The origin of the vertebrate jaw

20 downloads 83 Views 3MB Size Report
Aug 7, 2012 - New York: Henry Holt and. Company, 1996. 1–223 ... 1615–1632. 7 Heimberg A M, Cowper-Sallari R, Sémon M, et al. MicroRNAs re- veal the ...
COVER

Volume 57 Number 30 October 2012

The origin of the jaw was perhaps the most profound and radical evolutionary step in the evolutionary history of vertebrates. Advances in developmental genetics have led to the heterotopy theory of jaw evolution, i.e. the jaw evolved through a heterotopic shift of mesenchyme-epithelial interactions. According to this theory, the disassociation of the nasohypophyseal complex in jawless vertebrates was a fundamental prerequisite for the origin of the jaw. Recent studies using synchrotron radiation X-ray tomography of the cranial anatomy of galeaspids, a 435–370-million-year-old ‘ostracoderm’ group from China and northern Vietnam, have provided the earliest fossil evidence for the disassociation of the nasohypophyseal complex in vertebrate phylogeny. This paper reports fresh anatomical observations of the genus Shuyu that further show some derivative structures of the trabeculae in jawless galeaspids, thus shedding new light on the reorganization of the vertebrate head before the evolutionary origin of the jaw. This study provides an intriguing example of the intersection between developmental biology-based models and fossil evidence (Life and 3D virtual restorations of Shuyu, a 430-million-year-old jawless fish that lived in the ancient oceans of South China. Life restoration by Brian Choo, IVPP; see the review by GAI ZhiKun & ZHU Min on page 3819).

Journal Ownership by Science China Press; Copyright of articles: © The Author(s) 2012 Journal’s Policy for Open Access All articles published in the journal Chinese Science Bulletin are subject to the Creative Commons Attribution License (http:// creativecommons.org/licenses/by/2.0/). Publishing an article with open access leaves the copyright with the author and allows user to read, copy, distribute and make derivative works from the material, as long as the author of the original work is cited. Submission of a manuscript implies: that the work described has not been published before (except in the form of an abstract or as part of a published lecture, review, or thesis); that it is not under consideration for publication elsewhere; that its publication has been approved by all co-authors; if any, as well as – tacitly or explicitly – by the responsible authorities at the institution where the work has carried out. The author warrants that his/her contribution is original and that he/she has full power to make this grant. The author signs for and accepts responsibility for releasing this material on behalf of any and all co-authors. The use of general descriptive names, trade names, trademarks, etc., in this publication, even if not specifically identified, does not imply that these names are not protected by the relevant laws and regulations. While the advice and information in this journal are believed to be true and accurate at the date of its going to press, the authors, the editors, and the publishers cannot accept any legal responsibility for any errors or omissions that may be made. The publishers assume no liability, express or implied, with respect to the material contained herein Copyright and License Agreement For copyright regulations and license agreement, please go to www.springeropen.com/about/copyright

Abstracted/indexed in: Academic Search Alumni Edition Academic Search Complete Academic Search Elite Academic Search Premier ASFA 1: Biological Sciences and Living Resources ASFA 2: Ocean Technology, Policy and Non-Living Resources Biological Abstracts Biological Sciences BIOSIS Previews CAB Abstracts Chemical Abstracts Chemical and Earth Sciences Current Contents/Physical Current Mathematical Publications Digital Mathematics Registry

EMBio Environmental Engineering Abstracts Environmental Sciences and Pollution Management Google Scholar Inspec Mathematical Reviews MathSciNet Meteorological and Geoastrophysical Abstracts Pollution Abstracts Science Citation Index SCOPUS Water Resources Abstracts Zentralblatt MATH Zoological Record

Volume 57 Number 30 October 2012

CONTENTS

Progress of Projects Supported by NSFC REVIEW Geology 3819 The origin of the vertebrate jaw: Intersection between developmental biology-based model and fossil evidence GAI ZhiKun & ZHU Min

INVITED ARTICLE 3829

Condensed Matter Physics The orbital characters of low-energy electronic structure in iron-chalcogenide superconductor KxFe2−ySe2 CHEN Fei, GE QingQin, XU Min, ZHANG Yan, SHEN XiaoPing, LI Wei, MATSUNAMI Masaharu, KIMURA Shin-ichi, HU JiangPing & FENG DongLai

REVIEW 3836

Mechanical Engineering Bio-manufacturing technology based on diatom micro- and nanostructure ZHANG DeYuan, WANG Yu, CAI Jun, PAN JunFeng, JIANG XingGang & JIANG YongGang

LETTERS 3850

Organic Chemistry Significant effects of branches and bromine substitution of near-infrared two-photon photosensitizers on the generation of singlet oxygen LI HongRu, YE XiaoJuan, LIU Meng, GAO Fang, LIU XiaoJiao & GUO QinYuan

Geology 3855 Eocrinoids from the Cambrian Mantou Formation of Dalian, Liaoning HUANG DiYing

ARTICLES 3858

Condensed Matter Physics Numerical analysis on the current-sharing temperature of LTS/HTS hybrid conductor CUI YingMin, WANG YinShun & LÜ Gang

3862

Physical Chemistry Synthesis of chain-like MoS2 nanoparticles in W/O reverse microemulsion and application in photocatalysis LIU MeiYing, LI XiaoQian, XU ZhiLing, LI BoNa, CHEN LinLin & SHAN NanNan

3867

Analytical Chemistry Comparative crystal structure determination of griseofulvin: Powder X-ray diffraction versus single-crystal X-ray diffraction PAN QingQing, GUO Ping, DUAN Jiong, CHENG Qiang & LI Hui

3872

Plant Physiology Low concentrations of NaHSO3 enhance NAD(P)H dehydrogenase-dependent cyclic photophosphorylation and alleviate the oxidative damage to improve photosynthesis in tobacco WU YanXia, HE Wei, MA WeiMin, SHEN YunKang & MI HuaLing

3878

Molecular Biology Characterization of ligand response properties of the CRP protein from Pseudomonas putida JIANG Feng, TIAN ZheXian & WANG YiPing

3886

Molecular Virology Identification of in vivo interaction between rabbit hemorrhagic disease virus capsid protein and minor structural protein YANG ZongWei, NI Zheng, YUN Tao, CHEN ZongYan, LI ChuanFeng & LIU GuangQing

www.scichina.com | csb.scichina.com | www.springer.com/scp | www.springerlink.com

i

CONTENTS 3891

Preclinical Medicine Effects of Eriobotrya japonica (Lindl.) flower extracts on mercuric chloride-induced hepatotoxicity in rats ESMAEILI Amir Hossein, KHAVARI-NEJAD Ramazan Ali, HAJIZADEH MOGHADDAM Akbar, CHAICHI Mohammad Javad & EBRAHIMZADEH Mohammad Ali

3898

Bioinformatics Relationships of mRNA-protein secondary structures in the human β-globin gene HBB and four variants LI YanFei, YE DongHai, ZHANG Wen, WANG ChuanMing, LIU CiQuan & CAO Huai

Oceanology 3908 A quasi-global 1/10° eddy-resolving ocean general circulation model and its preliminary results YU YongQiang, LIU HaiLong & LIN PengFei 3917

Paleoproductivity variations in the southern Okinawa Trough since the middle Holocene: Calcareous nannofossil records ZHAO JingTao, LI TieGang, LI Jun & HU BangQi

