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Brain structure resolves the segmental affinity of anomalocaridid appendages

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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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Figure 1: L. unguispinus from the Chengjiang Lagerstätte.
Figure 2: L. unguispinus.
Figure 3: Comparison of onychophoran and L. unguispinus brain.
Figure 4: Evolutionary shift of frontal appendage and its ganglia.

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Data deposits

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.

References

  1. 1

    Budd, G. E. A palaeontological solution to the arthropod head problem. Nature 417, 271–275 (2002)

    ADS  CAS  Article  Google Scholar 

  2. 2

    Daley, A. C., Budd, G. E., Caron, J.-B., Edgecombe, G. D. & Collins, D. The Burgess Shale anomalocaridid Hurdia and its significance for early euarthropod evolution. Science 323, 1597–1600 (2009)

    ADS  CAS  Article  Google Scholar 

  3. 3

    Legg, D. A., Sutton, M. D. & Edgecombe, G. D. Arthropod fossil data increase congruence of morphological and molecular phylogenies. Nature Commun. 4, 2485 (2013)

    ADS  Article  Google Scholar 

  4. 4

    Haug, J. T., Waloszek, D., Maas, A., Liu, Y. & Haug, C. Functional morphology, ontogeny and evolution of mantis shrimp-like predators in the Cambrian. Palaeontology 55, 369–399 (2012)

    Article  Google Scholar 

  5. 5

    Hou, X. & Bergström, J. in Originations, Radiations and Biodiversity Changes: Evidences from the Chinese Fossil Record (eds Rong, J. et al.) 139–158, 847–850 (Science Press, 2006)

    Google Scholar 

  6. 6

    Vinther, J., Stein, M., Longrich, N. R. & Harper, D. A. T. A suspension-feeding anomalocarid from the Early Cambrian. Nature 507, 496–499 (2014)

    ADS  CAS  Article  Google Scholar 

  7. 7

    Daley, A. C. & Edgecombe, G. D. Morphology of Anomalocaris canadensis from the Burgess Shale. J. Paleontol. 88, 68–91 (2014)

    Article  Google Scholar 

  8. 8

    Daley, A. C. & Bergström, J. The oral cone of Anomalocaris is not a classic “peytoia”. Naturwissenschaften 99, 501–504 (2012)

    ADS  CAS  Article  Google Scholar 

  9. 9

    Paterson, J. R. et al. Acute vision in the giant Cambrian predator Anomalocaris and the origin of compound eyes. Nature 480, 237–240 (2011)

    ADS  CAS  Article  Google Scholar 

  10. 10

    Budd, G. E. Arthropod body-plan evolution in the Cambrian with an example from anomalocaridid muscle. Lethaia 31, 197–210 (1998)

    Article  Google Scholar 

  11. 11

    Ma, X., Hou, X., Edgecombe, G. D. & Strausfeld, N. J. Complex brain and optic lobes in an early Cambrian arthropod. Nature 490, 258–261 (2012)

    ADS  CAS  Article  Google Scholar 

  12. 12

    Tanaka, G., Hou, X., Ma, X., Edgecombe, G. D. & Strausfeld, N. J. Chelicerate neural ground pattern in a Cambrian great appendage arthropod. Nature 17, 364–367 (2013)

    ADS  Article  Google Scholar 

  13. 13

    Schürmann, F.-W. in Arthropod Brain: Its Evolution, Development, Structure and Function (ed. Gupta A. P. ) 159–180 (John Wiley, 1987)

    Google Scholar 

  14. 14

    Mayer, G. & Whitington, P. M. Neural development in Onychophora (velvet worms) suggests a step-wise evolution of segmentation in the nervous system of Panarthropoda. Dev. Biol. 335, 263–275 (2009)

    CAS  Article  Google Scholar 

  15. 15

    Mayer, G. & Harzsch, S. Distribution of serotonin in the trunk of Metaperipatus blainvillei (Onychophora, Peripatopsidae): implications for the evolution of the nervous system in Arthropoda. J. Comp. Neurol. 507, 1196–1208 (2008)

