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Specialized appendages in fuxianhuiids and the head organization of early euarthropods

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Abstract

The organization of the head provides critical data for resolving the phylogenetic relationships and evolutionary history of extinct and extant euarthropods1,2. The early Cambrian-period fuxianhuiids are regarded as basal representatives of stem-group Euarthropoda3,4,5,6,7, and their anterior morphology therefore offers key insights for reconstructing the ancestral condition of the euarthropod head1,2,3,8,9,10,11. However, the paired post-antennal structures in Fuxianhuia protensa remain controversial3,8,10; they have been interpreted as both ‘great appendages’1,2 and as gut diverticulae4,12,13. Here we describe Chengjiangocaris kunmingensis sp. nov. and Fuxianhuia xiaoshibaensis sp. nov. from a new early Cambrian (Stage 3) fossil Lagerstätte in Yunnan, China. Numerous specimens of both species show a unique ‘taphonomic dissection’ of the anterodorsal head shield, revealing the cephalic organization in detail. We demonstrate the presence of a pair of specialized post-antennal appendages (SPAs) in the fuxianhuiid head, which attach at either side of the posteriorly directed mouth, behind the hypostome. Preserved functional articulations indicate a well-defined but restricted range of limb movement, suggestive of a simple type of sweep feeding. The organization of the SPAs in fuxianhuiids is incompatible with the (deutocerebral) anterior raptorial appendages of megacheirans2,9,14,15, and argue against the presence of protocerebral limbs in the fuxianhuiids1,2,9. The positions of the fuxianhuiid antennae and SPAs indicate that they are segmentally homologous to the deutocerebral and tritocerebral appendages of crown-group Euarthropoda respectively2,11,16,17. These findings indicate that antenniform deutocerebral appendages with many podomeres are a plesiomorphic feature of the ancestral euarthropod head.

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Figure 1: Chengjiangocaris kunmingensis from the early Cambrian (Canglangpuan) Hongjingshao Formation, Yunnan, China.
Figure 2: Fuxianhuia xiaoshibaensis from the early Cambrian (Canglangpuan) Hongjingshao Formation, Yunnan, China.
Figure 3: Reconstruction of Chengjiangocaris kunmingensis.

References

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

    Article  CAS  ADS  Google Scholar 

  2. 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 

  3. Chen, J.-Y., Edgecombe, G. D., Ramsköld, L. & Zhou, G.-Q. Head segmentation in early Cambrian Fuxianhuia: implications for arthropod evolution. Science 268, 1339–1343 (1995)

    Article  CAS  ADS  Google Scholar 

  4. Waloszek, D., Chen, J., Maas, A. & Wang, W. Early Cambrian arthropods—new insights into arthropod head and structural evolution. Arthropod Struct. Dev. 34, 189–205 (2005)

    Article  Google Scholar 

  5. Waloszek, D., Maas, A., Chen, J. & Stein, M. Evolution of cephalic feeding structures and the phylogeny of Arthropoda. Palaeogeogr. Palaeoclimatol. Palaeoecol. 254, 273–287 (2007)

    Article  Google Scholar 

  6. 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)

    Article  CAS  ADS  Google Scholar 

  7. Budd, G. E. & Telford, M. J. The origin and evolution of arthropods. Nature 457, 812–817 (2009)

    Article  CAS  ADS  Google Scholar 

  8. Hou, X.-G. & Bergström, J. Arthropods of the Lower Cambrian Chengjiang fauna, southwest China. Fossils and Strata, No. 45, 1–116 (Wiley, 1997)

    Google Scholar 

  9. Scholtz, G. & Edgecombe, G. D. In Crustacea and Arthropod Relationships (Crustacean Issues) (eds Koenemann, S. & Jenner, R.A.) 139–165 (CRC Press, 2005)

    Book  Google Scholar 

  10. Budd, G. E. Head structure in upper stem-group euarthropods. Palaeontology 51, 561–573 (2008)

    Article  Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

  12. Bergström, J., Hou, X. G., Zhang, X.-G., Liu, Y. & Clausen, S. A new view of the Cambrian arthropod Fuxianhuia. Geologiska Föreningen 130, 189–201 (2008)

    Google Scholar 

  13. 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 

  14. Chen, J.-Y., Waloszek, D. & Maas, A. A new ‘great-appendage’ arthropod from the Lower Cambrian of China and homology of chelicerate chelicerae and raptorial antero-ventral appendages. Lethaia 15, 3–20 (2004)