3923

Atmospheric Science Global and China temperature changes associated with the inter-decadal variations of East Asian summer monsoon advances QIAN WeiHong, LIN Xiang & ZHU YaFen

3931

Materials Science Formation and mechanical properties of Zr-based bulk metallic glass composites with high oxygen levels LIU ZengQian, YANG YaoWei, LI Ran, HUANG Lu & ZHANG Tao

Optoelectronics 3937 The effect of multi-quantum barrier structure on light-emitting diodes performance by a non-isothermal model WANG TianHu, XU JinLiang & WANG XiaoDong 3943

Artificial Intelligence A computational coding model for saliency detection in primary visual cortex ZOU Qi, WANG Zhe, LUO SiWei, HUANG YaPing & TIAN Mei

3953

Engineering Thermophysics Experimental study of n-heptane ignition delay with carbon dioxide addition in a rapid compression machine under lowtemperature conditions GUANG HuanYu, YANG Zheng, HUANG Zhen & LU XingCai



Vol. 57 No. 30 October 25, 2012 (Published three times every month)

Supervised by Chinese Academy of Sciences Sponsored by Chinese Academy of Sciences and National Natural Science Foundation of China Published by Science China Press and Springer-Verlag Berlin Heidelberg Subscriptions China Science China Press, 16 Donghuangchenggen North Street, Beijing 100717, China Email: [email protected] Fax: 86-10-64016350 North and South America Springer New York, Inc., Journal Fulfillment, P.O. Box 2485, Secaucus, NJ 07096 USA Email: [email protected] Fax: 1-201-348-4505 Outside North and South America Springer Customer Service Center, Customer Service Journals, Haberstr. 7, 69126 Heidelberg, Germany Email: [email protected] Fax: 49-6221-345-4229 Printed by Beijing Zhongke Printing Co., Ltd., Building 101, Songzhuang Industry Zone, Tongzhou District, Beijing 101118, China Edited by Editorial Board of Chinese Science Bulletin, 16 Donghuangchenggen North Street, Beijing 100717, China Editor-in-Chief XIA JianBai CN 11-1785/N 广告经营许可证: 京东工商广字第0429号 ii

邮发代号: 80-214 (英) 国内每期定价: 108元 www.scichina.com | csb.scichina.com | www.springer.com/scp | www.springerlink.com

Review October 2012 Vol.57 No.30: 38193828

Progress of Projects Supported by NSFC Geology

doi: 10.1007/s11434-012-5372-z

The origin of the vertebrate jaw: Intersection between developmental biology-based model and fossil evidence GAI ZhiKun & ZHU Min* Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China Received May 8, 2012; accepted May 29, 2012; published online August 7, 2012

The origin of the vertebrate jaw has been reviewed based on the molecular, developmental and paleontological evidences. Advances in developmental genetics have accumulated to propose the heterotopy theory of jaw evolution, i.e. the jaw evolved as a novelty through a heterotopic shift of mesenchyme-epithelial interaction. According to this theory, the disassociation of the nasohypophyseal complex is a fundamental prerequisite for the origin of the jaw, since the median position of the nasohypophyseal placode in cyclostome head development precludes the forward growth of the neural-crest-derived craniofacial ectomesenchyme. The potential impacts of this disassociation on the origin of the diplorhiny are also discussed from the molecular perspectives. Thus far, our study on the cranial anatomy of galeaspids, a 435–370-million-year-old ‘ostracoderm’ group from China and northern Vietnam, has provided the earliest fossil evidence for the disassociation of nasohypophyseal complex in vertebrate phylogeny. Using Synchrotron Radiation X-ray Tomography, we further show some derivative structures of the trabeculae (e.g. orbitonasal lamina, ethmoid plate) in jawless galeaspids, which provide new insights into the reorganization of the vertebrate head before the evolutionary origin of the jaw. These anatomical observations based on new techniques highlight the possibility that galeaspids are, in many respects, a better proxy than osteostracans for reconstructing the pre-gnathostome condition of the rostral part of the braincase. The cranial anatomy of galeaspids reveals a number of derived characters uniquely shared with gnathostomes. This raises the potential possibility that galeaspids might be the closest jawless relatives of jawed vertebrates. Our study provides an intriguing example of intersection between developmental biology-based model and fossil evidence. jaw, agnathans, gnathostomes, galeaspids, trabecula, evolutionary developmental biology Citation:

Gai Z K, Zhu M. The origin of the vertebrate jaw: Intersection between developmental biology-based model and fossil evidence. Chin Sci Bull, 2012, 57: 38193828, doi: 10.1007/s11434-012-5372-z

The invention of the jaw appears to be a crucial innovation and perhaps the most profound and radical evolutionary step in the vertebrate history [1,2]. The importance of this invention is obvious, as the jaw allows vertebrates to become ‘superpredators’ at the top of the food chain [3,4], and subsequently gnathostomes (jawed vertebrates) expanded to occupy a broad range of ecological niches and account for 99.8% of vertebrate diversity today [5]. However, the sequence leading to the evolutionary origin of the jaw is still enigmatic largely due to the absence of data on the ancestral, intermediate condition [6]. Hagfishes and lampreys are the *Corresponding author (email: [email protected]) © The Author(s) 2012. This article is published with open access at Springerlink.com

only living jawless vertebrates (cyclostomes) which are generally considered as the sister group of crown gnathostomes [7,8]. Their phylogenetic position makes them critical to understand the emergence of novelties at the agnathan-gnathostome transition [9]. However, due to the large morphological gap between extant jawless and jawed vertebrates [10], the living cyclostomes actually provide little information about the profound reorganization of the vertebrate skull and body plan that occurred along with the origin of the jaw [11]. The extinct armoured jawless vertebrates, or ‘ostracoderms’, are regarded as precursors of jawed vertebrates [12–16] (‘Ostracoderms’, Figure 1) and provide insights into this formative episode in vertebrate evolution [11]. For csb.scichina.com

www.springer.com/scp

3820

Gai Z K, et al.

Chin Sci Bull

October (2012) Vol.57 No.30

Figure 1 Phylogenetic framework of vertebrates. The monophyly or paraphyly of cyclostomes (hagfishes and lampreys) has been the subject of heated debate for over a century. As the jawless ‘ostracoderms’ are closer to jawed vertebrates than cyclostomes, they fall into the total-group gnathostomes. In other words, the ‘ostracoderms’ are stem gnathostomes (note the distinction between gnathostomes and jawed vertebrates: the jawed vertebrates only include placoderms and the crown-group gnathostomes). Modified from [7,16].