    Article  Google Scholar 

  16. 16

    Eriksson, B. J., Tait, N. N., Budd, G. E. & Akam, M. The involvement of engrailed and wingless during segmentation in the onychophoran Euperipatoides kanangrensis (Peripatopsidae: Onychophora) (Reid 1996). Dev. Genes Evol. 219, 249–264 (2009)

    Article  Google Scholar 

  17. 17

    Strausfeld, N. J., Strausfeld, C. M., Stowe, S., Rowell, D. & Loesel, R. The organization and evolutionary implications of neuropils and their neurons in the brain of the onychophoran Euperipatoides rowelli . Arthropod Struct. Dev. 35, 169–196 (2006)

    CAS  Article  Google Scholar 

  18. 18

    Mayer, G., Whitington, P. M., Sunnucks, P. & Pflüger, H. J. A revision of brain composition in Onychophora (velvet worms) suggests that the tritocerebrum evolved in arthropods. BMC Evol. Biol. 10, 255 (2010)

    Article  Google Scholar 

  19. 19

    Wigglesworth, V. B. The use of osmium in the fixation and staining of tissue. Proc. R. Soc. Lond. B 147, 185–199 (1957)

    ADS  CAS  Article  Google Scholar 

  20. 20

    Strausfeld, N. J., Strausfeld, C. M., Loesel, R., Rowell, D. & Stowe, S. Arthropod phylogeny: onychophoran brain organization suggests an archaic relationship with a chelicerate stem lineage. Proc. R. Soc. B 273, 1857–1866 (2006)

    Article  Google Scholar 

  21. 21

    Boxshall, G. A. The evolution of arthropod limbs. Biol. Rev. Camb. Philos. Soc. 79, 253–300 (2004)

    Article  Google Scholar 

  22. 22

    Scholtz, G. & Edgecombe, G. D. The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence. Dev. Genes Evol. 216, 395–415 (2006)

    Article  Google Scholar 

  23. 23

    Stein, M. A new arthropod from the Early Cambrian of north Greenland, with a ‘great appendage’-like antennula. Zool. J. Linn. Soc. 158, 477–500 (2010)

    Article  Google Scholar 

  24. 24

    Legg, D. A. & Vannier, J. The affinities of the cosmopolitan arthropod Isoxys and its implications for the origin of arthropods. Lethaia 46, 540–550 (2013)

    Article  Google Scholar 

  25. 25

    Browne, W. E., Price, A. L., Gerberding, M. & Patel, N. H. Stages of embryonic development in the amphipod crustacean, Parhyale hawaiensis . Genesis 42, 124–149 (2005)

    Article  Google Scholar 

  26. 26

    Haas, M. S., Brown, S. J. & Beeman, R. W. Homeotic evidence for the appendicular origin of the labrum in Tribolium castaneum . Dev. Genes Evol. 211, 96–102 (2001)

    CAS  Article  Google Scholar 

  27. 27

    Boyan, G. S., Williams, J. L. D., Posser, S. & Braunig, P. Morphological and molecular data argue for the labrum being non-apical, articulated, and the appendage of the intercalary segment in the locust. Arthropod Struct. Dev. 31, 65–76 (2002)

    CAS  Article  Google Scholar 

  28. 28

    Strausfeld, N. J. Arthropod Brains: Evolution, Functional Elegance, and Historical Significance Ch 9, 427–446 (Belknap, 2012)

    Google Scholar 

Download references

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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Fossil data were analysed by all authors, all of whom contributed to the text.

Corresponding authors

Correspondence to Xianguang Hou or Nicholas J. Strausfeld.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Comparison of frontal appendages of Lyrarapax and Amplectobelua.

a, L. unguispinus, YKLP 13304a. bd, Immature specimens of A. symbrachiata. Scale bars: a, 2.5 mm; bd, 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: ac, 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 bh. 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; cg, 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

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