Durham Research Online Deposited in DRO: 14 September 2016 Version of attached le: Accepted Version Peer-review status of attached le: Peer-reviewed Citation for published item: Zhang, X.-G. and Smith, M.R. and Yang, J. and Hou, J.-B. (2016) 'Onychophoran-like musculature in a phosphatized Cambrian lobopodian.', Biology letters., 12 (9). p. 20160492. Further information on publisher's website: http://rsbl.royalsocietypublishing.org/ Publisher's copyright statement: Additional information: Use policy The full-text may be used and/or reproduced, and given to third parties in any format or medium, without prior permission or charge, for personal research or study, educational, or not-for-prot purposes provided that: • a full bibliographic reference is made to the original source • a link is made to the metadata record in DRO • the full-text is not changed in any way The full-text must not be sold in any format or medium without the formal permission of the copyright holders. Please consult the full DRO policy for further details. Durham University Library, Stockton Road, Durham DH1 3LY, United Kingdom Tel : +44 (0)191 334 3042 | Fax : +44 (0)191 334 2971 https://dro.dur.ac.uk Submitted to Biology Letters Onychophoran -like musculature in a phosphatized Cambrian lobopodian Journal:For Biology Review Letters Only Manuscript ID RSBL-2016-0492.R2 Article Type: Research Date Submitted by the Author: 23-Aug-2016 Complete List of Authors: Zhang, Xi-guang; Yunnan University, Key Laboratory for Palaeobiology; Smith, Martin; Durham University Yang, Jie; Yunnan University, The Key Laboratory for Palaeobiology Hou, Jin-bo; Yunnan University Subject: Evolution < BIOLOGY, Palaeontology < BIOLOGY Categories: Palaeontology Keywords: lobopodians, muscle, evolution, taphonomy, phylogenetics http://mc.manuscriptcentral.com/bl Page 1 of 14 Submitted to Biology Letters 1 Onychophoran-like musculature in a phosphatized Cambrian 2 lobopodian 3 4 Xi-Guang Zhang 1*, Martin R. Smith 2*, Jie Yang 1, Jin-Bo Hou 1 5 6 1Key Laboratory for Paleobiology, Yunnan University, Kunming 650091, China. 7 2Department of EarthFor Sciences, Review Durham University, Du rham,Only DH1 3LE, UK. 8 *These authors contributed equally to this work. 9 Subject areas: 10 Evolution, Palaeontology 11 Keywords: 12 Lobopodians, muscle, evolution, taphonomy, phylogenetics, Cambrian Stage 3 13 Author for Correspondence: 14 Xi-guang Zhang, e-mail: [email protected] 15 Abstract 16 The restricted, exclusively terrestrial distribution of modern Onychophora contrasts strikingly 17 with the rich diversity of onychophoran-like fossils preserved in marine Cambrian 18 Lagerstätten . The transition from these early forebears to the modern onychophoran body 19 plan is poorly constrained, in part due to the absence of fossils preserving details of the soft 20 anatomy. Here we report muscle tissue in a new early Cambrian (Stage 3) lobopodian, 21 Tritonychus phanerosarkus gen. et sp. nov., preserved in the Orsten fashion by three- http://mc.manuscriptcentral.com/bl1 Submitted to Biology Letters Page 2 of 14 Cambrian Onychophoran Muscle 2 Zhang et al. 22 dimensional replication in phosphate. This first report of Palaeozoic onychophoran 23 musculature establishes peripheral musculature as a characteristic of the ancestral 24 panarthropod, but documents an unexpected muscular configuration. Phylogenetic analysis 25 reconstructs T. phanerosarkus as one of a few members of the main onychophoran lineage – 26 which was as rare and as cryptic in the Cambrian period as it is today. 27 1. Introduction 28 The Panarthropod phylaFor – Euarthropoda, Review Tardigrada and Only Onychophora – evolved from a 29 paraphyletic grade of unsegmented leg-bearing worms, the lobopodians [1]. These organisms 30 illuminate otherwise intractable details of early panarthropod evolution [2,3], even if the full 31 significance of their fossils is difficult to evaluate. 32 Lobopodians from the onychophoran total group have a deep ancestry. First 33 represented by occurrences of their dorsal armature in the Tommotian (Cambrian Stage 2) 34 shelly fossil record [4,5], they rise to a more obvious prominence in the Chengjiang biota 35 (Cambrian Stage 3), where their carbonaceous compression fossils display a rich array of 36 morphologies [6]. Fine exterior structure, however, is only seen in three-dimensional 37 microfossils of Orsten-type deposits [7]. Orstenotubulus [8], the single lobopodian preserved 38 in this fashion, dates to the Guzhangian (latest mid-Cambrian), substantially after the burst of 39 lobopodian disparity documented by the early Cambrian (Stage 3) Chengjiang biota [9]. 