example, these extinct bony jawless vertebrates provide some evidence that many features, which are present in extant gnathostomes but absent in cyclostomes, such as the exoskeleton, perichondral bone, sclerotic ring, pectoral fins, and epicercal tail, have been acquired before the origin of the jaw [12,17]. However, none of them shows any structure that would possibly foreshadow a mandibular arch of the gnathostome type, i.e., with a palatoquadrate and a Meckelian cartilage [10]. In addition, as the visceral arches in extant cyclostomes and jawed vertebrates are positioned differently relative to the gill filaments (lateral in the former, but medial in the latter), the homology of visceral arches between jawless and jawed vertebrates had been a century-long heated debate [10,18–24]. In a sense, the origin of the jaw appears to be a sudden event in vertebrate evolution, probably lacking an ancestral, intermediate condition like the origin of the horizontal semicircular canal of the inner ear [25]. In a somewhat different field from the comparative anatomy of jawless and jawed vertebrates (searching for the ancestral, intermediate condition of jaws) [10,26], a series of advances in molecular, developmental and embryological studies have accumulated to present a new scenario for the developmental origin of the jaw. Kuratani and his collaborators proposed the heterotopy theory of the jaw evolution on the basis of the developmental genetics of the lamprey and gnathostome head [6,27–32]. Their theory assumes that the disassociation of the nasohypophyseal complex for the development of trabecula is a fundamental prerequisite for the origin of the jaw. Accordingly, the appearance of the diplorhiny and trabecula should have preceded that of the jaw [6,27–31]. The disassociation of the nasohypophyseal

complex is also regarded as a major event for the origin of diplorhiny [10,12,13], possibly allowing the Hh gene family to establish the lateral position of the nasal sacs. Recently, our studies on the cranial anatomy of galeaspids, a 435– 370-million-year-old ‘ostracoderm’ group from China and northern Vietnam [33], have provided the earliest fossil evidence for the disassociation of nasohypophyseal complex in vertebrate phylogeny [11]. Using Synchrotron Radiation X-ray Tomography, here, we further show that some derivative structures of the trabeculae (e.g. orbitonasal lamina, ethmoid plate) are also present in galeaspids. This indicates that galeaspids at least partly possessed the true trabeculae as in jawed vertebrates. The trabeculae cranii of jawed vertebrates has long been regarded as a major developmental advance over agnathans [34]. Previously, discussions on whether the trabecula is present in the jawless ancestors of gnathostomes mainly relied on the developmental biologybased model because for lack of relevant fossil evidence. The identification of trabecula-derived structures in jawless galeaspids sheds new light on the reorganization of the vertebrate head before the evolutionary origin of the jaw. Our study discusses the potential bearings of galeaspid head innovation on the vertebrate phylogeny, and provides an intriguing example of intersection between developmental biology-based model and fossil evidence.

1 Developmental model for the origin of the vertebrate jaw: the heterotopy theory The vertebrates are characterised by the presence of the

Gai Z K, et al.

Chin Sci Bull

neural crest and the placodes which provide the basis for the formation of a new head (e.g. paired sensory organs, trabeculae cranii) and visceral skeleton [35,36]. The comparative embryology of lampreys and gnathostomes indicates that the initial distribution of neural crest cells is conserved in both groups. From rostral to caudal, three distinct populations of neural crest cells—the trigeminal, hyoid and branchial crest cells—can be distinguished at the stage of pharyngula (pink, yellow and green, Figure 2(a),(b)) [27,37]. The trigeminal crest cells (pink, Figure 2(a),(b)) are distributed mainly in the region rostral to the first pharyngeal pouch (PA1, Figure 2(a),(b)). They can be further subdivided into the premandibular crest cells (pmc, Figure 2(c)–(f)) and the mandibular crest cells (mc, Figure 2(c)–(f)) which are the basic materials differentiating into the oral supporting apparatus (e.g. the jaw) [6,27,37]. The patterning of visceral arches including mandibular arch can be viewed as the neural crest cells in a Cartesian grid of the regulatory gene expression (Figure 2(a),(b)) [31]. Hox genes, a specific class of homeobox, are expressed along the antero-posterior axis of the embryonic pharynx. Through a nested pattern of Hox gene expression, each pharyngeal arch acquires its positional value to differentiate into specific morphology (Hox, Figure 2(a),(b)). In gnathostomes, the jaw is differentiated from the first pharyngeal arch (PA1, Figure 2(b)), which is characterised by the Hox code default state (no Hox genes expressed in mandibular arch) [27,38]. Cohn [39] reported that one of the Hox genes, HoxL6, is expressed in the mandibular arch of lampreys, and suggested that loss of Hox expression from the mandibular arch of gnathostomes may have facilitated the invention of the jaw. However, more recent observations in lamprey Lethenteron japonicum revealed no Hox cognate expresssion in the mandibular ectomesenchyme at any stage of development [38]. Kuratani [28] considered that the Hox-default state in mandibular arch is still important for the origin of the jaw (e.g. allowing the trigeminal ectomesenchyme to vary its range easily without the constraints of Hox code), and this default state was probably established in the common ancestor of lampreys and gnathostomes. Similarly, Dlx genes are expressed in a dorso-ventral nested pattern to differentiate the dorsoventral pattern of each visceral arch in gnathostomes (Dlx, Figure 2(b)) [40]. However, such nested expression of Dlx genes has not been detected in lampreys (Dlx, Figure 1(a)). Compared to the Hox-code default, the nested expression of Dlx genes can be observed in the madibular arch of gnathostomes [40]. With the aid of homeobox genes such as Dlx and Msx (the oral patterning program), the trigeminal ectomesenchyme differentiates into the oral supporting apparatus in lampreys and gnathostomes. According to the heterotopy theory [30], the jaw evolution has involved a caudal shift of the oral patterning program (e.g. Dlx, Msx and their growth factors FGF and BMP, Figure 2(c),(d)). In lampreys, the oral patterning program is expressed in both the mandibular and

October (2012) Vol.57 No.30

3821

premandibular ectomesenchyme (Dlx, FGF8, BMP4, Figure 2(c)). Thus, the premandibular ectomesenchyme differentiates into the upper lip (ulp, Figure 2(a),(c)), and the mandibular ectomesenchyme differentiates into the lower lip and velum (llp, vel, Figure 2(a),(c)). By contrast, in gnathostomes, the oral patterning program is restricted to the mandibular region (Dlx, FGF8, BMP4, Figure 2(d)), thus only the mandibular ectomesenchyme differentiates into the oral apparatus (mx, mn, Figure 2(b),(d)). The premandibular ectomesenchyme that used to differentiate as the agnathan upper lip (ulp, Figure 2(a),(c),(e)) is now utilized to form the gnathostome trabecula (tr, Figure 2(d),(f)). Consequently, the jaw evolved as an evolutionary novelty through tissue rearrangements and a heterotopic shift of mesenchymeepithelial interaction [27].

2 Disassociation of the nasohypophyseal complex as a fundamental prerequisite for the origin of the jaw According to the heterotopy theory [6,27–31], the heterotopic shift of tissue interaction should have taken place after the acquisition of the diplorhiny and trabecula. A substantial distinction in the head structures of cyclostomes, in comparison with gnathostomes, is the presence of a single median duct, or ‘nostril’ (no, Figure 3(a),(b)), leading to the nasohypophyseal organ (na, hy.d, Figure 3(a),(b)), which develops from a single median nasohypophyseal placode (nhp, Figure 2(e)). By contrast, gnathostomes possess the paired separate nasal sacs (na, Figure 3(e)) with individual externalized nostrils (no, Figure 3(e)) and independent hypophyseal organ (hy.d, Figure 3(e)). These three structures developed from three independent placodes, the paired laterally faced nasal placodes (np, Figure 2(f)) and the Rathke’s pouch (Rp, Figure 2(f)). Such placodal morphology allows premandibular crest cells (pmc, Figure 2(f)) of gnathostomes to grow rostrally to form the trabecula, and the mandibular ectomesenchyme (mc, Figure 2(f)) to grow anterolaterally to form the jaw. However, in lampreys, the rostral growth of the premandibular neural crests (pmc, Figure 2(e)) is precluded by the median nasohypophyseal placode. Thus, the invention of the jaw firstly required the disassociation of the nasohypophyseal placode for the development of trabecula. Kuratani [27] speculated that the jawless ancestors of gnathostomes may be found in the forms with paired nostrils and trabecula in the fossil record.

