A Rare Onychophoran-Like Lobopodian from the Lower Cambrian

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Dec 20, 2010 - and the spines is clearly demonstrated in both specimens. (Figs. 1.8, 1.9, 2.5) .... velvet worms (unpublished data from Georg Mayer, private correspondence, 2009); 2) .... Cephalization, condensation of frontal segments into ...
A Rare Onychophoran-Like Lobopodian from the Lower Cambrian Chengjiang Lagerstätte, Southwestern China, and its Phylogenetic Implications Author(s): Qiang Ou, Jianni Liu, Degan Shu, Jian Han, Zhifei Zhang, Xiaoqiao Wan, and Qianping Lei Source: Journal of Paleontology, 85(3):587-594. 2011. Published By: The Paleontological Society DOI: 10.1666/09-147R2.1 URL: http://www.bioone.org/doi/full/10.1666/09-147R2.1

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Journal of Paleontology, 85(3), 2011, p. 587–594 Copyright ’ 2011, The Paleontological Society 0022-3360/11/0085-0587$03.00

A RARE ONYCHOPHORAN-LIKE LOBOPODIAN FROM THE LOWER ¨ TTE, SOUTHWESTERN CHINA, CAMBRIAN CHENGJIANG LAGERSTA AND ITS PHYLOGENETIC IMPLICATIONS QIANG OU,1 JIANNI LIU,2 DEGAN SHU,2,1 JIAN HAN,2 ZHIFEI ZHANG,2 XIAOQIAO WAN,1 AND QIANPING LEI1 1 Early Life Evolution Laboratory, School of Earth Sciences and Resources, China University of Geosciences, Beijing 100083, P. R. China, ,[email protected].; and 2Early Life Institute and Department of Geology, Northwest University, Xi’an 710069, P. R. China, ,[email protected].

ABSTRACT—Lobopodians, which diversified and flourished in the Cambrian seas, have long drawn much attention in that not only their extant close relatives, onychophorans and tardigrades, but euarthropods (Chelicerata, Myriapoda, Crustacea, and Hexapoda) may have been deeply rooted in stem-group lobopodians. Antennacanthopodia gracilis new genus and species is described and interpreted here as an ‘‘unarmoured’’ lobopodian from the Chengjiang fossil Lagersta¨tte (Early Cambrian, ,520 Ma), Yunnan, southwestern China. This animal shares with other known Cambrian lobopodians such plesiomorphies (primitive characters) as onychophoran-like overall appearance; a metamerically segmented body covered by slightly sclerotized cuticle, and paired, unjointed lobopodal legs. Antennacanthopodia is also featured by a pair of frontal antennae, potential ocellus-like lateral visual organs, second antennae, a straight, voluminous midgut, diminutive spines arrayed on the leg and the trunk, well-developed leg musculature, highly sclerotized terminal leg pads, and presumptively a pair of posteriormost appendicules. This new taxon, with innovative characters (autapomorphies), furthers our understanding of early lobopodian diversification. Antennacanthopodia is considered closely allied to extant Onychophora based on considerable anatomical similarities. Taken together its ‘‘two-segmented’’ cephalization and appendage-bearing ‘‘ocular segment’’, this new form may shed some new light on the arthropod groundplan.

