Advertisement

Naturwissenschaften

, Volume 101, Issue 12, pp 1065–1073 | Cite as

Sanctacaris uncata: the oldest chelicerate (Arthropoda)

  • David A. Legg
Original Paper

Abstract

The morphology of the arthropod Sanctacaris uncata, from the Middle Cambrian Burgess Shale of Canada, is reinterpreted based on a restudy of previously described material. Although originally considered a chelicerate-like arthropod, these affinities were dismissed based primarily on interpretations of the anterior appendages and hypotheses which considered the megacheirans (‘great-appendage’ arthropods) as putative ancestors of chelicerates. The similarities between megacheirans and chelicerates appear to be overstated however, and this study instead reaffirms the identity of putative chelicerate feature in S. uncata and similar arthropods such as Sidneyia and Emeraldella, both also from the Middle Cambrian Burgess Shale. Newly interpreted features, including the presence of pediform exites, multi-partite trunk exopods, and a trunk differentiated into an anterior limb-bearing area and a differentiated posterior limbless abdomen, were coded into an extensive phylogenetic data set of fossil and recent arthropods. In all analyses, Sanctacaris resolved as the basal-most member of total-group Euchelicerata (the least inclusive group including horseshoe crabs and arachnids but not pycnogonids), thus making it the oldest chelicerate in the fossil record. The vicissicaudates (including Sidneyia, Emeraldella, aglaspidids, and cheloniellids—all of which have previously been allied to chelicerates) resolved as sister-taxon to crown-group Chelicerata. This topology indicates that many purported chelicerate features, such as lamellar gills, and a differentiated posterior abdomen evolved sequentially in the chelicerate stem-lineage.

Keywords

Burgess Shale Cambrian Artiopoda Chelicerata Megacheira Book-gills 

Notes

Acknowledgments

Thanks go to J.-B. Caron and P. Fenton, both at the Royal Ontario Museum, Toronto (ROM), for access to material in their care. Thanks also to Nicola Woods (ROM) for providing additional photographs of Sanctacaris uncata, J. Lamsdell (Yale Peabody Museum) for providing additional photos of Sidneyia inexpectans, G. Edgecombe (Natural History Museum, London) and J. Dunlop (Museum für Naturkunde, Berlin) for the comments on an earlier version of this manuscript and X. Ma (NHM, London) and J. Ortega-Hernández for the critical discussion.

Supplementary material

114_2014_1245_MOESM1_ESM.docx (89 kb)
ESM 1 (DOCX 88 kb)
114_2014_1245_MOESM2_ESM.docx (903 kb)
Supplementary figure 1 (DOCX 903 kb)