3 Hedgehog (Hh) gene family and the separation of nasal sacs The disassociation of the nasohypophyseal complex is also regarded as a major event for the evolutionary origin of the diplorhiny (nasal sacs with individual externalized nostrils)

3822

Gai Z K, et al.

Chin Sci Bull

October (2012) Vol.57 No.30

Figure 2 The comparative embryology of lampreys and gnathostomes. (a)–(b) Initial distribution of neural crest and the gene expression patterns of lampreys (a) and gnathostomes (b); pink, yellow, and green: trigeminal, hyoid, and branchial crest cells population, from Kuratani [27, fig. 3A]. (c)–(d) Distribution patterns of trigemnal crest cells and oral patterning program of lampreys (c) and gnathostomes (d), showing that the oral patterning program Dlx, Msx and their growth factors FGF8 and BMP4 have a caudal shift in gnathostomes, from Shigetani et al. [30, fig. 3A–D]. (e)–(f) Topographical relationships between oral ectoderm, nasohypophyseal complex and trigemnal crest cells in lampreys (e) and gnathostomes (f), from Kuratani [27, fig. 5C] and Kuratani et al. [6, fig. 9a]. In gnathostomes, the premandibular crest cells (pmc) grow rostrally between the Rathke’s pouch (Rp) and the paired nasal placodes (np) to form a part of the trabecular cartilage (tr). The mandibular crest cells (mc) grow antero-rostrally to form the upper jaw halves that fuse in front of the hypophysis. In lampreys, the rostral growth of the premandibular crest cells (pmc) is precluded by the nasohypophyseal plate (nhp) to form the upper lip. BMP, bone morphogenetic factor; e, eye; FGF, fibroblast growth factor; hy, hyoid arch; llp, lower lip; mc, mandibular crest cells; mhb, mid-hindbrain boundary; mn, mandibular process; mx, maxillary process; nas, nasal region; nc, nasal capsules; nhp, nasohypophyseal plate; np, nasal placodes; nt, notochord; oe, oral ectoderm; ot, otic vesicle; PA, pharyngeal arches; pm, premandibular mesoderm; pmc, premandibular crest cells; r1–r5, rhombomeres; Rp, Rathke’s pouch; tr, trabecular cartilage; ulp, upper lip; vel, velum; 1–8, pharyngeal slits or pouches.

Gai Z K, et al.

Chin Sci Bull

October (2012) Vol.57 No.30

3823

Figure 3 The early evolution of nasohypophyseal complex. Galeaspids are, in many ways, a better proxy than osteostracans for reconstructing the pregnathostome condition of the rostral part of the braincase. This raises the potential possibility that galeaspids might be the closest jawless relatives of jawed vertebrates, modified from [11]. ade, adenohypophysis; br, branchial duct or slit; eso, oesophagus; hy.d, hypophyseal or buccohypophyseal duct; hy.o, hypophyseal opening; m, mouth; nc, neural cord; na, nasal sacs; no, nostril; nt, notochord; olf.b, olfactory bulb; pha, pharynx.

at the agnathan—gnathostome transition [10,12,13]. Some advances in evolutionary developmental biology might provide molecular insights into the potential impacts of this event on the origin of the diplorhiny. The Hedgehog (Hh) gene family plays a critical role in regulating vertebrate organogenesis and patterning almost every aspect of the vertebrate body plan [41]. A striking aspect of Hh function is its role in establishing cell fates and gene expression patterns characteristic of the ventral midline throughout the neural tube [42]. In mice Shh mutant embryos (Shh/), the normally paired lateral structures such as the telencephalon, the mandibular and maxillary arches, the optic vesicles and the nasal placodes are fused to form a single structure in midline [42,43]. This phenotype is collectively known as holoprosencephaly, which is accompanied by cyclopia, fused single nasal chamber, fused single telencephalic vesicle, and other forebrain and facial midline defects [42,43]. Intriguingly, the fused nasal chamber in Shh mutant mice embryos [43] is reminiscent of the monorhiny in jawless vertebrates. Recently, the previously unreported Hh expression in the nasohypophyseal plate was observed in lampreys [44] (Figure 4). This probably indicates that the molecular mechanism separating the nasal sacs has been established in the common ancestor of lampreys and gnathostomes (Figure 4). In hagfishes and lampreys, the olfactory organs developed from an unpaired placode, the nasohypophyseal plate, but its primordium always has an indication of a median septum [45–47] which separates the olfactory organ into left and right halves [48]. This septum disappears in adult hagfishes, but retains in adult lampreys [13,49]. Therefore, to some extent, the olfacory organs can be regarded as paired,

but closely associated in cyclostomes. In addition, the presence of paired olfactory nerves and bulbs in all living vertebrates also suggests that the presence of paired olfactory organs represents the ancestral vertebrate condition [49]. This condition may have been establshied in such stem vertebrates as the Cambrian myllokunmingiid Haikouichthys [50–52]. If the key players involved in the development of diplorhiny were already recruited in the common ancestor of all vertebrates, it is intriguing to discuss why the monorhinic condition is developed in cyclostomes. The history of the olfactory organ is closely associated with that of the adenohypophysis [12]. In lampreys, the olfactory organs and adenohypophysis develop as a median nasohypophyseal plate. Although the Hh gene family expresses on the whole nasohypophyseal plate [44], the separation of the nasal placodes is probably constrained by the nasohypophyseal complex. Thus, a fused nasal chamber with a single nostril is developed in the midline. Like lampreys, the nasal and hypophyseal placodes of gnathostomes are also located very close to each other at early developmental stages [53], but the nasal placodes are topologically independent from the hypophysis [32]. As discussed previously, this developmental independence has been regarded as a key innovation for patterning the jaw and pituitary organ because it allows the reorganization of premandibular and mandibular ectomesenchyme in the head [6,27] and the reorganization of adenohypophysis in the oral ectoderm [32]. In gnathostomes, Shh is expressed throughout the ventral diencephalon, the oral ectoderm, and nasal placodes, but its expression is subsequently absent from the nascent Rathke’s pouch, creating a Shh boundary within the oral

3824

Gai Z K, et al.

Chin Sci Bull

October (2012) Vol.57 No.30

Figure 4 The disassociation of nasohypophyseal complex and the evolution of jaw, diplorhiny, and pituitary. The previously unreported Hh expression in the nasohypophyseal plate was observed in lampreys [44], probably indicating that the molecular mechanism separating the nasal sacs has been established in the common ancestor of lampreys and gnathostomes, but their separation was possibly precluded by the nasohypophyseal complex in cyclostomes. The separation of olfactory organs from the adenohypophysis is possibly a crucial innovation for the developmental origin of jaw [6,27] and diplorhiny [10,12,13]. Modified from Uchida et al. [32, fig. 8].

epithelium [32,43,54] (Figure 4). In subsequent developmental stages, the paired nasal placodes and the Rathke’s pouch are soon separated from each other. Kawamura and Kikuyama [55] and Gleiberman et al. [56] attributed this fast separation possibly partly to the rostral growth of the part of the brain that vertically induces Rathke’s pouch. Considering that the paired nasal placodes will form a fused nasal chamber in Shh mutant mice embryos [43], here, we suspect that this fast separation possibly has some relationship to the Shh expression on the nasal placodes establishing their lateral positions. If so, the disconnection of the olfactory placodes from the hypophyseal tube might be a key innovation for the Hh gene family to establish the lateral position of nasal sacs before the rise of the diplorhiny, as well as before the origin of the jaw.