INTRODUCTION

widespread, morphologically diverse, and phylogenetically intriguing, lobopodians were a group of fossil marine invertebrates that proliferated in the Early Cambrian and then declined but survived at least the end of the early Paleozoic (von Bitter et al., 2007). Generally characterized by a caterpillar-like overall shape, an undistinguished head, a long, segmented trunk covered by annulated, slightly sclerotized cuticle, and paired, unjointed, ventrolateral lobopods terminated in hooked claws, this grade of organisms have long been recognized as extinct close relatives of the extant onychophorans (e.g., Hutchinson, 1930; Whittington, 1978; Robison, 1985; Ramsko¨ld and Hou, 1991). For almost a century, at least 16 named species of lobopodians referred to 14 genera with soft-body preservation have been described from fossil Konservat-Lagersta¨tten distributed on the margins of four early Paleozoic landmasses: 1) Laurentia (Lower Cambrian to Middle Silurian): Aysheaia pedunculata Walcott, 1911 (see Hutchinson, 1930; Robison, 1985; Whittington, 1978), Hallucigenia sparsa Walcott, 1911 (see Conway Morris, 1977; Ramsko¨ld and Hou, 1991), Hadranax augustus Budd and Peel, 1998, and an unnamed species from the Eramosa fauna (von Bitter et al., 2007); 2) Baltica (Basal to Upper Cambrian): Xenusion auerswaldae Pompeckj, 1927 (see Dzik and Krumbiegel, 1989), and Orstenotubulus evamuellerae Maas et al., 2007; 3) South China (Lower to Middle Cambrian): Luolishania longicruris Hou and Chen, 1989 (see Ma et al., 2009; Liu et al., 2004), Microdictyon sinicum Chen et al., 1989 (see Chen et al., 1995a), Onychodictyon ferox Hou et al., 1991 (see Ramsko¨ld and Hou, 1991; Liu et al., 2008), Cardiodictyon catenulum Hou et al., 1991, Hallucigenia fortis Hou and Bergstro¨m, 1995, Paucipodia inermis Chen et al., 1995a (see Hou et al., 2004), Megadictyon haikouensis Luo and Hu, 1999 (Luo et al., 1999; see also Liu et al., 2007), Miraluolishania haikouensis Liu et al., 2004 (see also Xiao, 2004); Jianshanopodia decora Liu et al., 2006, Onycho-

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dictyon gracilis Liu et al., 2008, and Diania cactiformis, Liu et al., 2011; and 4) Gondwana (Upper Ordovician): a described but unnamed xenusiid from the Soom Shale fauna in South Africa (Whittle et al., 2009). In addition, Kerygmachela kierkegaardi Budd, 1993 and Pambdelurion whittintoni Budd, 1997 from the Early Cambrian Sirius Passet were considered as having lobopodian affinities (Budd, 1993, 1997, 1999). Other potential lobopodians documented in the Middle Cambrian fossil record include Aysheaia? prolata Robison, 1985 from the Wheeler Formation, Acinocricus stichus Conway Morris and Robison, 1988 from the Spence Shale (see Ramsko¨ld and Chen, 1998), and the ‘‘Collins’ Monster’’ from the Burgess Shale (Collins, 1986). The terrestrialization of lobopodians could be dated at least prior to the Middle Pennsylvanian, provided Helenodora inopinata Thompson and Jones, 1980 recovered from the Mazon Creek fauna is a fossil onychophoran. Other crowngroup onychophorans were reported from the Cretaceous (Cretoperipatus burmiticus Engel and Grimaldi, 2002) and Paleogene (Tertiapatus dominicanus Poinar, 2000 and Succinipatopsis balticus Poinar, 2000) fossiliferous amber (Grimaldi et al., 2002; Poinar, 1996, 2000). The Chengjiang deposit, a Konservat-Lagersta¨tte paralleled by the celebrated Burgess Shale Phyllopod bed (e.g., Whittington, 1985), has hitherto served as a ‘‘Rosetta Stone’’ to unravel the origination and innovation of Phanerozoic metazoan body plans, including the first vertebrates Myllokunmingia and Haikouichthys (Shu et al., 1999) and the extinct but pivotal phylum Vetulicolia (Shu et al., 2001). This Lagersta¨tte has provided abundant data on Cambrian lobopodians in both their diverse morphologies and such exceptional anatomies as the eye, hypopharynx, intestine, mesentery, gut diverticulum, dermal papilla, and even the brain and nerve chord. Herein we describe another rare lobopodian, Antennacanthopodia gracilis n. gen. n. sp. from the Lower Cambrian (Series 2, Stage 3)

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Chengjiang deposit in the southwest of the then-existing Yangtze Platform, South China. PRESERVATION

Both type specimens of Antennacanthopodia gracilis n. gen. n. sp. are dorsoventrally compacted in a life position in laminated mudstone which is yellowish after moderate weathering. The holotype, about 1.4 cm in sagittal length (excluding appendages), is largely parallel to the bedding, except for the two rows of legs splaying downward and crosscutting the laminae at a very low angle. In high contrast against the matrix, the purplish black soft tissues and reddish brown hard parts of the organism are preserved in exquisite detail. Due to the comparatively fine-grained host sediments the holotype exhibits superior preservation as compared to the paratype. Such excellent preservation, together with lifeconditions of the specimens, suggests they were catastrophically buried in situ (obrution) and sedimentation took place in a restricted-shelf, shallow sea (see Babcock et al., 2001). Highly-sclerotized parts, such as leg spines and leg pads, both with preserved reliefs, present secondary mineralization by pyrite (weathered to dark reddish iron dioxide), a mode of preservation typical of the Chengjiang fossils which may have occurred during early diagenesis and played an essential role in the exceptional preservation (e.g., Gabbott et al., 2004; Ou et al., 2009). Such selective pyritization also appears along and dimly defines the integumentary outline. In contrast, soft tissues, such as the intestine and musculature, are represented by remains of carbonaceous films of purplish gray to black. SYSTEMATIC PALEONTOLOGY

