A middle Cambrian arthropod with chelicerae and proto-book gills

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Abstract

The chelicerates are a ubiquitous and speciose group of animals that has a considerable ecological effect on modern terrestrial ecosystems—notably as predators of insects and also, for instance, as decomposers1. The fossil record shows that chelicerates diversified early in the marine ecosystems of the Palaeozoic era, by at least the Ordovician period2. However, the timing of chelicerate origins and the type of body plan that characterized the earliest members of this group have remained controversial. Although megacheirans3,4,5 have previously been interpreted as chelicerate-like, and habeliidans6 (including Sanctacaris7,8) have been suggested to belong to their immediate stem lineage, evidence for the specialized feeding appendages (chelicerae) that are diagnostic of the chelicerates has been lacking. Here we use exceptionally well-preserved and abundant fossil material from the middle Cambrian Burgess Shale (Marble Canyon, British Columbia, Canada) to show that Mollisonia plenovenatrix sp. nov. possessed robust but short chelicerae that were placed very anteriorly, between the eyes. This suggests that chelicerae evolved a specialized feeding function early on, possibly as a modification of short antennules. The head also encompasses a pair of large compound eyes, followed by three pairs of long, uniramous walking legs and three pairs of stout, gnathobasic masticatory appendages; this configuration links habeliidans with euchelicerates (‘true’ chelicerates, excluding the sea spiders). The trunk ends in a four-segmented pygidium and bears eleven pairs of identical limbs, each of which is composed of three broad lamellate exopod flaps, and endopods are either reduced or absent. These overlapping exopod flaps resemble euchelicerate book gills, although they lack the diagnostic operculum9. In addition, the eyes of M. plenovenatrix were innervated by three optic neuropils, which strengthens the view that a complex malacostracan-like visual system10,11 might have been plesiomorphic for all crown euarthropods. These fossils thus show that chelicerates arose alongside mandibulates12 as benthic micropredators, at the heart of the Cambrian explosion.

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Fig. 1: General morpho-anatomy of M. plenovenatrix.
Fig. 2: Morpho-anatomical details of M. plenovenatrix.
Fig. 3: Interpretative diagrams of M. plenovenatrix.
Fig. 4: Phylogenetic position and life reconstruction of M. plenovenatrix.

Data availability

All data generated or analysed during this study are included in the published Letter and its Supplementary Information. The ZooBank accession code for M. plenovenatrix is LSID: urn:lsid:zoobank.org:pub:6E2217D1-88C3-4CC7-85B7-F2C8E3477CAA.

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Acknowledgements

Fossils for this study were collected by Royal Ontario Museum field parties under several Parks Canada Research and Collections permits to J.-B.C. (YNP2012-12054, KOONIP 2014-16317 and YNP-2016-21639). We thank T. Keith from Parks Canada for facilitating fieldwork activities. Major funding support for fieldwork comes from the Royal Ontario Museum (research and collection grants, and natural history fieldwork grants), the Polk Milstein family, the National Geographic Society (no. 9475-14 to J.-B.C.), the Swedish Research Council (to M. Streng), the National Science Foundation (NSF-EAR-1554897) and Pomona College (to R. R. Gaines). Research was also supported by J.-B.C.’s NSERC Discovery Grant (no. 341944) and the Dorothy Strelsin Foundation (Royal Ontario Museum), and C.A.’s President’s International Fellowship Initiative Grant (no. 2018PC0043) and China Postdoctoral Science Foundation Grant (no. 2018M630616). We thank S. Scharf for editorial suggestions and J. Liang for the illustrations of M. plenovenatrix. This is Royal Ontario Museum Burgess Shale project number 84.

Author information

C.A. wrote the initial drafts of the manuscript, figures and Supplementary Discussion. J.-B.C. organized the palaeontological expeditions to Marble Canyon, photographed and prepared the specimens. Both C.A. and J.-B.C. contributed to the collection, observation and interpretation of fossils and to the final version of the manuscript.

Correspondence to Cédric Aria or Jean-Bernard Caron.