4 Intersection with fossil evidence: galeaspid head innovation Compared with the only living jawless vertebrates (hagfishes and lampreys), the extinct jawless ancestors of jawed vertebrates, or ‘ostracoderms’ were diverse and flourishing during the Silurian and Devonian periods [12,57]. These extinct groups have been consistently resolved as the stem

groups of gnathostomes (stem gnathostomes, Figure 1) and provide grounds to establish the sequence in which gnathostome characters appeared [12–15,58–61]. Among these ‘ostracoderms’, the 420–370-million-year-old osteostracans have been regarded as the closest jawless relatives of the gnathostomes (Figure 1) because they share with the latter a number of uniquely derived characters, such as girdle-supported paired fins, cellular perichondral bone, a sclerotic ring and an epicercal tail [12,13]. However, their massive, mineralized braincase has a median nasohypophyseal organ resembling the condition in lampreys. Consequently, osteostracans provide little insight into the evolutionary origin of jaw. Aside from osteostracans, the approximately coeval galeaspids are the only other ‘ostracoderm’ group whose cranial anatomy can conceivably be determined by virtue of the exceptionally preserved mineralized or calcified skull [11,62]. Using synchrotron radiation X-ray tomographic microscopy, we have elucidated the gross cranial anatomy of galeaspids and provided the earliest fossil evidence for the disassociation of nasohypophyseal complex in vertebrate phylogeny [11]. Our results indicate that the paired nasal sacs (na, Figure 5(b)–(e)) of galeaspids are located laterally in the oronasal cavity (on.c, Figure 5(c)), and the hypophyseal duct (hy.d, Figure 5(a)–(c),(e)) opens anteriorly

Gai Z K, et al.

Chin Sci Bull

October (2012) Vol.57 No.30

3825

Figure 5 The cranial anatomy of Shuyu zhejiangensis, a 430-million-year-old jawless fish from Zhejiang, China. The derivative structures of the trabeculae (rostrum, orbitonasal lamina, ethmoid plate) and the relative nervous and vascular canals such as the superficial ophthalmic nerve, profundus nerve, orbitonasal artery, and orbitonasal vein are shown by the synchrotron radiation X-ray tomography and restoration. (a) The 512th of 1024 sagittal slices of V14334.3. (b) Middle sagittal section through the braincase (V14334.3), showing the relationship between the hypophyseal duct and the nasal sacs. (c) Restoration for the endocast of the braincase, ventral view. (d) Virtual endocast of the skull, anterolateral view, reconstructed from V14334.1. (e) 3D reconstruction of ethmoid region, frontal view, reconstructed from V14334.3. ac.v, anterior cerebral vein; ae.a, anterior ethmoidal artery; all, anterior lateral line nerve; ao, dorsal aorta; dn.a, dorsal nasal artery; dn.v, dorsal nasal vein; ebr.a, efferent branchial artery; et.r, ethmoid rod; fr.a, frontal artery; fr.v, frontal vein; hy.r, hypophyseal recess; ic.a, internal carotid artery; mc.a, middle cerebral artery; mc.v, middle cerebral vein; mes, mesencephalic division; met, metencephalic division; olf.t, olfactory tract; on.a, orbitonasal artery; on.c, oronasal cavity; on.l, orbitonasal lamina; on.v, orbitonasal vein; orb, orbital opening; or.c, oral cavity; pe.a, posterior ethmoidal artery; pi, pineal organ; pr.f, precerebral fenestra; ro, rostrum; ter, terminal nerve; vcl, lateral head vein or dorsal jugular vein; II, III, IV, V0, V1, V0,1, V2,3, VI, optic (II), oculomotor (III), trochlear (IV), superficial ophthalmic (V0), profundus (V1), superficial ophthalmic plus profundus (V0,1), maxillomandibular (V2,3) of trigeminal (V), and abducens (VI). See Figure 3 for other abbreviations.

to the oronasal cavity in the middle of the head. Thus, these three structures are independent of each other, as in jawed vertebrates, rather than collocated, like the median nasohypophyseal complex of cyclostomes (hagfishes and lampreys) and osteostracans. Galeaspids, therefore, possessed the condition that current developmental models regard as the prerequisite for the development of jaws. Here, we further describe some derivative structures of the trabeculae (e.g. orbitonasal lamina, ethmoid plate) in galeaspids, which are speculated to be found in some jawless fossil ancestors of jawed vertebrates by the heterotopy theory [27]. Galeaspids are characterized by a large median dorsal opening (no, Figure 5(c)–(e)) in the anterior part of the head

(ethmoid region) that serves as both a common nostril and the main water intake device. In the ethmoid region, the large oval-shaped median dorsal opening is flanked by a pair of scoop-like cartilage for the rostrum (ro, Figure 5(d), (e)). Beneath the median dorsal opening is a large median oronasal cavity (on.c, Figure 5(c)) that opens ventrally to the mouth (m, Figure 3(d)) and caudally towards the pharynx (pha, Figure 3(d)). The nasal sacs (na, Figure 5(e)) are paired, large, cone-shaped, and located lateral to the base of the rostrum in the oronasal cavity. As the paired nasal sacs are located antero-lateral to the orbital cavity (orb, Figure 5(c)–(e)), a pair of large cartilaginous plates for the orbitonasal lamina (on.l, Figure 5(c),(d)) are present between

3826

Gai Z K, et al.