Phylum LOBOPODIA Snodgrass, 1938 Order ARCHONYCHOPHORA Hou and Bergstro¨m, 1995 Genus ANTENNACANTHOPODIA Ou and Shu new genus Diagnosis.—Antennacanthopodia distinguished from other lobopodian genera by 1) onychophoran-like, small-sized body; 2) differentiated head with two muscular and slender appendage pairs (prominent frontal and second antenna) attached; 3) putative lateral eyes situated basal of frontal antennae; 4) trunk devoid of obvious annuli and sclerotized plates; 5) stout lobopods armed with annuli of thorn-shaped spines and disc-shaped terminal pads; 6) diminutive spines arrayed in transverse rows on non-limb trunk portions, and 7) putative cirriform appendicules attached to terminal projection of trunk. Etymology.—From Latin antennatus and acanthopodus, respectively referring to two distinctive generic characters: antennae and spinous lobopods. Type species.—Antennacanthopodia gracilis new species. ANTENNACANTHOPODIA GRACILIS Ou and Shu new species Figures 1, 2 Diagnosis.—Body onychophoran-like, small-sized, consisting of a differentiated head and a homonomous trunk. Head with two muscular and slender appendage pairs attached, modified as prominent frontal and second antenna. Putative lateral eyes situated basal of frontal antennae, if present. Trunk elongate and serially segmented into nine segments, lacking obvious cuticular annuli and sclerotized plates. Lobopods stout, each armed with a minimum of seven annuli of highly-sclerotized, thorn-like spines (,10 spines per annulus); each lobopod bears well-developed internal musculature, distally terminating in a hardened, disc-shaped walking pad. Diminutive spines arrayed in transverse rows (,four rows per segment) on dorsum and lateral sides of non-limb

trunk portions. A pair of putative cirriform appendicules attached to terminal projection of trunk. Digestive system simple, featured by a straight, spacious midgut along almost the length of trunk. Etymology.—Greek gracilis, graceful or slender, referring to the appearance of the species. Types.—ELEL-EJ081876 (Fig. 1), holotype, and ELIJS022643 (Fig. 2), paratype, respectively reposited in the Early Life Evolution Laboratory (ELEL), School of Earth Sciences and Resources, China University of Geosciences, Beijing, P. R. China, and the Early Life Institute (ELI), Northwest University, Xi’an, P. R. China; recovered from Erjie section, Kunyang in 2008, and Jianshan section (,10 km northeast of Erjie), Haikou in 2002, both located ,48 km west of the classic Maotianshan section in the vicinity of Chengjiang area, Yunnan, China. Occurrence.—Eoredlichia–Wutingaspis Biozone, upper Yu’anshan Member, Heilinpu (formerly Qiongzhusi) Formation, Lower Cambrian. Absolute dating of the stratigraphically lower Niutitang Formation (Guizhou, South China) constrains the age of Chengjiang fossils to be later than 518 6 5 Ma (Zhou et al., 2008). Taken together biostratigraphic considerations (e.g., Zhang et al., 2001, 2008, 2009), the horizon that yields the Chengjiang biota falls into the Cambrian Series 2, Stage 3, ca. 520 Ma. Description.—The head terminates in a vaulted, unsclerotized frontal portion, which is posteriorly succeeded by the first segment bearing a pair of frontal antennae (Fig. 1.1–1.5). Frontal antennae are muscular, slender, gently curved, and anterolaterally pointed, with the base dorsolaterally connecting into an internal dusky structure, say, the brain, central in the head region (Fig. 1.1). They are fully exhibited in the paratype (Fig. 2.1, 2.2), about double the sagittal length of the head and one fourth of the body. Weak striations are preserved at proximal region of the frontal antennae (Fig. 2.3). An antenniform outgrowth closely adjacent to the frontal antenna (Fig. 1.1, 1.5) tapers distally and is slightly stouter than the frontal antenna. It is interpreted as a modified head appendage, most likely representing the second antenna (Fig. 3), considering its resemblance to the frontal antenna in tint (purplish gray), shape, and dimension. No sclerotized features indicative of jaws are visible. Two black, sub-rounded specks symmetrically situated on the bases of the frontal antennae in the holotype (Fig. 1.3–1.5) might be visual organs (eyes/ocelli) or alternatively merely weathered pyrite framboids coincidently located in the approximate position of lateral eyes. A prominent, rounded region of dark purple tint posterior of the head is considered to be remains of the pharyngeal bulb, which constricts rearward as a narrow, short portion that may represent the esophagus (Fig. 1.1–1.5), both collectively constituting the foregut. In the paratype, a positive relief indicative of sediment infill is tinted by purplish organic remains and occupies the posterior of the pharynx and the entire esophagus (Fig. 2.1). The cuticular outline of the trunk is markedly preserved in the holotype (Fig. 1.1, 1.3). The trunk is elongate and subequal in width, consisting of a longitudinal series of nine homonomous segments, each supported by a pair of lobopodal legs, and an endmost projection probably bearing cirriform structures. The trunk width reaches an acme at the segment bearing the fifth leg pair and slightly deceases anteriorly and posteriorly. Transverse rows of tiny spines adorn the surface of the trunk, with four rows on each segment. They are distributed on dorsal and lateral sides of non-limb trunk portions, observed in particular between the