40 This array of onychophoran-like lobopodians may straddle the onychophoran stem 41 lineage [9], or may predominantly belong to an extinct sister group [3]. Some features of the 42 onychophoran body plan are already evident in these Cambrian taxa [1], though other 43 distinctive characteristics, such as slime papillae, necessarily arose after onychophorans 44 colonised the land. New Cambrian fossils, and better resolution of their relationships, are key 45 to elucidating the evolutionary trajectory that led to the specialized anatomy of modern 46 onychophorans. We here present a new phosphatized lobopodian from early Cambrian http://mc.manuscriptcentral.com/bl2 Page 3 of 14 Submitted to Biology Letters Cambrian Onychophoran Muscle 3 Zhang et al. 47 Orsten-type deposits that provides a unique perspective on the cuticle and musculature of 48 early onychophoran-like lobopodians. 49 2. Materials and methods 50 The specimen was recovered by 5% acetic acid digestion of carbonate nodules from black 51 shales, and is deposited at the Key Laboratory for Palaeobiology, Yunnan University, Kunming, 52 China (YKLP). Phylogenetic analysis was conducted in TNT [10] using the methods of Smith 53 and Ortega HernándezFor [1] on a Reviewrevised matrix of 49 taxa Only and 115 unordered characters 54 integrating data from recent lobopodian analyses [1,3,9,11] (data and scripts available at Dryad 55 [12] in supplementary material ). Parsimony analysis employed implied weights, with 99 values 56 of Goloboff’s concavity constant [13] picked from a log-normal distribution (range: 1.061– 57 259.4; R function qlnorm((1:99)/100, meanlog=log(4), sdlog=log(6)) + 1), and equal 58 weights, with a consensus tree generated from all most parsimonious topologies [14]. Extended 59 implied weighting [15] does not affect the consensus tree. 60 3. Results 61 Systematic Palaeontology 62 Superphylum Ecdysozoa Aguinaldo et al. 1997 [16] 63 Stem-group Onychophora Grube 1853 [17] 64 Genus Tritonychus Zhang et Smith, gen. nov. 65 LSID. urn:lsid:zoobank.org:act:959A47D4-3323-47CB-ADB2-B6A8F5B945A0 66 Etymology . In reference to the third (τριτος , tritos ) claw (ονυχος , onychos ), a unique feature 67 among lobopodians. http://mc.manuscriptcentral.com/bl3 Submitted to Biology Letters Page 4 of 14 Cambrian Onychophoran Muscle 4 Zhang et al. 68 Diagnosis. Lobopodous appendages paired, ten times longer than wide, four times narrower 69 than trunk, each ending with three anteriorly-directed claws . Trunk and appendages 70 ornamented with bifurcating circumferential wrinkles and bearing dermal papillae. Two 71 discrete layers of longitudinal fibres peripheral to body cavity. 72 Type species: 73 Tritonychus phanerosarkus Zhang et Smith gen. et sp. nov. 74 LSID. urn:lsid:zoobank.org:act:1715A32E-C258-4EC2-AFor Review Only44D-EC1A1E3DC23E 75 Etymology . φανερος, phaneros, well-displayed, σαρκος, sarkos , muscle, flesh 76 Holotype. YKLP 12335 (Figure 1), the only known specimen. 77 Occurrence. Yu’anshan Formation (Eoredlichia–Wutingaspis Biozone, approximately late 78 Atdabanian = Cambrian Series 2, Stage 3), Xiaotan section, Yongshan, Yunnan Province. 79 Diagnosis. As genus. 80 Description. The specimen is a millimetre-long section of lobopodian trunk that is folded at 81 its midpoint and bears a pair of lobopods on its ventral surface near the presumed posterior 82 margin (figure 1a). It is incomplete at each end, and lacks most of its dorsal surface. 83 The trunk is ornamented with circumferential wrinkles, spaced at 10 µm, which 84 bifurcate and merge in an irregular fashion (figure 1b). Irregularly positioned conical 85 projections, 5 µm in diameter and 7 µm in height and situated on a round cuticular base 86 (figure 1b,c), presumably correspond to the dermal papillae of Orstenotubulus and extant 87 Onychophora [8]. Moving distally along each appendage, the cuticle wrinkles give way to a 88 reticulate pattern of polygonally-arranged ridges that conceivably correspond to cell 89 boundaries, and the papillae are less frequently expressed (figure 1f–h). http://mc.manuscriptcentral.com/bl4 Page 5 of 14 Submitted to Biology Letters Cambrian Onychophoran Muscle 5 Zhang et al. 90 The trunk is lined with three layers of fibrous tissue, each around 10 µm thick, which 91 we interpret as muscles. The outer layer (figure 1c–e, cyan) comprises 5–10 µm wide 92 longitudinal fibres; it parts between the appendages to leave a 60 µm wide gap, through 93 which a separate bundle of longitudinal fibres (white in figure 1 d) passes. The fibres part 94 again to the right of this point (green in figure 1c), perhaps reflecting the insertion of leg 95 levator musculature. A second layer of interwoven oblique fibres (crimson and mauve in 96 figure 1 c–e) sits within the first, and within that layer lie further fibres oriented perpendicular 97 to the body axis (yellowFor in Fig Review1c–e), presumably representing Only