Chin Sci Bull

the nasal sacs and orbital cavities which form the posterolateral walls of nasal sacs and anterior walls of orbital cavities as in gnathostomes. Like gnathostomes, the orbitonasal lamina is penetrated by the diagnostic nervous and vascular canals such as the superficial ophthalmic nerve (V0, Figure 5(c)–(e)), profundus nerve (V1, Figure 5(c)–(e)), orbitonasal artery (on.a, Figure 5(c)–(e)), and orbitonasal vein (on.v, Figure 5(c)–(e)). Medially, the orbitonasal lamina protrudes rostrally into the oronasal cavity as the ethmoid process (et.r, Figure 5(a), (b),(e)). The ethmoid process supports and partly floors the paired olfactory bulbs (olf.b, Figure 5(a)–(c),(e)). Compared to gnathostomes, the ethmoid plate of galeaspids is so small that it does not extend rostrally enough to separate the nasal sacs completely (nasal septum not formed). The rostrum, the orbitonasal lamina and the ethmoid plate are regarded as the main derivative structures of the trabeculae in gnathostomes. Their identification in galeaspids indicates that galeaspids at least partly possessed the gnathostome-like trabeculae. The trabeculae cranii of jawed vertebrates has long been regarded as a major evolutionary advance over agnathans [34]. Although the ‘trabeculae’ of cyclostomes has been reported [63,64], the ‘lamprey trabecula’ surrounds the hypophysis and extends anteriorly to the olfactory capsules. They are lateral rather than anterior to the notochord [65], and probably represent the anterior prolongation of parachordal cartilage [64,66]. The developmental data indicate that the ‘lamprey trabecula’ develops from the mandibular mesoderm, and is not homologous with the gnathostome trabecula, which develops from premandibular neural crest cells [27]. Although the developmental process is impossible to access in fossil jawless vertebrates, the presence of trabeculae cranii can be identified by its derivative structures. The nasohypophysial complex in osteostracans is also separated from the orbits by the cartilage, however this chondrous septum is located medial to the orbits and far behind the mandibular arch, and even the hyoid arch [12,13]. In gnathostomes, all derivative structures of the trabeculae (e.g. orbitonasal lamina, ethmoid plate) are developed from the premandibular neural crest. They are topologically rostral to the mandibular arch which is derived from the mandibular neural crest [6,27]. Therefore, the cartilage enclosing the nasohypophysial complex in osteostracans hardly corresponds to any derivative structures of the trabeculae. It is more likely to be the anterior prolongation of parachordal cartilage as in lampreys. As there is no mineralized or calcified endoskeletal skull preserved in other ‘ostracoderms’, the presence of trabecula remains unclear in these groups. Thus, galeaspids might provide the first evidence for the gnathostome-like trabeculae in jawless fishes. Our result indicates that galeaspids are, in many respects, a better proxy than osteostracans for reconstructing the pre-gnathostome condition of the rostral part of the braincase. Aside from the presence of orbitonasal lamina and

October (2012) Vol.57 No.30

ethmoid plate, galeaspids also share with gnathostomes some uniquely derived characters such as separate olfactory bulbs, independent olfactory tracts, terminal nerves, paired separate nasal sacs, the disassociation of nasohypophyseal complex, and the hypophyseal duct opening to the oral cavity [11,62]. This raises the potential possibility that galeaspids might be the closest jawless relatives of jawed vertebrates (Figure 3), and will add to our understanding of the early evolution of jawed vertebrates.

5 Conclusions (1) Some derivative structures of the trabeculae (e.g. orbitonasal lamina, ethmoid plate) in jawless galeaspids provide new insights into the reorganization of the vertebrate head before the evolutionary origin of the jaw. (2) The paired olfactory organs and the molecular mechanism for the separation of nasal sacs might have been established in the common ancestor of lampreys and gnathostomes, but their separation was probably precluded by the nasohypophyseal complex in cyclostomes. The separation of olfactory organs from the adenohypophysis is possibly a crucial innovation for the Hh gene family to establish the lateral position of nasal sacs before the rise of the diplorhiny. (3) Galeaspids provide the earliest evidence for the clear separation of the olfactory organs from the hypophyseal duct in vertebrate phylogeny, a prerequisite condition in evolutionary developmental models for the origin of the jaw [6,27] and diplorhiny [12,13]. Galeaspids display an intermediate condition in the establishment of diplorhiny and jaw in which the barrier to the forward growth of neuralcrest-derived craniofacial ectomesenchyme was removed. As evidenced by galeaspids, this event happened at least 435 million years ago. (4) No fossil evidence indicates that the diplorhinic condition (nasal sacs with individual externalized nostrils) has been established before the invention of the jaw, but an intermediate condition, paired laterally positioned nasal sacs and independent hypophyseal organ appeared in jawless galeaspids. The complete diplorhiny and the jaw arose later in the lineage leading to the extinct placoderms and the crown-group gnathostomes. (5) Galeaspids are, in many ways, a better proxy than osteostracans for reconstructing the pre-gnathostome condition of the rostral part of the braincase. This raises the potential possibility that galeaspids might be the closest jawless relatives of jawed vertebrates. (6) In absence of any evidence for increasingly active feeding strategies that are commonly invoked to explain the origin of the jawed vertebrates [35,36], galeaspids provide evidence that the assembly of gnathostome characters accrued piecemeal before the origin of the jaw rather than as bursts of innovations.

Gai Z K, et al.

Chin Sci Bull

We thank P. Janvier, P. Donoghue, M. M. Chang, S. Kuratani, J. Maisey, Q. M. Qu and J. H. Xiao for discussions, X. B. Yu and P. Ahlberg for reviewing the manuscript, F. X. Wu for the drawing of Figure 5(c). This work was supported by the National Natural Science Foundation of China (40930208), the National Basic Research Program of China (2012CB821902), the Knowledge Innovation Program of the Chinese Academy of Sciences (KZCX2-YW-156), and the CAS/SAFEA International Partnership Program for Creative Research Teams. 1 2 3 4 5 6

7

8

9

10

11

12

13 14 15 16

17

18 19

20 21 22

Maisey J G. Discovering Fossil Fishes. New York: Henry Holt and Company, 1996. 1–223 Kimmel C B, Miller C T, Keynes R J. Neural crest patterning and the evolution of the jaw. J Anat, 2001, 199: 105–119 Manzanares M, Nieto M A. A celebration of the new head and an evaluation of the new mouth. Neuron, 2003, 37: 895–898 Mallatt J. The origin of the vertebrate jaw: Neoclassical ideas versus newer, development-based ideas. Zool Sci, 2008, 25: 990–998 Nelson J S. Fishes of the World. 4th ed. New York: Wiley, 2006. 1–624 Kuratani S, Nobusada Y, Horigome N, et al. Embryology of the lamprey and evolution of the vertebrate jaw: Insights from molecular and developmental perspectives. Phil Trans R Soc B, 2001, 356: 1615–1632 Heimberg A M, Cowper-Sallari R, Sémon M, et al. MicroRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate. Proc Natl Acad Sci USA, 2010, 107: 19379–19383 Janvier P. MicroRNAs revive old views about jawless vertebrate divergence and evolution. Proc Natl Acad Sci USA, 2010, 107: 19137–19138 Kuratani S, Kuraku S, Murakami Y. Lamprey as an evo-devo model: Lessons from comparative embryology and molecular phylogenetics. Genesis, 2002, 34: 175–183 Janvier P. Homologies and evolutionary transitions in early vertebrate history. In: Anderson J S, Sues H D, eds. Major Transitions in Vertebrate Evolution. Bloomington and Indianapolis: Indiana University Press, 2007. 57–121 Gai Z K, Donoghue P C J, Zhu M, et al. Fossil jawless fish from China foreshadows early jawed vertebrate anatomy. Nature, 2011, 476: 324–327 Janvier P. Ostracoderms and the shaping of the gnathostome characters. In: Ahlberg P, ed. Major Events in Early Vertebrate Evolution: Palaeontology, Phylogeny, Genetics and Development. London: Taylor Francis, 2001. 172–186 Janvier P. Early Vertebrates. Oxford: Clarendon Press, 1996. 1–393 Forey P L. Agnathans recent and fossil, and the origin of jawed vertebrates. Rev Fish Biol Fish, 1995, 5: 267–303 Donoghue P C J, Forey P L, Aldridge R J. Conodont affinity and chordate phylogeny. Biol Rev, 2000, 75: 191–251 Donoghue P C J, Sansom I J, Downs J P. Early evolution of vertebrate skeletal tissues and cellular interactions, and the canalization of skeletal development. J Exp Zool B Mol Dev Evol, 2006, 306: 278–294 Long J A, Brian K H, McNamara K J, et al. The phylogenetic origin of jaws in vertebrates: Developmental plasticity and heterochrony. Kirtlandia, 2010, 57: 46–52 Goette, A. Über die Kiemen der Fische. Z Wiss Zool, 1901, 69: 533–577 Schaeffer B, Thomson K S. Reflections on agnathan-gnathostome relationships. In: Jacobs L L, ed. Aspects of VertebrateHistory: Essays in Honor of Edwin Harris Colbert. Flagstaff: Museum of Northern Arizona Press, 1980. 19–33 Jarvik E. Basic Structure and Evolution of Vertebrates, Volume 1, London: Academic Press, 1980. 1–575 Jarvik E. Basic Structure and Evolution of Vertebrates, Volume 2, London: Academic Press, 1980. 1–337 Mallatt J. Early vertebrate evolution: Pharyngeal structure and the origin of gnathostomes. J Zool, 1984, 204: 169–183