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FIGURE 1—Holotype of Antennacanthopodia gracilis n. gen. n. sp. (ELEL-EJ081876), Lower Cambrian Heilinpu Formation, Yunnan, China. 1, part, overall view of complete specimen, head region defined by frontal and second antennae and inferred lateral ocelli, trunk with paired, muscular lobopods (armed with tiny spines and terminated in disc-shaped leg pads), a straight, spacious midgut, and putative posterior cirriform appendicules; 2, interpretive drawing of 1, dark patches represent organic remains; 3, overall view of counterpart, note the spacious midgut, body cavity, and paired, segmental leg musculature; 4–5, enlarged views of head region in 3 and 1, respectively, showing the vaulted frontal portion, the frontal and second antennae, and potential lateral ocelli (arrowheads); 6–7, enlargement of lobopods L2 and L4 (part) respectively, showing terminal, heavily-sclerotized pad-like structures, and sharply pointed spines (arrowheads) both on the leg and trunk; 8–9, enlarged views of lobopods L5 and L6 (counterpart), respectively, both developed with internal muscle tissues and armed with annuli of highly-sclerotized, radially arrayed spines (staggered pattern of arrangement shown in 9); 10, enlarged view of the endmost portion of the trunk (Part), showing a hardened end attached with a pair of cirriform structures (arrowheads). Abbrevations: An5frontal antenna; Ans5second antenna; Bc5body cavity; Bm5body-wall musculature; Br5brain; Es5esophagus; Fp5frontal portion; Hr5head region; L1–L9, left lobopod 1–9; Lm5leg musculature; Lp5leg pad; Mg5midgut; Oc5Ocellus; Pa5posterior terminal appendicule; Ph5Pharynx; Pp5posterior projection; R1–R9, right lobopod 1–9; Sp5Spine; Tr5Trunk region. Scale bars represent 1 mm for 1–5 and 10; 500 mm for 6–9.

second and fourth leg pairs (Fig. 1.1, 1.2, 1.7). By extrapolation, this feature is common to other trunk portions. No paired sclerotized plates are visible along the trunk sides. Nor is there any tubercular structure on the trunk. The body cavity can be observed from the holotype (Fig. 1.1, 1.3) as represented by the void between the body wall (defined by the cuticular outline) and internal structures (e.g., intestine and musculature), extending into the legs (Fig. 1.6–1.9). The midgut is interpreted as the longitudinal, purplish black, straight, broad band running through the trunk. It is anteriorly connected to the above-mentioned esophagus, and can be traced along almost the entire length of body (Figs. 1.1,

1.3, 2.1, 2.2). In the holotype, the midgut is centrally situated in the trunk and of approximately even width, accounting for about 50 percent of the trunk width (Fig. 1.1, 1.3). Positive reliefs of fine sediments are present at the frontal and middle portions in the paratype (Fig. 2.1). Both specimens exhibit nine pairs of unjointed, stout legs (lobopods) ventrolaterally splaying on both sides (Figs. 1.1, 1.3, 2.1, 2.2). The legs in the holotype (part), in particular the right row, slant slightly downward relative to the trunk, being revealed after preparation. Based on disposition of leg spines (Fig. 1.6, 1.9), the legs must have originally been circular in cross-section. The leg length in the holotype, measured from the distal tip to the midpoint the overlying alimentary canal

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FIGURE 3—Reconstruction of Antennacanthopodia gracilis n. gen. n. sp. in life. Notice the frontal and second antennae, putative visual organs, lobopodal legs armed with annuli of thorn-like spines, sclerotized walking pads, trunk spines, and posteriormost projection with a pair of cirriform structures. Scale bar51 mm.

