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New macrobenthic cycloneuralians from the Fortunian (lowermost Cambrian) of South China
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New macrobenthic cycloneuralians from the Fortunian (lowermost Cambrian) of South China ⁎
T.Q. Shaoa, J.C. Qina, Y. Shaoa, Y.H. Liua, , D. Waloszekb, A. Maasc, B.C. Duand, Q. Wanga, Y. Xua, ⁎ H.Q. Zhange, a
School of Earth Science and Resources, Chang’an University, Xi’an 710054, China University of Lund, Sölvegatan 12, SE-22362 Lund, Sweden c Galgenackerweg 25, 89134 Blaustein, Germany d Research Center for Islands and Coastal Zone, First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China e State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing 210008, China b
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A B S T R A C T
Keywords: Scalidophora Cycloneuralia Ecdysozoa Cambrian Fortunian stage South China
Although morphology-based phylogenetic analyses and molecular data suggested that the cycloneuralians might have emerged in the Ediacaran Period, the oldest known fossil remains of cycloneuralians were first reported from the Cambrian Fortunian Stage of South China, and to date four genera and species as well as nine indeterminate forms have been described. Here, we report the latest discoveries of cycloneuralians from the Fortunian Kuanchuanpu Formation at Zhangjiagou Lagerstätte, Dahe Village, Xixiang County, southern Shaanxi Province, South China. A new genus and species Dahescolex kuanchuanpuensis n. gen. n. sp. is described, and a previously reported genus and species Eopriapulites sphinx is re-described. Dahescolex kuanchuanpuensis n. gen. n. sp. is suggested to be a stem-lineage derivative of Scalidophora, whereas E. sphinx may represent a stem-lineage derivative of Cycloneuralia. From the fragments discovered, the new specimens are suggested to have reached millimeters in dimension, and the original individuals are estimated to have dimensions in centimeter, hence falls within the size range of macrobenthos. Therefore, at least some of the Fortunian cycloneuralians can be considered macrobenthic, and it is suggested here that the Cycloneuralia may have originated in the Fortunian macrobenthos.
1. Introduction Morphology-based phylogenetic analyses propose that the Scalidophora (Priapulida, Loricifera and Kinorhyncha) and Nematoida (Nematoda and Nematomorpha) are sister taxon to each other, and they constitute the monophyletic Cycloneuralia (Ax, 2003; Nielsen, 2012; Giribet and Edgecombe, 2017). Cycloneuralians might have emerged in the Ediacaran Period and diversified in the early Cambrian (RotaStabelli et al., 2013). Although some trackways from the Ediacaran Period may have possibly been produced by some cycloneuralians or appendage-bearing bilaterians (Chen et al., 2018), the oldest known unambiguous fossils of cycloneuralians occurred in the Cambrian Fortunian Stage (Liu et al., 2014a; Zhang et al., 2015). As cuticle-bearing animals, cycloneuralians have relatively strong fossilisation potential relative to other taxa with simple epidermis, and thus not surprisingly left abundant fossils in the Cambrian Konservat-Lagerstätten (Maas,
⁎
2013). Previously reported Cambrian cycloneuralians occur mainly in Stage 3 and younger strata (Maas, 2013), such as the typical Burgess Shale-type Lagerstätten (Conway Morris, 1977; Briggs et al., 1994; Hou et al., 2017) and the Orsten-type Lagerstätten (Liu et al., 2014a, 2019; Maas et al., 2007a; 2009; Shao et al., 2018; Zhang et al., 2015, 2018), with minor occurrences as Small Carbonaceous Fossils (Harvey and Butterfield, 2017; Slater et al., 2018). In Stage 2, only a single species, known exclusively from embryos, was reported (Bengtson and Yue, 1997). In the Fortunian Stage, the cycloneuralians were not reported until 2014, and to date four genera and species as well as nine indeterminate forms have been described (Liu et al., 2014a, 2019; Shao et al., 2016, 2018; Zhang et al., 2015, 2018). Because of their occurrence close to the origin and early diversification of the cycloneuralians, the Fortunian cycloneuralians provide the possibility of helping to reconstruct the last common ancestors of Cycloneuralia and its ingroups Nematoida and Scalidophora.
