Hallucigenia’s onychophoran-like claws and the case for Tactopoda (original) (raw)

Nature volume 514, pages 363–366 (2014)Cite this article

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Abstract

The Palaeozoic form-taxon Lobopodia encompasses a diverse range of soft-bodied ‘legged worms’ known from exceptional fossil deposits1,2,3,4,5,6,7,8,9. Although lobopodians occupy a deep phylogenetic position within Panarthropoda, a shortage of derived characters obscures their evolutionary relationships with extant phyla (Onychophora, Tardigrada and Euarthropoda)2,3,5,10,11,[12](/articles/nature13576#ref-CR12 "Legg, D. A. et al. Lobopodian phylogeny reanalysed. Nature 476, http://dx.doi.org/10.1038/nature10267

             (10 August 2011)"),[13](/articles/nature13576#ref-CR13 "Budd, G. E. The morphology of Opabinia regalis and the reconstruction of the arthropod stem-group. Lethaia 29, 1–14 (1996)"),[14](/articles/nature13576#ref-CR14 "Wills, M. A., Briggs, D. E. G., Fortey, R. A., Wilkinson, M. & Sneath, P. H. A. in Arthropod Fossils and Phylogeny (ed. Edgecombe, G. D. ) 33–105 (Columbia Univ. Press, 1998)"),[15](/articles/nature13576#ref-CR15 "Dewel, R. A., Budd, G. E., Castano, D. F. & Dewel, W. C. The organization of the subesophageal nervous system in tardigrades: insights into the evolution of the arthropod hypostome and tritocerebrum. Zool. Anz. 238, 191–203 (1999)"). Here we describe a complex feature in the terminal claws of the mid-Cambrian lobopodian _Hallucigenia sparsa_—their construction from a stack of constituent elements—and demonstrate that equivalent elements make up the jaws and claws of extant Onychophora. A cladistic analysis, informed by developmental data on panarthropod head segmentation, indicates that the stacked sclerite components in these two taxa are homologous—resolving hallucigeniid lobopodians as stem-group onychophorans. The results indicate a sister-group relationship between Tardigrada and Euarthropoda, adding palaeontological support to the neurological[16](/articles/nature13576#ref-CR16 "Mayer, G., Kauschke, S., Rüdiger, J. & Stevenson, P. A. Neural markers reveal a one-segmented head in tardigrades (water bears). PLoS ONE 8, e59090 (2013)"),[17](/articles/nature13576#ref-CR17 "Mayer, G. et al. Selective neuronal staining in tardigrades and onychophorans provides insights into the evolution of segmental ganglia in panarthropods. BMC Evol. Biol. 13, 230 (2013)") and musculoskeletal[18](/articles/nature13576#ref-CR18 "Marchioro, T. et al. Somatic musculature of Tardigrada: phylogenetic signal and metameric patterns. Zool. J. Linn. Soc. 169, 580–603 (2013)"),[19](/articles/nature13576#ref-CR19 "Schulze, C. & Schmidt-Rhaesa, A. Organisation of the musculature of Batillipes pennaki. Meiofauna Mar. 19, 195–207 (2011)") evidence uniting these disparate clades. These findings elucidate the evolutionary transformations that gave rise to the panarthropod phyla, and expound the lobopodian-like morphology of the ancestral panarthropod.

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Acknowledgements

The authors are supported by Research Fellowships at Clare College (M.R.S.) and Emmanuel College (J.O.-H.), University of Cambridge, UK. Thanks to J.-B. Caron and T. Harvey for images, access to material and discussions. D. Erwin, K. Hollis and P. Fenton facilitated access to museum specimens, and S. Whittaker assisted with electron microscopy. E. kanangrensis were collected from the Blue Mountains, New South Wales, with assistance from G. Budd and N. Tait and funding from an H.B. Whittington Research Grant (Paleontological Society). N. Butterfield and R. Janssen provided additional material. Parks Canada provided research and collection permits to Royal Ontario Museum teams led by D. Collins. The software TNT is funded by the Willi Hennig Society.

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Authors and Affiliations

  1. Department of Earth Sciences, Downing Site, University of Cambridge, Cambridge CB2 3EQ, UK,
    Martin R. Smith & Javier Ortega-Hernández

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  1. Martin R. Smith
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  2. Javier Ortega-Hernández
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Contributions

M.R.S. conceived the project; dissected, described and interpreted specimens; and ran the phylogenetic analysis. J.O.-H. led the integration of developmental data into phylogenetic analysis and the interpretation of results. Both authors contributed equally to data analysis, discussion of results and manuscript preparation.

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Correspondence toMartin R. Smith.

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Extended data figures and tables

Extended Data Figure 1 Claw measurements.