FIGURE 2—Paratype of Antennacanthopodia gracilis n. gen. n. sp. (ELIJS022643), Lower Cambrian Heilinpu Formation, Yunnan, China. This specimen exhibits a seemingly slenderer appearance owing to the carcass devoid of cuticular outline. 1–2, part and counterpart respectively, showing the head region with frontal antennae (arrowheads), trunk with nine pairs of lobopods, voluminous midgut, and leg musculatures; 3, enlargement of the head region, showing the frontal antenna with transverse striations (arrowheads); 4, lobopod L4 (part) terminated in a sclerotized leg pad (arrowhead); 5, lobopod R3 and R4 (counterpart) and partial trunk, showing also the preserved muscles, midgut, and leg spines arrayed in circlets. Scale bar represents 1 mm for 1–3; 500 mm for 4–5.

crosscuts the internal tissue of the leg, shows a trend of being longer and sturdier in the middle of each row. The remains of extrinsic leg musculature, the internal soft tissue in each leg, is superbly preserved as a stubby, purplish gray band extending through the entire leg (Figs. 1.1, 1.3, 2.1, 2.2). The muscle insertions occupy a large portion of the leg cavities; their size varies in accord with that of the legs. In the holotype, the broader, proximal base of the muscle tissue attaches to what may be organic remains of body-wall musculature locally preserved underlying the darker midgut (Fig. 1.1, 1.3, 1.8, 1.9). Distally the muscle tissues tapers gently and attaches to a hardened disc structure at the tip. Thorn-like, sharply pointed leg spines are highly sclerotized and radially arranged in at least seven annuli or circlets on the surface of each lobopod (Fig. 1.6–1.9). They appear stiff and are conical in shape. The spatial relationship between the leg and the spines is clearly demonstrated in both specimens (Figs. 1.8, 1.9, 2.5), where spines of an individual annulus extend radially relative to the center of the leg cross-section. About 10 spines are distributed equidistantly along each circlet. Succeeding circlets show an apparent staggered pattern of arrangement (Fig. 1.9). The spine dimension gradually increases towards the proximal base of the leg (Fig. 1.8, 1.9).

Neither feet nor claws can be identified from the distal end of legs in both specimens, but a heavily-sclerotized, discshaped structure is interpreted here as leg pads. These hardened pads or ‘‘cushions’’ might have reinforced walking. The pads are represented by reddish brown iron oxide with positive relief and high rigidity (Figs. 1.6, 1.7, 2.4). They are connected to the distal tip of leg musculature. A pair of soft, cirriform structures protruding from the sclerotized terminal projection in the holotype is tentatively proposed as endmost, posterior appendicules (Fig. 1.1, 1.2, 1.10). The right branch winds rearward and extends approximate 60 percent the body length, whereas the left branch is poorly preserved with most of it broken from the slab. The appendicules are preserved with a pinkish tint and appear to have been highly flexible. COMPARISON AND DISCUSSION

Comparison to extant onychophorans.—The grade of organization to which Antennacanthopodia gracilis n. gen. n. sp. shows the most similarities is the living Onychophora, both in gross morphology and in anatomical details (Figs. 1–3). First, the most striking feature in the new form is the frontal, fleshy, gently tapering antennae (Figs. 1.1, 2.1, 2.2), conceivably functioning as prime tactile/chemosensory receptors. Transverse striae preserved at the proximal region probably suggest remains of circular muscles or dermal annuli on the antenna. In the living onychophorans, an almost identical structure (in terms of position, shape, and proportion to the body size) also exists as a key diagnostic characteristic for the phylum. The onychophoran antenna proves to be a modified anteriormost head appendage based on ultrastructural data (Mayer and Koch, 2005) and supported by the anterior-posterior order of innervation of head structures (Eriksson and Budd, 2001; Eriksson et al., 2003). We consider the frontal antenna as one of the essential plesiomorphies (ancestral traits) that have evolved from ancestral lobopoidans and still persist in the extant onychophorans, the former being the forerunner of typical onychophoran frontal appendages or antennae. Attached adjacent to the frontal antennae and more laterally positioned, the second antenna partially preserved in the holotype bears a resemblance, and might be a homologue, to the slime papilla in Onychophora, although the former could not have functioned similarly as the terrestrial form ejects a powerful adhesive to entangle prey. Second, the lobopods of Antennacanthopodia are unjointed and stout, mediated by well-developed musculature, each with an internal lumen continuous with the body cavity (Fig. 1), thus strongly reminiscent of the lobopodal legs of living