References

  1. Bergström J, Hou X-G (2003) Arthropod origins. Bull Geosci 78:323–334Google Scholar
  2. Bousfield EL (1995) A contribution to the natural classification of Lower and Middle Cambrian arthropods: food-gathering and feeding mechanism. Amphipacifica 2:3–34Google Scholar
  3. Boxshall GA (2004) The evolution of arthropod limbs. Biol Rev 79:253–300PubMedCrossRefGoogle Scholar
  4. Boxshall GA (2013) Arthropod limbs and their development. In: Minelli A, Boxshall G, Frusco G (eds) Arthropod biology and evolution. Molecules, development, morphology, Springer, pp. 241–267Google Scholar
  5. Briggs DEG, Collins D (1988) A Middle Cambrian chelicerate from Mount Stephen, British Columbia. Palaeontology 31:779–798Google Scholar
  6. Briggs DEG, Collins D (1999) The arthropod Alalcomenaeus cambricus Simonetta, from the Middle Cambrian Burgess Shale of British Columbia. Palaeontology 42:953–977CrossRefGoogle Scholar
  7. Briggs DEG, Siveter DJ, Siveter DJ, Sutton MD, Garwood RJ, Legg DA (2012) A Silurian horseshoe crab illuminates the evolution of chelicerate limbs. Proc Natl Acad Sci U S A 109:15702–15705PubMedCentralPubMedCrossRefGoogle Scholar
  8. Bruton DL (1981) The arthropod Sidneyia inexpectans, Middle Cambrian, Burgess Shale, British Columbia. Phil Trans R Soc Lond B 295:619–653CrossRefGoogle Scholar
  9. Bruton DL, Whittington HB (1983) Emeraldella and Leanchoilia, two arthropods from the Burgess Shale, middle Cambrian, British Columbia. Phil Trans R Soc Lond B 300:553–582CrossRefGoogle Scholar
  10. Budd G (2002) A palaeontological solution to the arthropod head problem. Nature 417:271–275PubMedCrossRefGoogle Scholar
  11. Chen J-Y, Waloszek D, Maas A (2004) A new ‘great-appendage arthropod’ from the Lower Cambrian of China and homology of chelicerate chelicerae and raptorial antero-ventral appendages. Lethaia 37:3–20Google Scholar
  12. Collins D, Briggs DEG, Conway MS (1983) New Burgess Shale fossil sites reveal Middle Cambrian faunal complex. Science 22:163–167CrossRefGoogle Scholar
  13. Cotton TJ, Braddy SJ (2004) The phylogeny of arachnomorph arthropods and the origin of Chelicerata. Trans R Soc Edinb Earth Sci 94:169–193Google Scholar
  14. Dewel RA, Dewel WC (1997) The place of tardigrades in arthropod evolution. In: Fortey RA, Thomas RH (eds) Arthropod relationships. Chapman & Hall, London, pp 109–123Google Scholar
  15. Dunlop JA (2005) New ideas about the euchelicerate stem-lineage. In: Deltshev C, Stoev P (eds) European arachnology 2005, pp. 9–23. Acta Zool Bulg Suppl 1Google Scholar
  16. Dunlop JA, Selden PA (1997) The early history and phylogeny of the chelicerates. In: Fortey RA, Thomas RH (eds) Arthropod relationships. Chapman & Hall, London, pp 221–238Google Scholar
  17. Dunlop JA, Anderson LI, Braddy SJ (2004) A redescription of Chasmataspis laurencii Caster & Brooks, 1956 (Chelicerata, Chasmataspidida) from the Middle Ordovician of Tennessee, USA, with remarks on chasmataspid phylogeny. Trans R Soc Edinb Earth Sci 94:207–225Google Scholar
  18. Edgecombe GD, García-Bellido DC, Paterson JR (2011) A new leanchoiliid megacheiran arthropod from the lower Cambrian Emu Bay Shale, South Australia. Acta Palaeontol Pol 56:385–400CrossRefGoogle Scholar
  19. Eldredge N (1974) Revision of the Synziphosura (Chelicerata, Merostomata), with remarks on merostome phylogeny. Am Mus Novit 2543:1–41Google Scholar
  20. Fletcher TP, Collins DH (1998) The Middle Cambrian Burgess Shale and its relationship to the Stephen formation in the Southern Canadian Rocky Mountains. Can J Earth Sci 17:400–418Google Scholar
  21. Fletcher TP, Collins DH (2003) The Burgess Shale and associated Cambrian formations west of the Fossil Gully Fault Zone on Mount Stephen, British Columbia. Can J Earth Sci 40:1823–1838CrossRefGoogle Scholar
  22. Goloboff PA (1999) Analyzing large data sets in reasonable times: solutions for composite optima. Cladistics 15:415–428CrossRefGoogle Scholar
  23. Goloboff PA, Carpenter JM, Salvador Arias J, Rafael Miranda Esquivel D (2008a) Weighting against homoplasy improves phylogenetic analysis of morphological data sets. Cladistics 24:758–773CrossRefGoogle Scholar
  24. Goloboff PA, Farris JS, Nixon KC (2008b) TNT, a free program for phylogenetic analysis. Cladistics 24:774–786CrossRefGoogle Scholar
  25. Haug JT, Waloszek D, Maas A, Liu Y, Haug C (2012) Functional morphology, ontogeny and evolution of mantis shrimp-like predators in the Cambrian. Palaeontology 55:369–399CrossRefGoogle Scholar
  26. Hesselbo SP (1992) Aglaspidida (Arthropoda) from the Upper Cambrian of Wisconsin. J Paleontol 66:885–923Google Scholar
  27. Hou X-G, Bergström J (1997) Arthropods of the lower Cambrian Chengjiang fauna, southwest China. Fossils Strata 45:1–116Google Scholar
  28. Lamsdell JC (2013) Revised systematics of the Palaeozoic ‘horseshoe crabs’ and the myth of monophyletic Xiphosura. Zool J Linn Soc 167:1–27CrossRefGoogle Scholar
  29. Lauterbach K-E (1980) Schlüsselereignisse in der Evolution des Grundplans der Arachnata (Arthropoda). Abh Verh Naturwiss Vereins Hamburg 26:293–320Google Scholar
  30. Lee MSY, Soubrier J, Edgecombe GD (2013) Rates of phenotypic and genomic evolution during the Cambrian explosion. Curr Biol 23:1–7Google Scholar