October (2012) Vol.57 No.30

23

24

25

26

27

28 29

30

31 32

33 34 35 36

37

38 39 40 41 42

43 44

45

46

47

3827

Janvier P. Patterns of diversity in the skull of jawless fishes. In: Hanken J, Hall B K, eds. The Skull. Chicago: University of Chicago Press, 1993. 131–188 Janvier P. The phylogeny of the Craniata, with particular reference to the significance of fossil “agnathans”. J Vertebr Paleontol, 1981, 1: 121–159 Mazan S, Jaillard D, Baratte B, et al. Otx1 gene-controlled morphogenesis of the horizontal semicircular canal and the origin of the gnathostome characteristics. Evol Dev, 2000, 2: 186–193 Gegenbaur C. Untersuchungen zur Vergleichenden Anatomie der Wirbeltiere. 3: Das Kopfskelett der Selachier. Leipzig: Englemann, 1872 Kuratani S. Evolution of the vertebrate jaw: Comparative embryology and molecular developmental biology reveal the factors behind evolutionary novelty. J Anat, 2004, 205: 335–347 Kuratani S. Evolution of the vertebrate jaw: Homology and developmental constraints. Paleontol Res, 2003, 7: 89–102 Kuratani S, Murakami Y, Nobusada Y, et al. Developmental fate of the mandibular mesoderm in the lamprey, Lethenteron japonicum: Comparative morphology and development of the gnathostome jaw with special reference to the nature of the trabecula cranii. J Exp Zool B Mol Dev Evol, 2004, 302: 458–468 Shigetani Y, Sugahara F, Kawakami Y, et al. Heterotopic shift of epithelial-mesenchymal interactions in vertebrate jaw evolution. Science, 2002, 296: 1316–1319 Shigetani Y, Sugahara F, Kuratani S. A new evolutionary scenario for the vertebrate jaw. BioEssays, 2005, 27: 331–338 Uchida K, Murakami Y, Kuraku S, et al. Development of the adenohypophysis in the lamprey: Evolution of epigenetic patterning programs in organogenesis. J Exp Zool B Mol Dev Evol, 2003, 300: 32–47 Zhu M, Gai Z K. Phylogenetic relationships of galeaspids (Agnatha). Front Biol China, 2007, 2: 151–169 Maisey J G. Heads and tails: A chordate phylogeny. Cladistics, 1986, 2: 201–256 Gans C, Northcutt R G. Neural crest and the origin of the vertebrates: A new head. Science, 1983, 220: 268–274 Baker C V H, Schlosser G. Editorial: The evolutionary origin of neural crest and placodes. J Exp Zool B Mol Dev Evol, 2005, 304B: 269–273 Kuratani S. Cephalic neural crest cells and the evolution of craniofacial structures in vertebrates: Morphological and embryological significance of the premandibular-mandibular boundary. Zoology, 2005, 108: 13–25 Takio Y, Pasqualetti M, Kuraku S, et al. Lamprey Hox genes and the evolution of jaws. Nature, 2004, 429, doi: 10.1038/nature02616 Cohn M J. Lamprey Hox genes and the origin of jaws. Nature, 2002, 416: 386–387 Depew M J, Lufkin T, Rubenstein J L R. Specification of jaw subdivisions by Dlx genes. Science, 2002, 298: 381–385 Varjosalo M, Taipale J. Hedgehog: Functions and mechanisms. Genes Dev, 2008, 22: 2454–2472 Chiang C, Ying L, Lee E, et al. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature, 1996, 383: 407–413 Cooper M K. Teratogen-mediated inhibition of target tissue response to Shh signaling. Science, 1998, 280: 1603–1607 Kano S, Xiao J H, Osório J, et al. Two lamprey hedgehog genes share non-coding regulatory sequences and expression patterns with gnathostome hedgehogs. PLoS One, 2010, 5: e13332 von Kupffer C. Studien zur Vergleichenden Entwicklungsgeschichte des Kopfes der Kranioten. Heft 4: zur Kopfentwicklung von Bdellostoma. München und Leipzig: Verlag von J. F. Lehmann, 1900. 1–86 Stensiö E A. The cyclostomes with special reference to the diphyletic origin of the Petromyzontida and Myxinoidea. In: Ørvig T, ed. Current Problems of Lower Vertebrate Phylogeney. Nobel Symposium 4, Stockholm: Almqvist & Wiksell, 1968. 13–70 Goodrich E S. Studies on the Structure and Development of Vertebrates. London: Macmillan, 1930

3828 48 49

50 51 52 53

54 55

56

57

Gai Z K, et al.

Chin Sci Bull

Jefferies R P S. The Ancestry of the Vertebrates. London: British Museum (Natural History), 1986 Northcutt R G. The brain and sense organs of the earliest vertebrates: Reconstruction of a morphotype. In: Foreman R, Gorbman A, Dodd J, et al. eds. Evolutionary Biology of Primitive Fishes. New York: Plenum Press, 1985. 81–112 Shu D G, Conway Morris S, Han J, et al. Head and backbone of the Early Cambrian vertebrate Haikouichthys. Nature, 2003, 421: 526–529 Shu D G, Luo H L, Conway Morris S, et al. Lower Cambrian vertebrates from south China. Nature, 1999, 402: 42–46 Janvier P. Vertebrate characters and the Cambrian vertebrates. C R Palevol, 2003, 2: 523–531 Couly G F, Le Douarin N M. Mapping of the early neural primordium in quail-chick chimeras. I. Developmental relationships between placodes, facial ectoderm, and prosencephalon. Dev Biol, 1985, 110: 422–439 Treier M, Shawn O, Anatoli G, et al. Hedgehog signaling is required for pituitary gland development. Development, 2001, 128: 377–386 Kawamura K, Kouki T, Kawahara G, et al. Hypophyseal development in vertebrates from amphibians to mammals. Gen Comp Endocrinol, 2002, 126: 130–135 Gleiberman A S, Fedtsova N G, Rosenfeld M G. Tissue interactions in the induction of anterior pituitary: Role of the ventral diencephalon, mesenchyme, and notochord. Dev Biol, 1999, 213: 340–353 Zhao W J, Zhu M. Diversification and faunal shift of Siluro-Devonian