OU ET AL.—RARE ONYCHOPHORAN-LIKE LOBOPODIAN FROM CHINA onychophorans. Still noteworthy is a single, hardened, disclike leg pad or ‘‘cushion’’ equipped at the distal end of each leg. The leg pads are highly sclerotized and appear much more resistant to decay, excluding the possibility that it has been used as an attachment disc or a holdfast. Instead, they are in function comparable to the onychophoran ‘‘spiny’’ walking pads, used to walk over smooth substrates, and on which the leg sits in its resting position (Brusca and Brusca, 2003). Given the dorsoventral preservation, it is unknown whether or not spines are present on the leg pad’s undersurface; if present, these spines would correlate with the sensilla or ‘‘spines’’ on the foot pads of velvet worms. Viewed from the layout of muscle bands, the frontal six leg pairs seem directed forward, whereas the seventh and eighth directed rearward, especially in the counterpart (Fig. 1.3). This circumstance probably suggests that contralateral legs of a segment moved synchronously rather than alternating in this fossil form, being consistent with the modern onychophoran gait. Third, the putative visual organs in the new form show most similarities with the living onychophorans. They correspond well with the beady eyes of living onychophorans such as Epiperipatus biolleyi (Mayer, 2006) in both lateral position and proportion to the head. The onychophoran eyes and antennae are considered situated on the same segment based on results from onychophoran head development (Eriksson et al., 2003). Intriguingly, the disposition of the eye relative to the frontal antenna in the new form seems to provide paleontological evidence for this conclusion. Fourth, the simple digestive system in the specimens can be compared to that of the living onychophoran, which also possess a prominent, straight, endodermal midgut as sites of extracellular digestion and absorption. Superficially, the purplish gray bands of organic remains within each leg, which we interpret as the leg musculature, are somewhat similar to segmentally arranged alimentary diverticula branching from the midgut and extending into each leg, a trait typical of the digestive system of chelicerate arthropods, in particular arachnids and pycnogonids, but lacking in extant Onychophora and Tardigrada. Similarly, a dark strand of ‘‘central canal,’’ usually preserved with a dark tint fainter than that of the alimentary canal, also exists in the legs of most known Cambrian lobopodians such as Hallucigenia (Conway Morris, 1977; Chen et al., 1995b), Microdictyon (Ramsko¨ld and Hou, 1991; Chen et al., 1995a), Onychodictyon (Hou et al., 1991; Ramsko¨ld, 1992; Liu et al., 2008), Paucipodia (Chen et al., 1995b; Hou et al., 2004), Cardiodictyon (Chen et al., 1995b; Hou et al., 2004), Jianshanopodia (Liu et al., 2006), Megadictyon (Liu et al., 2007), and Luolishania (Ma et al., 2009). This feature was variably interpreted as either the alimentary diverticulum, the blood vessel, the hydrostatic system, the nervous system, or a combination of these (see Conway Morris, 1977; Ramsko¨ld, 1992; Bergstro¨m and Hou, 2001; Hou et al., 2004). Neuroanatomical evidence seems to support the close affinity of onychophorans with chelicerates (Strausfeld et al., 2006; but see Mayer and Whitington, 2009 for different views), which implies the plausible existence of alimentary diverticula in fossil lobopodians. However, similar ‘‘central canals’’ can also be observed within papillae or appendicules protruding from the leg and the trunk in Onychodictyon (Liu et al., 2008, fig. 1), as well as within dendritic branches of the limbs in Jianshanopodia (Liu et al., 2006), which to some degree renders their use as intestinal ceca or diverticula impossible. Circumstances in favor of the dark tissue within each leg as musculature rather than digestive ceca are: 1) This structure is