  31. Legg DA (2013) Multi-segmented arthropods from the middle Cambrian of British Columbia (Canada). J Paleontol 87:493–501CrossRefGoogle Scholar
  32. Legg DA, Caron J-B (2014) New Middle Cambrian bivalved arthropods from the Burgess Shale (British Columbia, Canada). Palaeontology 57:691–711CrossRefGoogle Scholar
  33. Legg DA, Sutton MD, Edgecombe GD, Caron J-B (2012) Cambrian bivalved arthropod reveals origin of arthrodization. Proc R Soc B 279:4699–4704PubMedCentralPubMedCrossRefGoogle Scholar
  34. Legg DA, Sutton MD, Edgecombe GD (2013) Arthropod fossil data increase congruence of morphological and molecular phylogenies. Nat Commun 4:2485PubMedCrossRefGoogle Scholar
  35. Ma X, Hou X-G, Edgecombe GD, Strausfeld NJ (2012) Complex brain and optic lobes in an early Cambrian arthropod. Nature 490:258–261PubMedCrossRefGoogle Scholar
  36. Nixon KC (1999) The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15:407–414CrossRefGoogle Scholar
  37. Orr PJ, Siveter DJ, Briggs DEG, Siveter DJ, Sutton MD (2000) A new arthropod from the Silurian Konservat-Lagerstätte of Herefordshire, England. Proc R Soc Lond B 267:1497–1504CrossRefGoogle Scholar
  38. Ortega-Hernández J, Legg DA, Braddy SJ (2013) The phylogeny of aglaspidid arthropods and the internal relationships within Artiopoda. Cladistics 29:15–45CrossRefGoogle Scholar
  39. Reisinger PWM, Tutter I, Welsch U (1991) Fine structure of the gills of the horseshoe crabs Limulus Polyphemus and Tachypleus tridentatus and of the book lungs of the spider Eurypelma californicum. Zool Jahrb Abt Anat Ontog 121:331–357Google Scholar
  40. Rota-Stabelli O, Daley AC, Pisani D (2013) Molecular timetrees reveal a Cambrian colonization of land and a new scenario for ecdysozoan evolution. Curr Biol 23:392–398PubMedCrossRefGoogle Scholar
  41. Scholtz G, Edgecombe GD (2005) Head, Hox and the phylogenetic position of trilobites. In: Koenemann S, Jenner R (eds) Crustacea and arthropod relationships. Taylor & Francis, Oxford, pp 139–165CrossRefGoogle Scholar
  42. Scholtz G, Edgecombe GD (2006) The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence. Dev Genes Evol 216:395–415PubMedCrossRefGoogle Scholar
  43. Sharma PP, Schwager EE, Giribet G, Jockusch EL, Extavour CG (2013) Distal-less and dashshund pattern both plesiomorphic and apomorphic structures in chelicerates: RNA interference in the harvestman Phalangium opilio (Opiliones). Evol Dev 15:228–242PubMedCrossRefGoogle Scholar
  44. Siveter DJ, Briggs DEG, Siveter DJ, Sutton MD, Legg DA, Joomun S (2014) A Silurian short-great-appendage arthropod. Proc R Soc Lond B 281 (in press)Google Scholar
  45. Stein M (2013) Cephalic and appendage morphology of the Cambrian arthropod Sidneyia inexpectans. Zool Anz 253:164–178CrossRefGoogle Scholar
  46. Stein M, Selden PA (2012) A restudy of the Burgess Shale (Cambrian) arthropod Emeraldella brocki and reassessment of its affinities. J Syst Palaeontol 10:361–383CrossRefGoogle Scholar
  47. Størmer L (1944) On the relationships and phylogeny of fossil and recent Arachnomorpha. Skrift Norske Vidensk Acad I Oslo 5:1–158Google Scholar
  48. Strausfeld NJ (2012) Arthropod brains: evolution, functional elegance, and structural significance. Harvard University Press, Cambridge, p 650Google Scholar
  49. Sutton MD, Briggs DEG, Siveter DJ, Siveter DJ, Orr PJ (2002) The arthropod Offacolus kingi (Chelicerata) from the Silurian of Herefordshire, England: computer based morphological reconstructions and phylogenetic affinities. Proc R Soc Lond B 269:1195–1203CrossRefGoogle Scholar
  50. Tanaka G, Hou X-G, Ma X, Edgecombe GD, Strausfeld NJ (2013) Chelicerate neural ground pattern in a Cambrian great appendage arthropod. Nature 502:364–367PubMedCrossRefGoogle Scholar
  51. Van Roy P, Orr PJ, Botting JP, Muir LA, Vinther J, Lefebvre B, el Hariri K, Briggs DEG (2010) Ordovician faunas of Burgess Shale type. Nature 465:215–218PubMedCrossRefGoogle Scholar
  52. Waloszek D, Dunlop JA (2002) A larval sea spider (Arthropoda: Pycnogonida) from the Upper Cambrian ‘Orsten’ of Sweden, and the phylogenetic position of pycnogonids. Palaeontology 45:421–446CrossRefGoogle Scholar
  53. Weygoldt P (1986) Arthropod interrelationships—the phylogenetic-systematic approach. J Zool Syst Evol Res 24:19–35CrossRefGoogle Scholar
  54. Wills MA, Briggs DEG, Fortey RA, Wilkinson M (1995) The significance of fossils in understanding arthropod evolution. Verh Dtsch Zool Ges 88:203–215Google Scholar
  55. Wills MA, Briggs DEG, Fortey RA, Wilkinson M, Sneath PHA (1998) An arthropod phylogeny based on fossil and recent taxa. In: Edgecombe GD (ed) Arthropod fossils and phylogeny. Columbia University Press, New York, pp 33–105Google Scholar
  56. Yang J, Ortega-Hernández J, Butterfield NJ, Zhang X-G (2013) Specialized appendages in fuxianhuiids and the head organization of early arthropods. Nature 494:468–471PubMedCrossRefGoogle Scholar
  57. Zhang Z-Q (2011) Phylum Arthropoda von Siebold 1848. Zootaxa 3148:99–103Google Scholar
  58. Zhang X-L, Shu D-G (2005) A new arthropod from the Chengjiang Lagerstätte, Early Cambrian, southern China. Alcheringa 29:185–194CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Oxford University Museum of Natural HistoryOxfordUK

Personalised recommendations