in China over the past two decades have yielded a spectacular array of new discoveries. Fossil deposits in China offered new information in recent years for nearly every segment of the fossil record. These include:
  1. The spectacular fossil embryos from Neoproterozoic rocks of the Doushantuo Formation
  2. The Cambrian Chengjiang biota (Yunnan),
  3. The feathered dinosaurs and exquisite mammal fossils from the Jurassic and Cretaceous (Northeastern China).
In addition, through decades of painstaking work, Chinese scientists have established some of the best stratigraphic sequences in world for documenting such critical transitions as the Permian-Triassic mass extinction. These paleontological discoveries and advances in China have attracted scientists in other research disciplines; their significance transcends paleontology. The fossilized animal embryos in the Neoproterozoic allow us to explore the evolutionary development of major animal phyla. The earliest-known Mesozoic fossils of angiosperm plants and the modern mammal lineages are important for testing the hypotheses about phylogenetic relationships and timing of evolution by recent successful molecular studies on the evolution of these groups, and can be useful for calibrating the molecular evolutionary clock.

In the recent decades, the US scientists have developed an integrative and multi-disciplinary approach to paleobiology and the studies of earth history. There have been breakthroughs in using new analytical methods such as combining the morphological datasets from fossils with molecular phylogeny. There has also been a parallel development of database infrastructures for paleobiology and the integration of organic geochemistry with paleontology.

It has only recently become fruitful to apply an integrated approach to study the large-scale problem of the critical transitions that have been intractable despite their tantalizing promise. For example, the recent studies by high-precision geochronology and organic and isotopic chemostratigraphy have placed the biotic processes that occurred in the Neoproterozoic and across the Permian-Triassic transition in a global context, providing a framework for understanding the ecological response of the biotas to changes in physical environment.

The strength of the China - US collaborative effort in the studies of these critical transitions is complementary and synergistic, and thus has had a far greater impact. Since the late 1970s, the collaborative research by the American and Chinese scientists have covered all major areas of research in geology and paleontology, with many notable accomplishments.

With the support from the National Science Foundation (USA) and the National Natural Science Foundation of China, the US and Chinese geologists and paleontologists organized two workshops (November 2005 in USA and June 2006 in China) to review the recent progress and accomplishments, to identify future opportunities, to develop strategies to meet the challenges in collaborative research on Critical Transitions In History of Life.

To exemplify an enormous body of successful collaborative work geology and paleontology, we hereby showcase three scientific areas where the Chinese and American collaboration made significant progress in the understanding of history of life: (1) The early evolution of metazoan animal groups during the Neoproterozoic (1000 to 540 million years ago); (2) Research on dinosaurs and origin of birds; and (3) Origins and early evolution of mammals during the Mesozoic (250-65 million years ago).

Early evolution of metazoan animal groups during the Neoproterozoic (1000 to 540 million years ago)
The Neoproterozoic-Cambrian transition represents an important moment in Earth systems history. As tumultuous climatic perturbations waned in the terminal Neoproterozoic, animals and other multicellular eukaryotes began to diverge and diversify, followed by explosive radiation of most extant animal bodyplans in the Cambrian. This key transition provides a unique opportunity to understand the limit of climatic change and its impact on biospheric evolution, as well as the planetary effects of biological innovations on Earth's surface. The collaborative team takes a multidisciplinary approach to analyze the intricate interactions between biological evolution and environmental changes during the Neoproterozoic-Cambrian transition.

Major progress has been made in the following areas:
  1.  Paleontological evidence for the Neoproterozoic origin and divergence of multicellular clades, including animals. Following the initial reports of multicellular algae animal embryos from the Neoproterozoic Doushantuo Formation in South China (Zhang, 1989; Li et al., 1998; Xiao et al., 1998), a number of new discoveries have been announced. These include possible stem group cnidarians (Chen et al., 2002), red algae (Xiao et al., 2004), macoralgae (Xiao et al., 2002), acritarchs (Yuan and Hofmann, 1998; Zhang et al., 1998), and marine lichenoids (Yuan et al., 2005). There are also a number of problematic fossils from the Doushantuo Formation that have been interpreted as sponge amphiblastula and parenchymella larvae (Li et al., 1998),  anthozoan gastrulae and planula larvae (Chen et al., 2000; Chen et al., 2002; Chen and Chi, 2005), hydrozoans (Chen et al., 2002), and bilaterian embryos and adults (Chen et al., 2000; Chen et al., 2004). These fossils have the potential to expand our knowledge about multicellular evolution after the Cryogenian glaciations.