To reconstruct the relationship between the stacked constituent elements, a digital image of a sclerite (a) was duplicated, rotated and enlarged such that its outer sclerite precisely overlay the inner sclerite in the original image (b; the cyan image has been enlarged by 5% and rotated to match the inner sclerite in the yellow image). Repetition of this process demonstrates a logarithmic growth trajectory (c); a logarithmic spiral was fitted to this trajectory and its Raupian parameters22 calculated. This process was most accurate in the inner jaw elements, whose dentate margin provided multiple landmarks that allowed the precise fitting of subsequent images. Estimates were also obtained for the outer jaws and appendicular claws of Euperipatoides, and the claws and spines of H. sparsa. Hallucigenia spines demonstrated variability in Raup’s D because they are sometimes obliquely preserved, so the maximum value was taken as representative. The implied growth rate of 2.4 ± 2.7% in Euperipatoides sclerites (range 0–8%; measured from five inner and six outer jaw sclerites) cannot persist throughout the organism’s lifespan, since moulting consistently occurs every 2 weeks (ref. 38). Either moulting occurs less frequently in wild populations, the rate of growth varies during ontogeny or the constituent elements deform slightly during growth.

Extended Data Figure 2 Density of scaly ornament in a hallucigeniid spine with three constituent elements (Geological Survey of Canada 136958).

a, Complete spine, showing regions of enlargement; b, apex of spine showing tips of two internal elements; c, margins of two internal elements faintly visible (dotted lines); density of scales where three elements are superimposed is 0.050 scales per square micrometre; where two elements are superimposed it is 0.039 scales per square micrometre; for a single element it is 0.026 scales per square micrometre; slight deviation from a 3:2:1 ratio is attributed to decreased visibility of individual scales in occluded regions; d, up to five scales overlap; only two could overlap if scales were restricted to the front and back surfaces of a single element. Transmitted light images from multiple focal planes combined using CombineZM (A. Hadley). Scale bar, a, 100 µm; b, 40 µm; c, 10 µm; d, 5 µm.

Extended Data Figure 3 Claws of Euperipatoides kanangrensis (Onychophora).

a, b, Secondary electron images of a single claw, separated into outermost element (a) and inner elements (b), each with ornamented basal region. c, d, Differential image contrast images of a single claw, separated into outermost element (c) and inner elements (d). Nomarski interference contrast accentuates the basal ornament. e–g, Single claw, separated into innermost element (e) and outer elements (f); pigmented foot tissue only associated with inner two elements; g, digital superposition of e and f showing original claw construction. h, Abnormal claw with blunt tip reflected in each constituent element. Transmitted light images from multiple focal planes combined using TuFuse (M. Lyons). Scale bar, 100 µm.

Extended Data Figure 4 Sclerite constitution in other taxa.

a, b, Single constituent element in claws of (a) Nephrotoma spp. (Tipulidae, Hexapoda, Euarthropoda) and (b) Eutardigrada (species indeterminate). Nomarski interference contrast. c–e, Small carbonaceous fossils with stacked constituent elements, interpreted as appendicular sclerites of total-group onychophorans (images courtesy of T. Harvey): c, d, from the basal mid-Cambrian (Stage 5) Kaili biota39; e, articulated pair from the mid- to late Cambrian Deadwood Formation, each claw comprising two constituent elements. f, Three appendicular sclerites (claws: arrowed) from a single appendage of Aysheaia pedunculata from the mid-Cambrian Burgess Shale (ROM 63052), each comprising a single element. Transmitted light images from multiple focal planes combined using TuFuse (M. Lyons) and CombineZM (A. Hadley). Scale bars, 100 µm.

Supplementary information

Supplementary Information

This file contains details of character coding for phylogenetic analysis, analytical methodology, and transformations implied by our most parsimonious tree. (PDF 1341 kb)

Supplementary Data

Zipped archive containing character matrix in Nexus and Excel formats, most parsimonious trees for all values of k in Nexus format (all individual trees, plus MPTs) and human-readable PDF format (MPTs only), and TNT script used to generate trees. (ZIP 515 kb)

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Smith, M., Ortega-Hernández, J. _Hallucigenia_’s onychophoran-like claws and the case for Tactopoda.Nature 514, 363–366 (2014). https://doi.org/10.1038/nature13576

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Editorial Summary

Organizing the early arthropods

The early fossil record of arthropods, jointed-legged animals, is replete with fossils of lobopodians - wormlike animals with legs and sometimes elaborate body armour. The lobopodians bear a passing resemblance to the velvet worms or onychophorans, predators among the leaf-litter of modern tropical forest floors, but apart from general morphology, no specific links between the two groups were known. Now Martin Smith and Javier Ortega-Hernndez have identified a trait that links them - the tiny claws on the ends of the legs of the Cambrian lobopod Hallucigenia closely resemble the claws and jaws of extant onychophores in their unique method of construction. This allows lobopods and onychophores to be grouped together with tardigrades ('water bears'), the closest extant relatives of true arthropods (including insects, crustaceans and spiders), and suggests that the earliest ancestor of the arthropods and their kin would have looked like a lobopodian.