Corresponding authors. E-mail addresses: [email protected] (Y.H. Liu), [email protected] (H.Q. Zhang).
https://doi.org/10.1016/j.precamres.2019.105413 Received 5 March 2019; Received in revised form 18 June 2019; Accepted 8 August 2019 0301-9268/ © 2019 Elsevier B.V. All rights reserved.
Please cite this article as: T.Q. Shao, et al., Precambrian Research, https://doi.org/10.1016/j.precamres.2019.105413
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Fig. 1. Location map and stratigraphic column of the Zhangjiagou section in southern Shaanxi Province, South China. The key horizon yielding the current specimens is denoted by an arrow.
Geology and Palaeontology. In order to detect possible internal biologic structures, selected specimens were scanned using Micro-CT at Nanjing Institute of Geology and Palaeontology, and the Micro-CT data were analyzed using Amira 5.3. The current specimens are deposited at the University Museum of Chang’an University (UMCU), Xi'an.
Here, we describe new material of cycloneuralians from the Fortunian Zhangjiagou Lagerstätte in southern Shaanxi Province, South China. Although fragmentarily preserved, the new material suggests that these specimens have reached several millimeters in dimensions, and the original individuals may be at a centimeter scale, thus falling within the size range of the macrobenthos.
3. Systematic palaeontology 2. Materials and methods
Cycloneuralia Ahlrichs, 1995
The current specimens were extracted from the lower part of the second member of the Kuanchuanpu Formation at the Zhangjiagou Lagerstätte (Shao et al., 2018), Dahe Village, Xixiang County, southern Shaanxi Province, South China (Fig. 1). They are three-dimensionally phosphatized and soft-bodied, i.e., with Orsten-type preservation (Müller and Walossek, 1991; Waloszek, 2003; Maas et al., 2006). The key horizon that yielded the present material has previously been constrained to be part of the small shelly fossils Anabarites trisulcatus–Protohertzina anabarica Assemblage Zone (Li, 1984; Liu et al., 2014b, 2014a; Shao et al., 2018; Steiner et al., 2014; Zhang et al., 2015), and has an estimated age of about 535 Ma (Steiner et al., 2007, 2014), within the Fortunian Stage of the Cambrian Period (Peng et al., 2012). As in the previous studies (Liu et al., 2014b, 2014a, 2019; Shao et al., 2018; Zhang et al., 2015), rock samples from the key horizon at the Zhangjiagou section were processed through a routine etching method with diluted acetic acid (10%) at the Chang’an University. Undissolvable residues were dried naturally and then handpicked under a binocular microscope. Microfossils were picked out and mounted on aluminum stubs for observation under an LEO 1530VP field-emission environmental scanning electron microscope at the Nanjing Institute of
Genus Dahescolex Zhang HQ, Shao TQ, and Liu YH new genus
Type and single species.—Dahescolex kuanchuanpuensis Zhang HQ, Shao TQ, and Liu YH new genus and new species, by monotypy. Diagnosis.—As for the type species. Occurrence.—Kuanchuanpu Formation, Zhangjiagou section, southern Shaanxi Province, South China; Anabarites trisulcatus–Protohertzina anabarica Assemblage Zone, Fortunian Stage, Cambrian. Etymology.—From Dahe, with reference to its occurrence in Dahe Village, and scolex, Greek, worm. Dahescolex kuanchuanpuensis Zhang HQ, Shao TQ, and Liu YH new genus and new species Figs. 2–4, Supplementary data set 1. Holotype and single specimen.—UMCU 13CHD0718-006, a possible juvenile or young adult, from the Fortunian Kuanchuanpu Formation at Zhangjiagou section, southern Shaanxi Province, South China. Diagnosis.—Body bi-partite, composed of an anterior part, the 2
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Fig. 2. Dahescolex kuanchuanpuensis n. gen. n. sp. from the Cambrian Fortunian Zhangjiagou Lagerstätte. (1) holotype, UMCU 13CHD0718-006; (2) left lateral view of (1); (3) opposite side of (1), showing the preserved trunk part, A1–A6 refer to the first to the sixth annuli; (4) right lateral view of (1). Scale bar represents 1 mm.