  2.  Paleontological and developmental insights into the Cambrian explosion and the rise of modern animal body plans.

  3. Geochronometric calibration of evolutionary rates during the Neoproterozoic-Cambrian transition. High-precision U-Pb zircon geochronology has revolutionized our understanding of the Neoproterozoic by allowing correlation of global chemostratigraphic signals. Recent work shows a potential relationship between perturbations of the carbon cycle and Metazoan evolution (Fig. 4). It is now possible to date volcanic ash beds in the Neoproterozoic to ±1 my or better.
 Future Collaborative Research: With improving age constraints (Zhou et al., 2004; Condon et al., 2005; Yin et al., 2005; Zhang et al., 2005), the team is planning to move forward to the next stage of its collaborative research. The major goal is to integrate paleontological, stratigraphic, geochemical, and geochronological data in order to test hypotheses about the causal relationship among Neoproterozoic-Cambrian evolutionary events (such as the rise and fall of Doushantuo-Pertatataka acritarchs and classic Ediacara organisms, the divergence and diversification of animals, and the initiation of biomineralization) and environmental events (the Gaskiers glaciation, the Acraman impact, major eustatic changes, and regional to global anoxia events).

Origins and early evolution of mammals during the Mesozoic (250-65 million years ago)
Mammals are one of the most visible vertebrate groups in the world today and they have many derived biological features and a spectacular array of adaptations. Some key mammalian features evolved from the Late Triassic (230 Ma) through Early Jurassic (180 Ma). Major modern mammalian lineages - placentals (e.g., human), marsupials (pouched mammals such as kangaroo) and monotremes (egg-laying mammals, like the platypus) can be traced, at least, to Middle Jurassic (~165 Ma). Collaborative studies by Chinese and American scientists on new Mesozoic mammals discovered in the last decade have gained significant insight into some long-standing problems of mammalian evolution:
  1. Stepwise evolution of key mammalian biological adaptations
    Many mammalian biological functions are associated with the bony features that can be preserved in their fossils. Joint Sino-US studies on the Early Jurassic mammals from Yunnan have established a stepwise pattern in evolution of diagnostic mammalian features in the ear (for sensory perception), the jaw hinge (for feeding), tooth replacement (related to lactation) and brain enlargement (related to physiological functions)  (e.g., Luo et al. 2001; Carnegie-IVPP collaboration) (Fig. 1). A new docodont mammaliaform (Ònear-mammal relativeÓ) from the Middle Jurassic of Inner Mongolia reveals the presence of mammalian hairs in the primitive relatives to the modern mammals. These integument structures (hairs and the inferred skin glands) in mammaliaforms indicate that endothermic (Òwarm-bloodÓ) physiology had already evolved in mammaliaforms, long before the diversification modern mammals (Ji et al. 2006; CAGS-Carnegie collaboration) (Fig. 2). By mapping the precursory condition of mammalian features on phylogenetic trees, these studies enriched our understanding about when and how the modern biological adaptations arose in the earliest mammalian history (220 to 160 Ma).
  2. Origins and divergence of placental and marsupial mammals
    The Chinese and American paleontologists discovered the world's earliest-known relatives (stem taxa) of placentals  and marsupials that make up 99.9% of the 4600 living mammal species of the world (Ji et al. 2002; Luo et al. 2003; CAGS-Carnegie collaboration). Eomaia and Sinodelphys from the Lower Cretaceous of Liaoning (Fig. 3) are the most primitive fossils that can be unequivocally placed onto the placental lineage and the marsupial lineage. Their anatomy presents the ancestral conditions from which the later placentals and marsupials have evolved. These excellent skeletal fossils have made it feasible, for the first time in mammalian evolutionary studies, to integrate the skeletal characters of Mesozoic taxa with those of extant placentals and marsupials that are under active evolutionary and genomic studies of molecular biologists. The supermatrix analyses of well-preserved new fossils revealed that a large number of stem taxa from the Cretaceous are clustered in successive episodes of diversification; their ranks on phylogenetic tree are in broad congruence with their chronological sequence (Luo and Wible 2005; Li and Luo 2006). This demonstrated that many stem taxa basal to marsupials and placentals are older than the molecular time estimate for the diversification of modern placental and marsupial orders, in concordance with their basal phylogenetic positions. With the recently improved molecular estimates (Murphy et al. 2001; Douzery et al. 2004; Nilsson et al. 2004), new fossils of Eomaia and Sinodelphys extended the minimal divergence time for marsupials and placentals, and reduced the previous gaps of molecular time-estimate and the fossil record, although some areas of discrepancy between molecular estimates and fossil records have yet to be reconciled.

