Brain structure resolves the segmental affinity of anomalocaridid appendages (original) (raw)
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- Published: 16 July 2014
Nature volume 513, pages 538–542 (2014)Cite this article
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Abstract
Despite being among the most celebrated taxa from Cambrian biotas, anomalocaridids (order Radiodonta) have provoked intense debate about their affinities within the moulting-animal clade that includes Arthropoda. Current alternatives identify anomalocaridids as either stem-group euarthropods1,2,3, crown-group euarthropods near the ancestry of chelicerates4, or a segmented ecdysozoan lineage with convergent similarity to arthropods in appendage construction5. Determining unambiguous affinities has been impeded by uncertainties about the segmental affiliation of anomalocaridid frontal appendages. These structures are variably homologized with jointed appendages of the second (deutocerebral) head segment, including antennae and ‘great appendages’ of Cambrian arthropods, or with the paired antenniform frontal appendages of living Onychophora and some Cambrian lobopodians. Here we describe Lyrarapax unguispinus, a new anomalocaridid from the early Cambrian Chengjiang biota, southwest China, nearly complete specimens of which preserve traces of muscles, digestive tract and brain. The traces of brain provide the first direct evidence for the segmental composition of the anomalocaridid head and its appendicular organization. Carbon-rich areas in the head resolve paired pre-protocerebral ganglia at the origin of paired frontal appendages. The ganglia connect to areas indicative of a bilateral pre-oral brain that receives projections from the eyestalk neuropils and compound retina. The dorsal, segmented brain of L. unguispinus reinforces an alliance between anomalocaridids and arthropods rather than cycloneuralians. Correspondences in brain organization between anomalocaridids and Onychophora resolve pre-protocerebral ganglia, associated with pre-ocular frontal appendages, as characters of the last common ancestor of euarthropods and onychophorans. A position of Radiodonta on the euarthropod stem-lineage implies the transformation of frontal appendages to another structure in crown-group euarthropods, with gene expression and neuroanatomy providing strong evidence that the paired, pre-oral labrum is the remnant of paired frontal appendages1.
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This published work and the nomenclatural acts it contains have been deposited in ZooBank under accession number http://zoobank.org/urn:lsid:zoobank.org:pub:189DCAFF-0DD6-49C2-BE80-E999DDF059C1.
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Acknowledgements
This work was supported by the National Natural Science Foundation of China (U1302232, 41372031 and 40962001), a Leverhulme Trust Research Project Grant (F/00 696/T), by the Center for Insect Science, University of Arizona, and by a grant from the Air Force Research Laboratory (FA86511010001) to N.J.S. We thank T. Goral for assistance with energy dispersive X-ray spectroscopy. We acknowledge A. Daley’s advice about anomalocaridid anatomy.
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Authors and Affiliations
- Yunnan Key Laboratory for Palaeobiology, Yunnan University, Kunming, 650091, China
Peiyun Cong, Xiaoya Ma & Xianguang Hou - Department of Earth Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK,
Xiaoya Ma & Gregory D. Edgecombe - Department of Neuroscience, University of Arizona, Tucson, 85721, Arizona, USA
Nicholas J. Strausfeld - Center for Insect Science, University of Arizona, Tucson, 85721, Arizona, USA
Nicholas J. Strausfeld
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- Peiyun Cong
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Fossil data were analysed by all authors, all of whom contributed to the text.
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Correspondence toXianguang Hou or Nicholas J. Strausfeld.
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Extended data figures and tables
Extended Data Figure 1 Comparison of frontal appendages of Lyrarapax and Amplectobelua.
a, L. unguispinus, YKLP 13304a. b–d, Immature specimens of A. symbrachiata. Scale bars: a, 2.5 mm; b–d, 2 mm.
Extended Data Figure 2 Eyes of L. unguispinus and onychophoran brain.
a, Horizontal aspect of right eye of YKLP 13304b. The fracture plane has exposed radiating reliefs suggestive of rhabdomeres (rh) in a clear zone that terminate as pale bases (rhb) within a darker area interpreted as pigment withdrawn to level of basement membrane (bm) lying above paler bluish areas corresponding to expected locations of optic neuropil (opn). Occasional lenses (le) are resolved. b, Inset of same eye in the counterpart of YKLP 13304a, reversed for direct comparison with the part, radiating reliefs arrowed (rh). c, Cartoon of a, depicting identified components in a and b. d, Left eye of YKLP 13304b, with profiles (arrowed) suggestive of lenses. Scale bars: c, 0.5 mm; d, 0.5 mm. e, Frontal ganglion (frg) of E. rowelli (Onychophora) showing its supply by frontal appendage nerve (fan). Lateral protocerebrum, lpr; optic tract, opt. Scale bars: a–c, 200 μm; d, 500 μm; e, 100 μm.
Extended Data Figure 3 L. unguispinus.
a, Dorsal view of whole specimen YKLP 13306a with intact head shield (hs), eyestalks (eys), neck (ne) and eight exposed trunk segments. Rectangles refer to insets b–h. b, Right eyestalk and retina (re). c, Enlargement of the ‘shoulder’ (sh) of greatly extended flap (fl) from first trunk segment. d, Flaps of trunk segments 6 and 7 with enlargement (in e) to show setal blades (sb) and muscle (m). f, Head shield showing characteristic oval anterior margin. g, left eye stalk (eys) of counterpart (YKLP13306b) showing brown corneal layer (o) overlying darker photoreceptor layer. Scale bars: a, 2 cm; b, 3 mm; c–g, 1 cm.
Extended Data Figure 4 Relationships of Radiodonta.
Strict consensus of 108 shortest cladograms (96 steps) under equal character weights, based on modified data set from ref. 6 (Supplementary Information).
Supplementary information
Supplementary Information
This file contains details of specimen preservation, morphological description of specimens, description of phylogenetic analysis, and supplementary references. This file was replaced on 21 July 2014. (PDF 247 kb)
Supplementary Data
Dataset of characters for phylogenetic analysis in Nexus format (editable in Mesquite or NDE). (TXT 11 kb)
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Cong, P., Ma, X., Hou, X. et al. Brain structure resolves the segmental affinity of anomalocaridid appendages.Nature 513, 538–542 (2014). https://doi.org/10.1038/nature13486
- Received: 03 April 2014
- Accepted: 16 May 2014
- Published: 16 July 2014
- Issue Date: 25 September 2014
- DOI: https://doi.org/10.1038/nature13486
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Editorial Summary
Neuroanatomy of arthropod lineage
The anomalocaridids were a successful group of predators found in the Cambrian oceans. Their long, grasping claws have been a focus of particular interest, partly because it has proved difficult to equate them with any extant arthropod appendage. The discovery of near-complete specimens of a new anomalocaridid species with well-preserved traces of brain structure has provided Gregory Edgecombe and colleagues with the opportunity to map the correspondences between appendages and their innervation in unprecedented detail. They conclude that the anomalocaridids' paired appendages were associated with the type of brain recognized today in velvet worms (Onychophora), segmented terrestrial animals also equipped with frontal appendages and representing an ancient group of moulting animals that appeared before the evolution of jointed limbs.