arranged in longitudinal rows (Fig. 3.1). Between every two longitudinal rows of scalids, there are additional two longitudinal rows of relatively small scalids, extending only from the second to the fifth circlets (Fig. 3.1). The trunk is demarcated off from the proboscis by the beginning of the first trunk annulus (Fig. 2). The trunk portion of the specimen at hand indicates that the species had at least six annuli, each with an annular ring of five to seven spinose sclerites (Fig. 2.3). The lengths of the annuli are more or less the same. Spinose sclerites are positioned at the anterior part of each annulus, and take up two-thirds or three-quarters of the annular length. The anterior margin of the spinose sclerites is aligned with the anterior margin of the annulus. The spinose sclerites have an expanded and long elliptic base and a spine antero-centrally. The bases of the sclerites do not contact with those of the adjacent ones, with membranous cuticle in between. There is a large spinose sclerite straddling on the fifth and sixth annuli. The large spinose sclerite has an expanded, round base and a central spine. The posterior part of the trunk is unknown in the specimen at hand. Etymology.—From kuanchuanpu, with reference to its occurrence in the Kuanchuanpu Formation. Comparisons.—Dahescolex kuanchuanpuensis n. gen. n. sp. differs
proboscis and a posterior part, the trunk; proboscis composed of an anterior region, the teeth-bearing pharynx, and a tubular posterior region, the introvert, with at least eight circlets of spine-shaped, internally hollow scalids; scalids arranged in longitudinal rows; between every two rows of scalids there are additional two longitudinal rows of relatively small scalids, extending only from the second to the fifth circlets; trunk with at least six annuli, each with an annular ring of spinose sclerites. Occurrence.—Kuanchuanpu Formation, Zhangjiagou section, southern Shaanxi Province, South China; Anabarites trisulcatus–Protohertzina anabarica Assemblage Zone, Fortunian Stage, Cambrian. Description.—The body of Dahescolex kuanchuanpuensis n. gen. n. sp. is composed of two major body regions (Fig. 2). The anterior part is the proboscis, and it is subdivided into the pharynx, as the expandable and intrudible anterior end of the esophagal part of the gut, and a posterior more or less tubular region, called introvert. The pharynx and its teeth are unknown in the specimen at hand. The introvert bears at least eight circlets of cuticular scalids (Fig. 3.1). The scalids are long, spine-shaped (Figs. 2.1, 3.1, 3.3) and internally hollow (Figs. 2.2, 3.2), and are
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Fig. 3. Dahescolex kuanchuanpuensis n. gen. n. sp. from the Cambrian Fortunian Zhangjiagou Lagerstätte. (1) close-up of the introvert of the holotype UMCU 13CHD0718-006 (Fig. 2.1), sc1–sc8 refer to the first to the eighth circlets of scalids, numbers and white arrows denote the scalids in each circlet, and black arrows denote the relatively small scalids; (2) right lateral view of (1), arrows indicate the internally hollow scalids; (3) left lateral view of (1), arrow indicates a spine-shaped scalid. Scale bar represents 500 μm.
considered embryonic, because the worm-like forms were found embedded in an egg case, though completely annulated and with anterior and posterior spine structures preserved, is Markuelia, found in the middle Cambrian rocks in Australia and middle and upper Cambrian rocks of South China (Haug et al., 2009; Dong et al., 2010). Also here, there are clear differences to D. kuanchuanpuensis gen. et sp. nov., e.g. in the arrangement pattern of the introvert scalids, or the presence/absence of sclerites on the trunk. Measurements.—The holotype UMCU 13CHD0718-006 (Fig. 2.1) is about 3.73 mm long and 1.58 mm wide. The proboscis is about 2.99 mm long, and 1.01 mm wide at its basal part, whereas the trunk part is about 3.40 mm long and 1.49 mm wide. Because the specimen is flattened, the original diameter of the proboscis and the trunk part is about 643 μm and 949 μm, respectively. The scalid in the second circlet (Fig. 3.1) is about 555 μm long and 160 μm wide at the base, and a relatively small scalid beside it is about 262 μm long, and 52 μm wide at its base. The base of the large spinose sclerite is about 500 μm in diameter, and the base of each spinose sclerite is about 430 μm long and 170 μm wide. Each annulus is about 650 μm long. Reconstruction.—An artistic reconstruction of Dahescolex kuanchuanpuensis n. gen. n. sp. is presented in Fig. 4. Remarks.—Micro-CT analysis suggests that the holotype of Dahescolex kuanchuanpuensis n. gen. n. sp. is internally solid (Supplementary data set 1).