October (2012) Vol.57 No.30

58 59

60

61 62

63

64 65 66

vertebrates of China. Geol J, 2007, 42: 351–369 Forey P L, Janvier P. Agnathans and the origin of jawed vertebrates. Nature, 1993, 361: 129–134 Janvier P. The dawn of the vertebrates: Characters versus common ascent in the rise of current vertebrate phylogenies. Palaeontology, 1996, 39: 259–287 Donoghue P C J, Smith M P. The anatomy of Turinia pagei (Powrie), and the phylogenetic status of the Thelodonti. Trans R Soc Edinb Earth Sci, 2001, 92: 15–37 Gess R W, Coates M I, Rubidge B S. A lamprey from the Devonian period of South Africa. Nature, 2006, 443: 981–984 Wang N Z. Two new Silurian galeaspids (jawless craniates) from Zhejiang Province, China, with a discussion of galeaspid-gnathostome relationships. In: Chang M M, Liu Y H, Zhang G R, eds. Early Vertebrates and Related Problems of Evolutionary Biology. Beijing: Science Press, 1991. 41–66 Damas H. Recherches sur le développement de Lampetra fluviatilis L. Contribution a l'étude de la céphalogenese de Vertébrés. Arch Biol, 1944, 55: 1–285 Johnels A G. On the development and morphology of the skeleton of the head of Petromyzon. Acta Zool, 1948, 29: 139–279 Jollie M. Chordate Morphology. New York: Reinhold Books, 1962. 1–478 de Beer G R. The Development of the Vertebrate Skull. Oxford: Oxford University Press, 1937

Open Access This article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.

Information for Authors Chinese Science Bulletin (CSB) is a multidisciplinary academic journal supervised by the Chinese Academy of Sciences and co-sponsored by the Chinese Academy of Sciences and National Natural Science Foundation of China. Its mission is to encourage communication of basic and innovative research results of high quality in the fields of natural sciences and high technologies, especially focusing on breakthroughs by the Chinese scientists. All papers should be intelligible for a broad scientific audience. CSB is published three times every month from 2010. Contributions are invited from researchers all over the world. CSB is indexed by Academic Search Alumni Edition, Academic Search Complete, Academic Search Elite, Academic Search Premier, ASFA 1: Biological Sciences and Living Resources, ASFA 2: Ocean Technology, Policy and Non-Living Resources, Biological Abstracts, Biological Sciences, BIOSIS Previews, CAB Abstracts, Chemical Abstracts, Chemical and Earth Sciences, Current Contents/Physical, Current Mathematical Publications, Digital Mathematics Registry, EMBio, Environmental Engineering Abstracts, Environmental Sciences and Pollution Management, Google Scholar, Inspec, Mathematical Reviews, MathSciNet, Meteorological and Geoastrophysical Abstracts, Pollution Abstracts, Science Citation Index, SCOPUS, Water Resources Abstracts, Zentralblatt MATH, Zoological Record. Its impact factor and total citation for 2010 are 1.087 and 6148. 1. Contributions published in CSB include the following: News & Views: Introduce and comment on the research highlights published in CSB and other journals and outstanding work awarded by the national prizes (approximately 1–2 pages). Progress: Introduce and comment on the substantial advance and its importance in the fast-developing areas (approximately 3–4 pages). Review: Summarize the representative progress in core scientific disciplines, comment on the research status, and make suggestions for future work. It should be closely related to or based on the author’s own research work (approximately 6–8 pages, with a 600-word abstract). Frontiers: Comment on excitement and existing problems of hot fields or hot topics, and offer suggestions for future research. The contributions are usually solicited by editor’s invitation. Articles: Originally report the innovative and valuable findings in natural sciences (approximately 4–7 pages, with a 300-word abstract). Letters: Briefly report the novel and innovative findings in natural sciences (approximately 3 pages, with a 300-word abstract). Forum: Comment on the important academic issues, administration policies and state scientific programmes, and give views about the theoretical problems such as the relation between scientific development and social evolution (approximately 3–4 pages, with a 200-word abstract). Correspondence: Discuss and reply to the contributions published in CSB, or introduce and comment on a controversial issue of general interest (approximately 2–3 pages). Trend: Report weighty scientific news, information, and academic affairs, as well as the significant international conferences held in China (approximately 1 page). Book Reviews: Introduce and comment on recent quality monographs of natural sciences (approximately 1 page). 2. Contributions are required of a concise, focused account of the findings and reliable essential data. They should be well organized and written clearly and simply, avoiding exhaustive tables and figures. Authors are advised to use internationally agreed nomenclature, express all measurements in SI units, and quote all the relevant references. 3. Authors are recommended to use our online submission services. To submit a manuscript, please visit www.scichina.com, log on at Journal Management System, get an account, and follow the instructions to upload the text and image/table files. 4. The final decision to accept a contribution for publication will be made by the editorial committee of this journal. If the authors do not receive decision letter after two months, they can submit the contributions for publication elsewhere, except an agreement has been made in advance. Authors are usually informed timely if the contribution is not considered, but their manuscripts will not be returned, except for the photographic material asked to be sent back. 5. Authors of each published article will be presented one sample copy. If more offprints and sample copies are required, please contact the managing editor and pay the extra fee. The full text in Chinese and in © Science China Press and Springer-Verlag Berlin Heidelberg 2010

English opens free to the readers in China at csb.scichina.com, and the full text in English is available to overseas readers at www.springerlink.com. 6. Since the OFC of each issue is designed based on the content of contributions, full colour illustrations or photographs are always welcome. 7. For detailed information concerning online submission, manuscript format, authorship, copyright transfer, etc., please visit www.scichina.com. Subscription information ISSN print edition: 1001-6538 ISSN electronic edition: 1861-9541 Volume 57(36 issues) will appear in 2012 Subscription rates For information on subscription rates please contact: Customer Service China: [email protected] North and South America: [email protected] Outside North and South America: [email protected] Orders and inquiries: China Science China Press 16 Donghuangchenggen North Street, Beijing 100717, China Tel: +86 10 64019709 Fax: +86 10 64016350 Email: [email protected] North and South America Springer New York, Inc. Journal Fulfillment P.O. Box 2485, Secaucus, NJ 07096 USA Tel: 1-800-SPRINGER or 1-201-348-4033 Fax: 1-201-348-4505 Email: [email protected] Outside North and South America Springer Customer Service Center Customer Service Journals Haberstr. 7, 69126 Heidelberg, Germany Tel: +49-6221-345-0, Fax: +49-6221-345-4229 Email: [email protected] Cancellations must be received by September 30 to take effect at the end of the same year. Changes of address: Allow for six weeks for all changes to become effective. All communications should include both old and new addresses (with postal codes) and should be accompanied by a mailing label from a recent issue. According to § 4 Sect. 3 of the German Postal Services Data Protection Regulations, if a subscriber’s address changes, the German Federal Post Office can inform the publisher of the new address even if the subscriber has not submitted a formal application for mail to be forwarded. Subscribers not in agreement with this procedure may send a written complaint to Customer Service Journals, Karin Tiks, within 14 days of publication of this issue. Microform editions are available from: ProQuest. Further information is available at http://www.il.proquest.com/uni. Electronic edition An electronic version is available at springerlink.com. Production Science China Press 16 Donghuangchenggen North Street, Beijing 100717, China Tel: +86 10 64034559 Fax: +86 10 64016350 Printed in the People’s Republic of China Springer-Verlag is part of Springer Science+Business Media Published by: Science China Press and Springer-Verlag Berlin Heidelberg Sole distributor outside Mainland China: Springer csb.scichina.com

www.springerlink.com