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A Superarmored Lobopodian from the Cambrian of China and Early Disparity in the Evolution of Onychophora

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A Superarmored Lobopodian from the Cambrian of China and Early Disparity in the Evolution of Onychophora A superarmored lobopodian from the Cambrian of China and early disparity in the evolution of Onychophora Jie Yanga, Javier Ortega-Hernándezb,1, Sylvain Gerberb, Nicholas J. Butterfieldb, Jin-bo Houa, Tian Lana, and Xi-guang Zhanga,1 aYunnan Key Laboratory for Paleobiology, Yunnan University, Kunming 650091, China; and bDepartment of Earth Sciences, University of Cambridge, Cambridge CB2 3EQ, United Kingdom Edited by Graham E. Budd, Uppsala University, Uppsala, Sweden, and accepted by the Editorial Board June 1, 2015 (received for review March 23, 2015) We describe Collinsium ciliosum from the early Cambrian Xiaoshiba Stage 5 Spence Shale (5); Luolishania longicruris early Cambrian Lagerstätte in South China, an armored lobopodian with a remark- Stage 3, Chengjiang (6); Collins’ monster, early Cambrian Stage able degree of limb differentiation including a pair of antenna-like 4, Emu Bay Shale (7), and middle Cambrian Stage 5, Burgess appendages, six pairs of elongate setiferous limbs for suspension Shale (4). feeding, and nine pairs of clawed annulated legs with an anchor- ing function. Collinsium belongs to a highly derived clade of lobo- Collinsium ciliosum gen. et sp. nov. podians within stem group Onychophora, distinguished by a Etymology. Named after Desmond Collins, who discovered and substantial dorsal armature of supernumerary and biomineralized first illustrated the eponymous fossil (4); ciliosum (Latin), hairy. spines (Family Luolishaniidae). As demonstrated here, luolishaniids Type material. Holotype YLKP 12127 (Fig. 1A); paratypes YLKP display the highest degree of limb specialization among Paleozoic 12128 (Fig. 2A) and YLKP 12129 (Figs. 1D and 2D). YLKP: Key lobopodians, constitute more than one-third of the overall mor- Laboratory for Paleobiology, Yunnan University. phological disparity of stem group Onychophora, and are substan- Referred material. An additional 26 topotype specimens (YKLP tially more disparate than crown group representatives. Despite 12130–12155). having higher disparity and appendage complexity than other Locality and horizon. Xiaoshiba section, Kunming, Yunnan Prov- lobopodians and extant velvet worms, the specialized mode of life ince; Cambrian Stage 3 (local upper Qiongzhusian), lower por- embodied by luolishaniids became extinct during the Early Paleo- tion of the Hongjingshao Formation (10, 11) (SI Appendix, Fig. zoic. Collinsium and other superarmored lobopodians exploited a S1). The horizon has also been verified by a similar fossil as- unique paleoecological niche during the Cambrian explosion. semblage found from another section in Kunming (13). Diagnosis. Armored lobopodian with six pairs of setulose anterior Collins’ monster | Xiaoshiba Lagerstätte | Cambrian explosion | evolution | appendages and 15 biomineralized sclerite sets: first sclerite set phylogeny represented by a single pair of short dorsolateral spines; sets 2–15 composed of five spines of variable length. Nine posterior nychophorans, or velvet worms, comprise a relatively small Ophylum (∼180 species) of soft-bodied panarthropods con- walking legs with single terminal claws. Head with pair of stituting a minor component of modern rainforest ecosystems around the world (1). The overall organization of extant ony- Significance chophorans is remarkably conserved (2), typified by a low mor- phological variability and homogeneous autoecologies as ambush Paleozoic lobopodians constitute a diverse assemblage of predators of small invertebrates. An emerging fossil record, worm-like organisms that are known from various exceptional however, points to a substantially wider range of forms and fossil deposits and were among the earliest animals to develop habits during their early evolutionary history (3–8). Paleozoic skeletonized body parts for protection. Here, we describe lobopodians—a paraphyletic group of soft-bodied extinct or- Collinsium ciliosum gen. et sp. nov., an armored lobopodian ganisms resembling worms with legs—occupy basal phylogenetic from the early Cambrian Xiaoshiba Lagerstätte (South China). positions within the stem lineages of Onychophora, Tardigrada, Collinsium belongs to an extinct clade of superarmored lobo- and Euarthropoda (3, 6, 9), and thus offer critical insights about podians characterized by supernumerary dorsal spines, and the early evolution and paleobiology of panarthropod phyla. specialized limbs for filter feeding; collectively, these fossil taxa Here, we describe the stem group onychophoran Collinsium represent a well-defined group within the lineage leading to ciliosum,a“superarmored” lobopodian with complex limbs, extant velvet worms (Onychophora). Despite their greater based on a large and exquisitely preserved population from the morphological variety and appendage complexity compared early Cambrian (Stage 3) Xiaoshiba Lagerstätte in South China with other lobopodians and extant velvet worms, Collinsium (10, 11) (SI Appendix, Fig. S1). and its close relatives embodied a unique, yet ultimately failed, autoecology during the Cambrian explosion. Systematic Paleontology Superphylum Panarthropoda, Phylum (Stem Group) Onychophora, Author contributions: N.J.B. and X.