from the co-occurring Eopriapulites sphinx Liu and Xiao in Liu et al., 2014a (Liu et al., 2014a; Shao et al., 2016, 2018) in the arrangement pattern of the introvert scalids and also in the presence/absence of sclerites on the trunk. Dahescolex kuanchuanpuensis n. gen. n. sp. differs from the coeval Eokinorhynchus rarus Zhang et al., 2015 in that E. rarus has annular rings of closely-spaced rectangular plates without spines, randomly distributed spines, and bilaterally positioned large spinose sclerites, and also in that E. rarus has pentaradially arranged introvert scalids. Dahescolex kuanchuanpuensis n. gen. n. sp. differs from the Qinscolex and Shanscolex (Liu et al., 2019) in the arrangement pattern of the introvert scalids and also in the shape and arrangement of the spinose sclerites on the trunk. Dahescolex kuanchuanpuensis n. gen. n. sp. differs from the palaeoscolecids in that the latter forms have long and slender trunks with annular ring(s) of plates with nodes, platelets, or microplates (Müller and Hinz-Schallreuter, 1993; Zhang and Pratt, 1996; Duan et al., 2012; Liu et al., 2018). Assuming that D. kuanchuanpuensis n. gen. n. sp. lacks loricae at this ontogenetic stage, it is different from the loricate Eolorica deadwoodensis Harvey and Butterfield, 2017. Shergoldana australiensis Maas et al., 2007a from the middle Cambrian of Australia is known only from its small, possibly earliest larval semaphoront/larval stage, measuring no more than 120 µm in length. Its subdivision into (intruded) pharynx and four more body regions sets it off until now from the new species and all other described Cambrian fossils assigned to Cycloneuralia, but its shared features like the sclerites with spines and bifid trunk end make it clearly an interesting form for future discussions of the basic set of features of this group and further evolutionary developments of its ingroup taxa. Orstenoloricus shergoldii Maas et al., 2009 from the middle Cambrian of Australia was also established on larval forms. They possess a trunk region made of 20 plates, thus representing a lorica, and, accordingly, were clearly assignable to the taxon Vinctiplicata (sister taxon to Kinorhyncha; Ax, 2003) within Scalidophora. Therefore, closer systematic relationships of the two Australia species with D. kuanchuanpuensis gen. et sp. nov. are currently ruled out. Another taxon, based on larval stages, often
Genus Eopriapulites Liu and Xiao in Liu et al., 2014a
Type and single species.—Eopriapulites sphinx Liu and Xiao in Liu et al., 2014a from the Fortunian Zhangjiagou section, southern Shaanxi Province, by original designation. Diagnosis.—As for the type species. Occurrence.—Kuanchuanpu Formation, Zhangjiagou section, southern Shaanxi Province, South China; Xinli Member, Dengying Formation, Xinli section, northern Sichuan Province, South China; Anabarites trisulcatus–Protohertzina anabarica Assemblage Zone, Fortunian Stage, Cambrian. Eopriapulites sphinx Liu and Xiao in Liu et al., 2014a
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Fig. 5. Eopriapulites sphinx Liu and Xiao in Liu et al., 2014a from the Cambrian Fortunian Zhangjiagou Lagerstätte. (1) UMCU 14CHD0816-007; (2) opposite side of (1); (3) UMCU 14CHD0816-008; (4) opposite side of (3); (5) UMCU 14CHD0816-009, lateral view; (6) posterior view of (5). Scale bar represents 1 mm.