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highly comparable to the complex leg musculature in extant velvet worms (unpublished data from Georg Mayer, private correspondence, 2009); 2) Purplish gray tint preserved in this tissue is similar to that of the antenniform head appendages, but distinct from the much darker midgut (Figs. 1.1, 1.3, 2.1, 2.2); 3) In contrast to the ‘‘central canal’’ in other known lobopodians’ leg, this structure is much more stout and conspicuous, proximally displaying a connection to the tissue (could be the body-wall musculature) adjoining the midgut rather than to the midgut itself; 4) It is distally terminated and attached to the leg pad (Fig. 1.1, 1.3, 1.6–1.9) and might have functioned as retractors; 5) It differs in essence from the reniform digestive ceca in Chengjiang lobopodians Jianshanopodia (Liu et al., 2006) and Megadictyon (Liu et al., 2007), and in Sirius Passet Pambdelurion (Budd, 1997); and 6) Extant chelicerates, especially pycnogonids, are characterized by a greatly reduced body (hence the nickname ‘‘no-bodies’’), thus gut ceca and even gonads are squeezed into the legs. However, it seems unlikely for the new form to accommodate additional digestive organs in the legs, given its voluminous midgut within a broad trunk (Fig. 1.1, 1.3). Finally, in onychophorans, transverse annulations ubiquitously present on the trunk and appendages are an adaption for flexibility, and a manifestation of subcutaneous arrangement of transverse hemal channels with surrounding circular musculature. This feature also occurs as an important plesiomorphy in ancestral lobopodians, although it also existed in other fossil groups such as palaeoscolecids. Evidence for annulations in Antennacanthopodia is weak. Nevertheless, striae preserved on the frontal antenna, annuli of leg spines, as well as trunk spines preserved in transverse rows (Fig. 1.6–1.9) suggests the existence of annulations in the new form. In addition, the body cavity and the terminal projection in Antennacanthopodia are also comparable to that in onychophorans. Soft tissues adjacent to the midgut and connected to the leg musculature (Fig. 1.1, 1.3) in the new form presumably represent remains of body-wall musculature, which might be in accord with the circular, oblique, and longitudinal muscles that collectively constitute the onychophoran body wall. Comparison to Cambrian lobopodians.—This new form resembles the Burgess Shale Aysheaia (see Hutchinson, 1930; Delle Cave and Simonetta, 1975; Whittington, 1978) in the overall shape, effacement of sclerotized plates on the trunk, presence of frontal modified appendages, a seemingly terminal mouth, and stubby, spine-bearing lobopods. In contrast, the spines of the frontal appendages in Aysheaia are directed antero-laterally, while the lobopod spines pointed forwards or backwards in one direction, which differs essentially from the radial leg spines in the new form. The trunk posteriorly merges with the last leg pair in Aysheaia, whereas in the new form, a trunk projection exits posterior to the last leg pair. Besides, the stout legs of Antennacanthopodia seem to lack terminal claws, a scenario different from some Chengjiang lobopodians having slenderer, clawed limbs (e.g., Microdictyon, Hallucigenia, Miraluolishania, Onychodictyon). The new form shares with Miraluolishania a defined head region (Liu et al., 2004). Antenniform structures have been reported in Miraluolishania (Liu et al., 2004), Luolishania (Ma et al., 2009), and Onychodictyon (Ramsko¨ld and Hou, 1991; Liu et al., 2008). Nevertheless, when compared to the undisputable frontal antennae in Antennacanthopodia, they are flagellate and appear less typical of onychophoran antennae. Potential visual organs are observed not only in Miraluolishania (Liu et al., 2004), Luolishania (Ma et al., 2009), but in Hallucigenia, Paucipodia, and Onychodictyon

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(Ou, unpublished finding from new material). However, in contrast to the dorsal eyes in Miraluolishania (Schoenemann et al., 2009), the ocellus-like structures in the new form are apparently laterally situated on the head region. The endmost cirriform structure pair, which may have functioned as tactile/chemosensory receptors or as a prehensile organ to aid in locomotion, resembles the caudal furcae in Kerygmachela, a basal arthropod or ‘‘gilled’’ lobopodian (Budd, 1993; Edgecombe, 2010), thus implying that it could be a segmental structure. However, the possibility could not be excluded that they were just viscera (such as gut or genital ducts) coming out from the anus or the genital opening owing to the hemolymph pressure inside, since such postmortem circumstances occur in extant onychophorans (Georg Mayer, private correspondence, 2009) PHYLOGENETIC IMPLICATIONS