-g.Z. designed research; J.Y., J.O.-H., S.G., N.J.B., J.-b.H., Family Luolishaniidae (12). T.L., and X.-g.Z. performed research; J.-b.H. and T.L. collected material; J.Y. collected and prepared all material; J.O.-H. and S.G. analyzed data; and J.O.-H. and N.J.B. wrote Diagnosis. Armored lobopodians with thorn-shaped dorsal scler- the paper. ites, arranged in odd-numbered sets of three or more per trunk The authors declare no conflict of interest. appendage pair; sclerite sets irregularly spaced, with separation This article is a PNAS Direct Submission. G.E.B. is a guest editor invited by the Editorial decreasing progressively toward the anterior and posterior ends Board. of the body; anteriormost five or six trunk limb pairs slender with 1To whom correspondence may be addressed. Email: [email protected] or jo314@cam. double rows of long setiform spines (emended from ref. 6). ac.uk. Included taxa. Collinsium ciliosum gen. et sp. nov., early Cam- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. brian Stage 3, Xiaoshiba; Acinocricus stichus,middleCambrian 1073/pnas.1505596112/-/DCSupplemental. 8678–8683 | PNAS | July 14, 2015 | vol. 112 | no. 28 www.pnas.org/cgi/doi/10.1073/pnas.1505596112 Downloaded by guest on September 29, 2021 Fig. 1. Anterior morphology of Collinsium ciliosum from the early Cambrian (Stage 3) Xiaoshiba Lagerstätte. (A–C) YKLP 12127, holotype: (A) laterally preserved specimen, showing antenna-like limbs, six pairs of setiferous appendages, and limb correlation with sets of sclerotized dorsal spines; (B)detailofthe head; (C) detail of the base of the fifth dorsal spine and short filiform setae. (D–F) YKLP 12129a, para- type: (D) lateral view showing correlation of ap- pendages and sets of dorsal sclerotized spines; (E) details of the annulations, papillae, and fine hair- like setae; (F) bases of the dorsolateral spines and the lateral spines of the seventh sclerite set. (G and H) YKLP 12128, specimen with six pairs of setiferous appendages (arrowed): (G) lateral view; (H) detail of lateral overlap of the paired anterior sclerites on the head region; arrows indicate the outline of the left sclerite. (I) YKLP 12136, dorsal view showing organi- zation of sclerite sets. Abbreviations: ann, annula- tions; ant, antennae; asc, anterior dorsal sclerites; dls, dorsal lateral spine; gut, digestive tract; hs, hair-like setae; ls, lateral spine; ms, medial spine; pa, papillae; set, setiform spines; SS1–15, sclerite series; tap1–15, appendages. anterior antenna-like limbs and paired dorsal sclerites. Head and and 2 A, D, and E, and SI Appendix, Figs. S5 and S6). Whereas anterior trunk region densely covered by short filiform setae. the first sclerite set comprises a pair of short (<1-mm) dorso- Description. Except for the three-dimensionally preserved dorsal lateral spines (Fig. 1I), the 2nd to 15th sets consist of five spines, spines, Collinsium specimens are preserved as flattened compression including the following: (i) a single, prominent, 6- to 12-mm-long fossils. Complete individuals reach a maximum length of 85 mm. medial spine; (ii) a pair of medium-sized (approximately one- The elongate body is approximately tubular, widening gradually third the length of the associated median spine) dorsolateral toward the middle section by a factor of ∼1.5. The head region is spines; and (iii) two smaller (approximately one-eighth the bulbous, curves ventrally, and bears a terminal mouth lacking length of the associated median spine) lateral spines (Figs. 1 A, accessory oral structures (Fig. 1 A, B, and G, and SI Appendix, C, D, F, G, and I, and 2 A, D, and E). The distal portions of the Fig. S3). A pair of subrectangular sclerotized plates converge spines curve gently toward the anterior (Figs. 1 A, D, and G, and dorsomedially on the head (Fig. 1 B and G–I), followed by a pair 2A). The distance between sclerite sets and their respective of anteriorly directed uniramous antenniform appendages (Fig. ventral limb pairs decreases toward the anterior and posterior 1B); there is no evidence of eyes. The paired trunk limbs are ends of the animal, such that sets 1–6 and 12–15 are separated by uniramous and represented by two distinct morphotypes: the first ∼1–1.5 times the maximum width of the median spine, compared to sixth pairs of trunk appendages are elongate (approximately with a separation
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