proboscis, and a posterior part, the trunk; proboscis consisting of a pharynx with multiple circlets of pharyngeal teeth, 18 of which are present in the basal circlet, and each has a base and an apical cusp, an eversible collar with possibly 12 anteriorly directed coronal scalids, an eversible introvert with 12 circlets of nine scalids, each circlet alternates with the adjacent one(s), forming 18 longitudinal rows; coronal and introvert scalids spine-shaped and internally hollow; trunk densely annulated, with estimated several hundreds or even thousands of microannuli; pits distributed at random at the middle trunk part; posterior trunk part decreasing in diameter gradually toward the end; a sharp decrease of diameter before the terminal end; terminal end with longitudinal striations. Description.—The general morphology of Eopriapulites sphinx follows Liu et al. (2014a) and Shao et al. (2016), with only minor revisions to the trunk. The trunk is tube-shaped, with densely-spaced microannuli (Figs. 5.1–5.4, 6.1, 6.2). On the middle part of the trunk, there are some pits (Fig. 6.1, 6.2). The pits are situated on the microannuli or inserted in between two adjacent microannuli; they appear to be distributed at random. Each pit (Fig. 6.3) has a central hole housing a ball-shaped structure. The major part of the trunk has uniform diameter (Fig. 5.1, 5.2), but it decreases slightly and gradually toward the posterior end (Fig. 5.3, 5.4). Slightly before the terminal end, there is a sharp decrease in diameter (Fig. 5.3, 5.4). The trunk end bears not only microannuli but also longitudinal striations (Figs. 5.5, 5.6, 6.4, 6.5). At the terminal end, there are only longitudinal striations, and the cuticle recurves first interiorly then slightly backwards (Figs. 5.6, 6.5). The anus is situated terminally, and the backwardly recurved cuticle is lined with the posterior part of the assumed gut (Fig. 7.1–7.3; Supplementary data sets 2 and 3). Materials.—Three fragmentary specimens are examined, UMCU
Fig. 4. Reconstruction of Dahescolex kuanchuanpuensis n. gen. n. sp. The posterior trunk part is artfully blurred. Scale bar represents 1 mm.
Figs. 5–7, Supplementary data sets 2 and 3
2014a 2016 2017 2018 2018
Eopriapulites sphinx Liu and Xiao in Liu et al., figs. 2, 3 Eopriapulites sphinx Liu and Xiao; Shao et al., figs. 2–6 Eopriapulites sphinx Liu and Xiao; Liu and Zhang, fig. 4.1, 4.2 unnamed form C; Zhang et al., fig. 6 Eopriapulites sphinx Liu and Xiao; Shao et al., fig. 7
Holotype.—A body fragment (UMCU No.CGM16) from the Fortunian Zhangjiagou section in southern Shaanxi, South China, now deposited at the University Museum of Chang'an University, Xi'an (Liu et al., 2014a, figs. 2, 3). Revised diagnosis.—Body bipartite, composed of an anterior part, the 5
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Fig. 6. Eopriapulites sphinx Liu and Xiao in Liu et al., 2014a from the Cambrian Fortunian Zhangjiagou Lagerstätte. (1) UMCU 14CHD0816-007, close-up of Fig. 5.1, arrows indicate pits; (2) UMCU 14CHD0816-007, close-up of Fig. 5.2, arrows indicate pits; (3) close-up of a pit; (4) UMCU 14CHD0816-008, close-up of Fig. 5.3, arrows indicate annuli with longitudinal striations; (5) UMCU 14CHD0816-008, close-up of Fig. 5.4, black arrow indicates the longitudinal striations, white arrow indicates the recurved cuticle. Scale bar under (3) represents 20 μm and is applied to (3) only. Scale bar between (1) and (2) represents 100 μm and applies to (1), (2), (4), and (5).