Onychophoran affinity.—Paleozoic lobopodians have been generally accepted having onychophoran affinities (Hutchinson, 1930; Whittington, 1978; Dzik and Krumbiegel, 1989; Ramsko¨ld and Hou, 1991; Hou and Bergstro¨m, 1995). Compared to other known lobopodians, Antennacanthopodia gracilis n. gen. n. sp. shows the most resemblances to extant terrestrial Onychophora in many aspects. These similarities are considered as indicating their homologies and a close affinity rather than a convergence of adaptations to similar environments or habitats. We consider the following characters as potential homologous features shared by the new form and extant onychophorans: 1) muscular, unjointed, anterior antenna, 2) lateral ocellus-like visual structures, 2) metamerically segmented body covered by lightly sclerotized cuticle, 3) unsegmented lobopod mediated by internal musculature and armed with 4) terminal walking pad. In addition, the vaulted, unsclerotized frontal portion of the head (Fig. 1.1, 1.3) in the new form implies an antero-apically positioned, primeval mouth (see Eriksson and Budd, 2001; Eriksson et al., 2003; Scholtz and Edgecombe, 2006 for discussions on ancestral position of the mouth in Onychophora and Arthropoda groundplans). Thus, this extinct form probably displays a ‘‘groundplan’’ for Onychophora and could be viewed as a representative of an ancestral lobopodian stock that may have evolved and given rise to extant onychophorans. Arthropod affinity.—Basal arthropods may have evolved from ancestral lobopodians (see Budd and Telford, 2009 and Edgecombe, 2009 for a review). Cephalization, condensation of frontal segments into an anterior tagma responsible for primary functions, is considered a critical scenario in arthropod evolution (e.g., Mu¨ller, 1996; Scholtz and Edgecombe, 2006). Antennacanthopodia exhibits the acquisition of arthropod characters to some extent, most notably the distinctive head region, which seemingly consists of two fused frontal segments, each being expressed by an antenniform head appendage. Previous work has repeatedly suggested a two-segmented head as an ancestral feature of arthropods (e.g., Chen et al., 1995c; Waloszek et al., 2005, 2007). Supporting evidence also comes from investigations into onychophoran brain development (Mayer et al., 2010), which suggests that the last common ancestor of Onychophora and Arthropoda possessed a two-segmented brain. Antennacanthopodia seemingly possesses, besides other characters, a head composed of only two segments, i.e., those bearing the frontal antenna and the second antenniform appendage. The frontal antenna, in conjunction with the putative visual structure located at the base, can thus be considered an anteriormost appendage-

bearing ‘‘ocular segment,’’ as purported to exist in the euarthropod groundplan (Budd, 2002; Eriksson et al., 2003). Taken together with the notion that onychophorans are the closest living relatives of arthropods (e.g., Ballard et al., 1992; Aguinaldo et al., 1997; Dunn et al., 2008; Mayer and Whitington, 2009), Antennacanthopodia gracilis n. gen. n. sp. offers remarkable potential to fill the wide gap separating extant arthropods from their sister group, onychophorans, and can be reasonably positioned on the stem lineages of the extant panarthropod clades. ACKNOWLEDGMENTS

This paper has benefited from valuable comments and constructive critiques provided by G. Mayer (Department of Genetics, Friedrich-Schiller-University Jena, Germany). Special thanks are also due to Ge Sun (China University of Geosciences, Beijing) for her painstaking line drawings. Insightful comments by referees G. B. Budd and X. G. Zhang greatly improved the paper. We thank J. P. Zhai, M. R. Cheng (Early Life Institute, Northwest University, Xi’an, China), and native workers (Y. X. Han, J. G. Xiao, G. H. Xiao, Y. L. Xiao, L. F. Li, J. L. Li, Y. P. Li, H. L. Xu, F. X. Zhao, H. P. Li, L. H. Gao, A. N. Zhou, and H. Z. Xiao) for their strenuous field work. Financial support for this study is provided by the National Natural Science Foundation of China (Grant No. 40802011, 40830208, and 40602003), the National 973 Project (Grant No.2006CB806401), the Fundamental Research Funds for the Central Universities (2010ZY07), and the Program for Changjiang Scholars and Innovative Research Team in University (PCSIRT). REFERENCES

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