Fuxianhuiid Ventral Nerve Cord and Early Nervous System Evolution in Panarthropoda
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Fuxianhuiid ventral nerve cord and early nervous system evolution in Panarthropoda Jie Yanga, Javier Ortega-Hernándezb,1, Nicholas J. Butterfieldb, Yu Liua,c,d, George S. Boyanc, Jin-bo Houa, Tian Lane, and Xi-guang Zhanga,2 aYunnan Key Laboratory for Paleobiology, Yunnan University, Kunming 650091, China; bDepartment of Earth Sciences, University of Cambridge, Cambridge CB2 3EQ, United Kingdom; cDevelopmental Neurobiology Group, Biocenter, Ludwig-Maximilians-Universität, 82152 Martinsried, Germany; dGeoBio-Center Ludwig-Maximilians-Universität, Munich 80333, Germany; and eCollege of Resources and Environmental Engineering, Guizhou University, Guiyang 550003, China Edited by Gregory D. Edgecombe, The Natural History Museum, London, United Kingdom, and accepted by the Editorial Board January 29, 2016 (received for review November 14, 2015) Panarthropods are typified by disparate grades of neurological feature as the VNC. This interpretation is supported by com- organization reflecting a complex evolutionary history. The fossil parisons with other preserved components of the internal anat- record offers a unique opportunity to reconstruct early character omy. For instance, the VNC can be readily distinguished from evolution of the nervous system via exceptional preservation in the digestive tract of C. kunmingensis, which is expressed as a extinct representatives. Here we describe the neurological archi- comparatively larger (maximum width, ∼860 μm) but fully tecture of the ventral nerve cord (VNC) in the upper-stem group compressed, linear structure running almost the entire length of euarthropod Chengjiangocaris kunmingensis from the early Cam- the animal (23, figure 1 d and e). The VNC extends from at least brian Xiaoshiba Lagerstätte (South China). The VNC of C. kunmin- the five anteriormost reduced trunk tergites (i.e., dorsal exo- gensis comprises a homonymous series of condensed ganglia that skeletal plates) to tergite T23 at the posterior end of the trunk extend throughout the body, each associated with a pair of bi- (Figs. 1 and 2 and Figs. S1, S2, and S3). Although the VNC ramous limbs. Submillimetric preservation reveals numerous seg- would have continued into the head region in life, our material mental and intersegmental nerve roots emerging from both sides does not preserve any anterior neurological structures that have of the VNC, which correspond topologically to the peripheral been previously identified as the dorsal brain or nerves leading to nerves of extant Priapulida and Onychophora. The fuxianhuiid the antennae and specialized postantennal appendages (8). The VNC indicates that ancestral neurological features of Ecdysozoa absence of fossilized brains in these otherwise exceptionally persisted into derived members of stem-group Euarthropoda but preserved specimens can be attributed to the small sample size were later lost in crown-group representatives. These findings il- and moderate postmortem disarticulation; likewise, other studies luminate the VNC ground pattern in Panarthropoda and suggest addressing neurological structures in Cambrian fossils rarely the independent secondary loss of cycloneuralian-like neurological report the CNS preserved in its entirety (8–11). The VNC also characters in Tardigrada and Euarthropoda. expresses a distinctive dark/light color banding throughout its length, with the dark bands varying from black to reddish-brown stem-group Euarthropoda | Onychophora | phylogeny | Cambrian Explosion | Xiaoshiba Lagerstätte Significance he nervous system represents a critical source of phylogenetic Understanding the evolution of the CNS is fundamental for Tinformation and has been used extensively for exploring the resolving the phylogenetic relationships within Panarthropoda evolutionary relationships of extant Panarthropoda (i.e., Ony- – (Euarthropoda, Tardigrada, Onychophora). The ground pattern chophora, Tardigrada, Euarthropoda) (1 7). Identification of of the panarthropod CNS remains elusive, however, as there is fossilized nervous tissues has provided a unique perspective on uncertainty on which neurological characters can be regarded early euarthropod brain neuroanatomy and suggests that broad as ancestral among extant phyla. Here we describe the ventral patterns of extant neurological diversity were already in place by – nerve cord (VNC) in Chengjiangocaris kunmingensis, an early the Cambrian (8 11). The ventral nerve cord (VNC) reflects Cambrian euarthropod from South China. The VNC reveals fundamental aspects of panarthropod body organization that extraordinary detail, including condensed ganglia and regu- complement the organization of the brain and together illuminate – – larly spaced nerve roots that correspond topologically to the the evolution of the CNS (1 3, 5, 7, 12 16). The early evolutionary peripheral nerves of Priapulida and Onychophora. Our findings history of the panarthropod postcephalic CNS, however, remains demonstrate the persistence of ancestral neurological features obscure due to the exclusive preservation of brains in most available of Ecdysozoa in early euarthropods and help to reconstruct the fossils (8, 10, 11). Moreover, the unresolved phylogenetic relation- VNC ground pattern in Panarthropoda. ships within Panarthropoda complicate accurate reconstruction of – the CNS ground pattern (16 22). In this study, we demonstrate the Author contributions: J.Y., N.J.B., and X.-g.Z. designed research; J.Y., J.O.-H., N.J.B., Y.L., exceptional preservation of postcephalic neurological features in the J.-b.H., T.L., and X.-g.Z. performed research; Y.L. and G.S.B. contributed new reagents/ early Cambrian fuxianhuiid Chengjiangocaris kunmingensis,anup- analytic tools; J.O.-H. analyzed data; J.O.-H. and N.J.B. wrote the paper; J.Y. collected and per stem-group euarthropod (17) from the Xiaoshiba Lagerstätte, prepared all the fossil material; J.O.-H. performed light photography; N.J.B. and X.-g.Z. discussed and approved the manuscript; Y.L. and G.S.B. performed immunohistochemistry South China (23). These fossils clarify the neurological organization and living animal microscopy; and J.-b.H. and T.L. collected fossil material and of the VNC in early euarthropod ancestors, thereby polarizing the performed photography. evolution of the panarthropod CNS. The authors declare no conflict of interest. This article is a PNAS Direct Submission. G.D.E. is a guest editor invited by the Editorial Results Board. Five individuals of C. kunmingensis display a narrow (maximum 1Present address: Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, width, ∼170 μm) and slightly convex rope-like structure with a United Kingdom. metameric pattern that extends medially throughout the body 2To whom correspondence should be addressed. Email: [email protected]. (Figs. 1 and 2, Figs. S1 and S2, and Table S1); its segmental This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. organization and position at the ventral midline identifies this 1073/pnas.1522434113/-/DCSupplemental. 2988–2993 | PNAS | March 15, 2016 | vol. 113 | no. 11 www.pnas.org/cgi/doi/10.1073/pnas.1522434113 Downloaded by guest on September 23, 2021 Fig. 1. VNC in C. kunmingensis. Anterior at top. (A) YKLP 12023 (Holotype), complete specimen preserved in dorsal view with taphonomically dissected head shield (hs) showing internal organization of anterior region. (B) YKLP 12324, complete specimen preserved in dorsolateral view showing preserved VNC extending throughout the almost the entire length of the body. (C) YKLP 12324, magnification of VNC on the anterior trunk region showing the differential preservation of the condensed ganglia (ga) and longitudinal connectives (cn) as dark and light colored bands, respectively, and one-to-one correspondence between the ganglia and the walking legs (wl) (upper box in B). (D) YKLP 12024, magnification of the VNC on the posterior trunk region showing the progressive reduction of size of the ganglia and connectives toward the rear end of the body (lower box in B). Dotted lines highlight the anterior and posterior tergal borders of T15 for comparative purposes with the number of preserved ganglia. ant, antennae; SPA, specialized postantennal appendage; Tn, trunk tergites. between specimens (Figs. 1 and 2 and Figs. S1 and S2C); this remain separate throughout the entire VNC, with no indication variability in color reflects differences in the extent of weathering of fusion or specialization. There is a progressive reduction in between individual specimens. Raman spectroscopy indicates the the size of individual ganglia along the body, with the anterior- presence of residual organic carbon associated with the dark- most being ∼3 times longer and 1.5 times wider than the pos- colored bands (Fig. S4) but not in the light ones, likely mirroring terior ones (Fig. 1 C and D). The preserved proximal portions of differences in their original histology and early diagenesis. In the trunk endopods indicate that each ganglion was associated addition to the carbonaceous films, the VNC is typified by with a single pair of biramous appendages (Fig. 1C and Fig. S2 A modest relief relative to adjacent exoskeletal features, attesting and B), which, like the ganglia, become progressively smaller to a degree of early diagenetic permineralization before com- posteriorly (Fig. 1D). As such, each of the five anteriormost plete degradational collapse (24). reduced tergites (Fig. 1A) correlates with an individual ganglion Neurologically, the C. kunmingensis VNC