2012; Zhang et al., 2015), but they resulted in more conflicts, and this is largely because of the ambiguity of the ground pattern characters of the last common ancestors of the Cycloneuralia and its ingroups Scalidophora and Nematoida (Maas et al., 2007b). Here, a formal morphologybased phylogenetic analysis is not suggested, and instead we follow Maas et al. (2007b) and Maas (2013) that the Cambrian priapulid-like cycloneuralians represent stem-lineage derivatives of Cycloneuralia, or at most stem-lineage derivatives of Scalidophora. As to the current study, it is suggested that Dahescolex kuanchuanpuensis n. gen. n. sp. may represent a stem-lineage derivative of the Scalidophora, and we follow Shao et al. (2018) and regard Eopriapulites sphinx as a stemlineage derivative of the Cycloneuralia. Macrobenthic cycloneuralians in the Fortunian Stage.—The body length of the cycloneuralians in the Cambrian Stage 3 MaotianshanShale biota is generally in the centimeter range, with some smaller specimens of millimeter scale and some larger ones even of decimeter scale (Maas et al., 2007b). The current study demonstrates that some Fortunian cycloneuralians may have reached lengths of several millimeters or even centimeters, therefore being comparable in size with the cycloneuralians of the Maotianshan-Shale biota (Maas et al., 2007b). Here, we take the current material as an example. The not quite complete holotype of Dahescolex kuanchuanpuensis n. gen. n. sp. (Fig. 2.1) was apparently folded in the process of dying and subsequent fossilization. When unfolded and straightened during life time, as reconstructed in our Fig. 4, the holotype specimen would have reached a length of more than six mm and a trunk diameter of about one mm. If we suppose that the original animal had a body length-width ratio of 10–15, the original body length of this animal might have been between 9.5 mm and 1.4 cm. Specimen UMCU 14CHD0816-009 (Fig. 5.5) represents an animal with a trunk diameter of at least 1.84 mm. Based on the relatively long fragments at hand and the previously published material of this species (Liu et al., 2014a; Shao et al., 2016, 2018), the body length-width ratio of Eopriapulites sphinx is herein estimated to be 15–20, and the original animal may have had reached a body length between 2.8 and 3.7 cm. Therefore, it appears likely to us that these cycloneuralians were only temporary meiobenthic during their younger ontogenetic stages, but would have left the meiobenthos and joined the
14CHD0816-007 (Fig. 5.1, 5.2), UMCU 14CHD0816-008 (Fig. 5.3, 5.4), and UMCU 14CHD0816-009 (Fig. 5.5, 5.6). Comparisons.—Specimens UMCU 14CHD0816-007 (Fig. 5.1, 5.2) and UMCU 14CHD0816-008 (Fig. 5.3, 5.4) are assigned to Eopriapulites sphinx based on co-occurrence and identical trunk morphology with the holotype. Specimen UMCU 14CHD0816-009 (Fig. 5.5, 5.6) is interpreted as the terminal trunk end of the same species based on co-occurrence and identical morphology with the trunk end of specimen UMCU 14CHD0816-008 (Fig. 5.3, 5.4). Measurements.—The specimen UMCU 14CHD0816-007 (Fig. 5.1) is slightly distorted and flattened. If straightened, it would be about 2.57 mm long and 566 μm wide; there are about seven annuli every 100 μm. The pits (Fig. 6.3) on the cuticle are each about 15 μm in diameter. The specimen UMCU 14CHD0816-008 (Fig. 5.3) is curved but not compressed; thus its width is equal to its diameter. If it were straightened, it would be about 2 mm long. Its anterior part has a diameter of about 436 μm; its posterior trunk part has a diameter of about 333 μm; the trunk end with longitudinal striations has a diameter of 232 μm and a length of 214 μm. There are about eight annuli every 100 μm, and about 15 longitudinal striations every 100 μm. The specimen UMCU 14CHD0816-009 (Fig. 5.5) has a diameter of about 977 μm, with six longitudinal striations every 100 μm. Reconstruction.—A revised reconstruction of Eopriapulites sphinx is presented (Fig. 7.4), showing that the estimated body length–width ratio is about 15 (see discussion below). Remarks.—The current diagnosis is emended from Liu et al. (2014a) and Shao et al. (2016), with new information added, i.e., the pits on the trunk and the narrowed trunk end based on the current material. 4. Discussion Affinities.—The affinity of the Cambrian cycloneuralians is a longterm debated topic, and it is beyond the scope of this paper to review this lengthy debate. Many morphology-based phylogenetic analyses have previously been proposed to probe the phylogenetic positioning of the Cambrian cycloneuralians (Dong et al., 2010; Harvey et al., 2010; Liu et al., 2014a; Ma et al., 2014; Shao et al., 2016, 2018; Wills et al., 6