    Future Collaborative Research: Recent research on mammalian evolution has opened up the possibility of a full integration of morphological features from all Mesozoic mammal groups, with the molecular data (some including entire genomes) of all modern mammal orders. Further American and Chinese collaboration is planned for a combined morphologic and genomic approach to mammalian phylogenetics. This holds a good promise both for comparative genomics that requires a mammalian evolutionary tree corroborated by fossils, and for paleontology to gain a new perspective on rates and timing of mammalian evolution.
  3. Mesozoic mammalian ecomorphological diversification
     As recent as 1999, a widely endorsed concept was that Mesozoic mammals were small terrestrial insectivores with generalized structure. Constrained by their small size and general features, their ecomorphological may not be manifest during their phyletic splits. This is now shown to be inaccurate by functional analyses of new fossils from China and US. The climbing locomotory features of Sinodelphys and Eomaia (Fig. 3) suggest that the marsupial-placental divergence was associated with ecological diversification. Castorocauda suggests that some mammals invaded aquatic niche in Mesozoic (Fig. 2). Several Mesozoic mammals, such as Repenomamus (Hu et al. 2005; IVPP-AMNH collaboration) and Castorocauda (Ji et al. 2006) were large enough to be carnivorous and feeding on small vertebrates (Hu et al. 2005). Others developed the highly specialized feeding of social insects (Luo and Wible 2005). These collaborative studies have now demonstrated significant ecomorphological diversification of Mesozoic mammals, some of which occurred 100 million years earlier than the convergent ecological diversification in unrelated Cenozoic mammals.

    Future Collaborative Research: It is now feasible to estimate the ecomorphological parameters (feeding, locomotory, and body size ranges) of major vertebrate groups in such well preserved biotas as the Yixian Formation. If correlated with paleoenvironmental and taphonomic data, such research can enrich our understanding of the rise of the modern terrestrial ecosystems in the Mesozoic.
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Dinosaurs, feathers and origin of birds
 Dinosaur fossils with feathers from Early Cretaceous sediments in Liaoning, northeastern China, are providing remarkable insights into the origin of birds. These feathered dinosaurs demonstrate that feathers arose among theropod dinosaurs before the origin of powered flight and that some of the closest relatives of birds had flight feathers on both their fore and hind limbs. Cooperative research between Chinese and American scholars on these and other theropod dinosaur discoveries is helping to clarify the changes that took place among theropods as birds arose from them.

Most of what we know about dinosaurs comes from their skeleton, which is all that is preserved in the vast majority of cases. Fossil deposits in Liaoning, in northeastern China, offer a rare glimpse into what the rest of these animals looked like.  Specimens from these deposits often preserve skin and other soft tissues, and include a diverse fauna of terrestrial and aquatic animals 125 million years old. The most spectacular fossils from these beds are the Òfeathered dinosaursÓ, dinosaurs bearing bird-like feathers that provide the strongest evidence that birds are descended from dinosaurs. In the same beds are found exceptionally pristine skeletons lacking soft tissues but preserved in three dimensions, and include dinosaurs preserved in a sleeping posture, apparently overcome by volcanic ashes. NSF-funded research involving US and Chinese paleontologists has supported much of this research.

 Skeletal similarities shared by birds and dinosaurs indicate that birds evolved from within the Theropoda, a group comprising carnivorous dinosaurs such as T. rex. Analyses of these similarities reveal that some theropods are closer to birds than are others. Among the closest relatives of birds are ÒraptorsÓ such as Velociraptor from the Gobi Desert of Mongolia and China. NSF funded research is mapping out the details of this major evolutionary transition, from ground-living dinosaurs to flying birds.

 Seven different feathered dinosaurs are known from these deposits, some closer to birds than others. Fully vaned feathers, similar to the flight feathers of birds, are found only on those species closest to birds. More distantly related theropods, including tyrannosaurs, have only simple, filamentous feathers. Remarkably, the feathered dinosaur fossils strongly suggest that feathers evolved before flight, because none of these forms appear to have been capable of flying. Even more surprising, some of the feathered dinosaurs preserve well-developed vaned feathers not only on their forelimbs but on their hindlimbs, tantalizing evidence for the origin of flight that paleontologists are trying to understand.

Future Collaborative Research: Important discoveries continue to be made in Liaoning, and several teams of researchers are describing feathered dinosaur remains as they arise. Important questions concern the precise pattern of feather distribution in each species, the function of feathers prior to the origin of powered flight, and the taxonomic distribution of feathers among different groups of dinosaurs. Collaborative research funded by NSF also includes related projects such as field work in Xinjiang, northwestern China, that is discovering the oldest remains of several theropod groups closely related to birds, such as tyrannosaurs.

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