    Google Scholar 

  15. 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 

  16. Mittmann, B. & Scholtz, G. Development of the nervous system in the “head” of Limulus polyphemus (Chelicerata, Xiphosura): morphological evidence for a correspondence between the segments of the chelicerae and of the (first) antennae of Mandibulata. Dev. Genes Evol. 213, 9–17 (2003)

    PubMed  Google Scholar 

  17. Harzsch, S., Wildt, M., Battelle, B. & Waloszek, D. Immunohistochemical localization of neurotransmitters in the nervous system of larval Limulus polyphemus (Chelicerata, Xiphosura): evidence for a conserved protocerebral architecture in Euarthropoda. Arthropod Struct. Dev. 34, 327–342 (2005)

    Article  CAS  Google Scholar 

  18. Eriksson, B. J., Tait, N. N., Budd, G. E., Janssen, R. & Akam, M. Head patterning and Hox gene expression in an onychophoran and its implications for the arthropod head problem. Dev. Genes Evol. 220, 117–122 (2010)

    Article  Google Scholar 

  19. Liu, J. et al. An armoured Cambrian lobopodian from China with arthropod-like appendages. Nature 470, 526–530 (2011)

    Article  CAS  ADS  Google Scholar 

  20. Hou, X. G. et al. The Cambrian Fossils of Chengjiang, China: the Flowering of Early Animal Life (Blackwell Publishing, 2004)

  21. Harzsch, S. & Waloszek, D. Serotonin-immunoreactive neurons in the ventral nerve cord of Crustacea: a character to study aspects of arthropod phylogeny. Arthropod Struct. Dev. 29, 307–322 (2000)

    Article  CAS  Google Scholar 

  22. Olesen, J. Phylogeny of Branchiopoda (Crustacea)—character evolution and contribution of uniquely preserved fossil. Arthropod Syst. Phyl. 67, 3–39 (2009)

    Google Scholar 

  23. Liu, Y., Maas, A. & Waloszek, D. Early development of the anterior body region of the grey widow spider Latrodectus geometricus Koch, 1841 (Theridiidae, Araneae). Arthropod Struct. Dev. 38, 401–416 (2009)

    Article  Google Scholar 

  24. Liu, Y., Maas, A. & Waloszek, D. Early development of the head region of Gryllus assimilis Fabricius, 1775 (Orthopera, Insecta). Arthropod Struct. Dev. 39, 382–395 (2010)

    Article  Google Scholar 

  25. Popadíc, A., Panganiban, D. R., Shear, W. A. & Kaufman, T. C. Molecular evidence for the gnathobasic derivation of arthropod mandibles and for the appendicular origin of the labrum and other structures. Dev. Genes Evol. 208, 142–150 (1998)

    Article  Google Scholar 

  26. Posnien, N. F., Bashasab, F. & Bucher, G. The insect upper lip (labrum) is a non-segmental appendage-like structure. Evol. Dev. 11, 440–488 (2009)

    Article  Google Scholar 

  27. Bitsch, J. & Bitsch, C. The tritocerebrum and the clypeolabrum in mandibulate arthropods: segmental interpretation. Acta Zool. 91, 249–266 (2010)

    Article  Google Scholar 

  28. Steinmetz, P. R. H. et al. Six3 demarcates the anterior-most developing brain region in bilaterian animals. Evodevo 1, 14 (2010)

    Article  Google Scholar 

  29. Legg, D. A., Sutton, M. D., Edgecombe, G. D. & Caron, J.-B. Cambrian bivalved arthropod reveals origin of arthrodization. Proc. R. Soc. B 279, 4699–4704 (2012)

    Article  Google Scholar 

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Acknowledgements

This study is supported by the National Natural Science Foundation of China (41272027), and the PhD Fund of the Ministry of Education of China (20115301110005). J.O.-H. is funded by CONACYT (Consejo Nacional de Ciencia y Tecnología, México), the University of Cambridge Trusts and Darwin College, University of Cambridge. We thank C. Shen, T. Lan and J.-B Hou for assistance in the field.

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Author Contributions The LSID urn:lsid:zoobank.org:pub:B3E00449-6531-4B15-9A36-411C10F1B466 has been deposited in ZooBank. J.Y. discovered the fossil localities, and collected and prepared all the material. J.O.-H. wrote the manuscript with input from the other authors. N.J.B. and X.-g.Z. designed the research.

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Correspondence to Xi-guang Zhang.

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Yang, J., Ortega-Hernández, J., Butterfield, N. et al. Specialized appendages in fuxianhuiids and the head organization of early euarthropods. Nature 494, 468–471 (2013). https://doi.org/10.1038/nature11874

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