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(Liu et al., 2014a, 2019; Zhang et al., 2015; this study), ancestral cycloneuralians should have occurred in the lowermost Cambrian. Among the Fortunian cycloneuralians, Eopriapulites sphinx has previously been proposed to be an ancestral cycloneuralian, or more exactly be close to the ancestral cycloneuralian (Liu et al., 2018; Shao et al., 2018), because it has priapulid-like trunk morphology and matches the reconstruction of an ancestral cycloneuralian (Budd, 2001, 2003; Webster et al., 2006). Here, we follow this suggestion that E. sphinx may represent an ancestral cycloneuralian, or more precise, close to the last common ancestor of modern cycloneuralians. In previous studies, mainly meiobenthos-sized specimens of E. sphinx were studied, thus it was proposed that ancestral cycloneuralians might have been microscopic, and that the taxon Cycloneuralia might have originated in the Fortunian meiobenthic community (Liu et al., 2018; Shao et al., 2018). The current study demonstrates that E. sphinx could reach a macrobenthic body size during later ontogenetic stages, therefore we propose herein that the last common ancestor of the Cycloneuralia may have been macroscopic, introvert-bearing, microannulated, and lacking trunk armatures such as cuticular sclerites and spines, that the Cycloneuralia may have originated in the Fortunian as part of the macrobenthos community, and that E. sphinx may be an ancestral representative of the Cycloneuralia. Acknowledgements This work was supported by the National Natural Science Foundation of China (grant numbers 41872014, 41572007 and 41572009), the Strategic Priority Research Program of Chinese Academy of Sciences (grant number XDB26000000), the State Key Laboratory of Paleobiology and Stratigraphy, Nanjing Institute of Geology and Paleontology, Chinese Academy of Sciences (grant number 193123), the Youth Innovation Promotion Association, Chinese Academy of Sciences (2016283), the Basic Research Plan of Natural Science of Shaanxi Province (grant number 2018JM4002), the Graduate Student Scientific Research Innovation Projects of Chang’an University (grant numbers 2019383 and 2019368). We thank two anonymous reviewers for their comments and suggestions, and we thank Dinghua Yang and Suping Wu for technical help during artistic reconstruction and Micro-CT scanning. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.precamres.2019.105413. References Ahlrichs, W.H., 1995. Ultrastruktur und Phylogenie von Seison nebaliae (Gruber 1859) und Seison annulatus (Claus 1876). Hypothesen zu phylogenetischen Verwandtschaftsverhältnissen innerhalb der Bilateria. Georg-August-University of Göttingen, Göttingen, pp. 1–310. Ax, P., 2003. In: Multicellular Animals: Order in Nature-System Made by Man. SpringerVerlag, Berlin Heidelberg, New York, pp. 317. Bengtson, S., Yue, Z., 1997. Fossilized metazoan embryos from the earliest Cambrian. Science 277 (5332), 1645–1648. Briggs, D.E.G., Erwin, D.H., Collier, F.J., 1994. The Fossils of the Burgess Shale. Smithsonian Institution Press, Washington, D.C., pp. 238. Budd, G.E., 1999. The morphology and phylogenetic significance of Kerygmachela kierkegaardi Budd (Buen Formation, Lower Cambrian N Greenland). Trans. R. Soc. Edinb.-Earth Sci. 89 (04), 249–290. Budd, G.E., 2001. Tardigrades as “stem-group arthropods”: the evidence from the Cambrian fauna. Zool. Anz. 240 (3–4), 265–279. Budd, G.E., 2003. Arthropods as ecdysozoans: the fossil evidence. In: Legakis, A., Sfenthourakis, S., Polmeni, R., Thessalou-Leggaki, M. (Eds.), The New Panorama of Animal Evolution. Proceedings of the XVIII International Congress of Zoology, Sofia, Pensoft, pp. 479–487 September 2000, Athens, Greece. Chen, Z., Chen, X., Zhou, C.M., Yuan, X.L., Xiao, S., 2018. Late Ediacaran trackways produced by bilaterian animals with paried appendages. Sci. Adv. 4 (6), 6691. Conway Morris, S., 1977. Fossil priapulid worms. Spec. Pap. Palaeontol. 20, 1–95. Dong, X.P., Bengtson, S., Gostling, N.J., Cunningham, J.A., Harvey, T.H.P., Kouchinsky, A., Val'kov, A.K., Repetski, J.E., Stampanoni, M., Marone, E., Donoghue, P.C.J., 2010.