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Competing interests

The authors declare no competing interests.

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Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Peer review information Nature thanks Jason Dunlop and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Extended data figures and tables

Extended Data Fig. 1 Anterior dorso-ventral morpho-anatomy and elemental mapping of M. plenovenatrix.

al, Specimen ROMIP 62978. a, b, Full specimen (part and counterpart). c, d, Close-up of anterior region (part and counterpart). el, Backscatter (BS) images (e) and elemental maps (fl). Asterisk points to a taphonomic artefact. bc, base of chelicera. For other acronyms, see Figs. 1, 2. Scale bars, 3 mm (a, b), 1.5 mm (c, d, f).

Extended Data Fig. 2 General morpho-anatomy and additional details of M. plenovenatrix.

ad, Specimen ROMIP 65015. a, b, Full specimen (part and counterpart). Areas in the white boxes in a and b are shown in c and d, respectively. c, d, Close-up of trunk region showing multi-lobate exopods (part and counterpart). e, Specimen ROMIP 65263. Putative moult, full specimen (counterpart) (the part is shown in Fig. 1d). f, g, Specimen ROMIP 65278. f, Full specimen. Area in white box is shown in g. g, Close-up of head region, showing appendages. h, Specimen ROMIP 65299. Full specimen, curled on itself with pygidium partially disarticulated. For acronyms, see Figs. 1, 2. Scale bars, 2 mm (ad), 1 mm (eh).

Extended Data Fig. 3 Key morpho-anatomical features with interpretative drawings of M. plenovenatrix.

a, Specimen ROMIP 62978. Close-up of chelicerae in their lateral view. b, Holotype ROMIP 65264. Close-up of chelicerae in their dorsal view. c, Specimen ROMIP 65015. Close-up of trunk exopods. d, e, Lateral (d) and dorsal (e) renderings of the chelicerae of the camel spider Rhagodes shown for comparison. f, Specimen ROMIP 65262. Close-up of post-frontal cephalic appendages preserved in frontal aspect. g, Specimen ROMIP 62978. Close-up of left eye, preserved in dorsal aspect. Arrowheads point to margin of innermost neuropil. se, setae. For other acronyms, see Figs. 1, 2. Scale bars, 0.5 mm (ac), 1 mm (f, g). Renderings of Rhagodes chelicerae are reproduced with permission from ref. 32.

Extended Data Fig. 4 Gut, pleural articulation and pygidial appendages of M. symmetrica.

ac, Specimen ROMIP 65302. a, Full specimen in cross-polarized light. Area in white box is shown in c. b, Specimen coated with ammonium chloride sublimate; note the three-dimensional apatite preservation of the gut. Arrows point to articulating furrows on pleurae. c, Close-up of pygidium, showing exopod lamellae jutting out underneath the cuticle. For acronyms, see Figs. 1, 2. Scale bars, 2 mm (a, b), 1 mm (c).

Extended Data Fig. 5 General and anterior morpho-anatomy, including remains of chelicerae and neural tissues, of M. gracilis.

a-f, Specimen MCZ 1811. ad, Full specimen (part and counterpart). a, c, Specimen in cross-polarized light, and dry. b, d, Specimen in cross-polarized light, and wet. e, f, Close-up of head region (part and counterpart). Arrows point to the articulating pleural furrows in b. For acronyms, see Figs. 1, 2. Scale bars, 2 mm (a), 1 mm (e). Images are courtesy of D. Collins (ROM).

Extended Data Fig. 6 Maximum clade credibility tree from a Bayesian analysis of panarthropod relationships.

The tree is based on a matrix of 101 taxa and 267 characters. The main topology shown does not include Pycnogonida (topology in Fig. 4). Inset shows the Panchelicerata clade (red branch) with Pycnogonida included. The position of Chelicerata sensu stricto (as defined by the presence of chelifores and chelicerae) is dependent upon the problematic placement of pycnogonids (Supplementary Discussion). The numbers on the right of nodes are posterior probabilities.

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