Fig. 7. Eopriapulites sphinx Liu and Xiao in Liu et al., 2014a from the Cambrian Fortunian Zhangjiagou Lagerstätte. (1–3) Micro-CT images of UMCU 14CHD0816-008 (Fig. 5.3); (1, 2) longitudinal sections through the posterior trunk part, arrows denote the gut; (3) transverse section through the posterior trunk part, arrow denotes the gut; (4) reconstruction, with body length/width ratio of about 15. Scale bar below (1) applies to (1–3), and scale bar right to (4) applies to (4) only. Scale bar represents 1 mm.
macrobenthos subsequently when reaching larger body sizes. The last common ancestor of the Cycloneuralia.—It has previously been proposed that the last common ancestor of the Cycloneuralia may have been a macroscopic, microannulated, and introvert-bearing worm, and that the Cambrian palaeoscolecids may represent such ancestral cycloneuralians (Budd, 1999, 2001, 2003; Eriksson and Budd, 2000). This rather priapulid-like last common ancestor of the Cycloneuralia is also supported by mitogenomics and phylogenomics, which suggest extant priapulids as a model of the last common ancestors of the Cycloneuralia (Webster et al., 2006). Because the cycloneuralians have emerged in the Fortunian Stage 7
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The anatomy, taphonomy, taxonomy and systematic affinity of Markuelia: early Cambrian to Early Ordovician scalidophorans. Palaeontology 53 (6), 1291–1314. Duan, B.C., Dong, X.P., Donoghue, P.C.J., 2012. New palaeoscolecid worms from the Furongian (upper Cambrian) of Hunan, South China: is Markuelia an embryonic palaeoscolecid? Palaeontology 55 (3), 613–622. Eriksson, B.J., Budd, G.E., 2000. Onychophoran cephalic nerves and their bearing on our understanding of head segmentation and stem-group evolution of Arthropoda. Arthropod. Struct. Dev. 29 (3), 197–209. Giribet, G., Edgecombe, G.D., 2017. Current understanding of Ecdysozoa and its internal phylogenetic relationships. Integr. Comp. Biol. 57 (3), 455–466. Harvey, T.H.P., Butterfield, N.J., 2017. Exceptionally preserved Cambrian loriciferans and the early animal invasion of the meiobenthos. Nat. Ecol. Evol. 1 (3), 0022. Harvey, T.H.P., Dong, X.P., Donoghue, P.C.J., 2010. Are palaeoscolecids ancestral ecdysozoans? Evol. Dev. 12 (7), 177–200. Haug, J.T., Maas, A., Waloszek, D., Donoghue, P.C.J., Bengtson, S., 2009. A new species of Markuelia from the Middle Cambrian of Australia. In: Memoirs of the Association of Australasian Palaeontologists, pp. 303–313. Hou, X.G., Siveter, Da.J., Siveter, De.J., Aldridge, R.J., Cong, P.Y., Gabbott, S.E., Ma, X.Y., Purnel, M.A., Williams, M., 2017. In: The Cambrian Fossils of Chengjiang, China, The Flowering of Early Animal Life Second Edition. Wiley-Blackwell, Oxford, pp. 328. Li, Z.P., 1984. The discovery and its significance of small shelly fossils in Hexi area, Xixiang, Shaanxi. Geol. Shaanxi 2 (1), 73–77 (in Chinese with English abstract). Liu, Y.H., Wang, Q., Shao, T.Q., Zhang, H.Q., Qin, J.C., Li, C., Liang, Y., Chen, C., Xue, J.Q., Liu, X., 2018. New material of three-dimensionally phosphatized and microscopic cycloneuralians from the Cambrian Paibian Stage of South China. J. Paleontol. 92 (1), 87–98. Liu, Y.H., Li, Y., Shao, T.Q., Zhang, H.Q., Wang, Q., Qiao, J.P., 2014b. Quadrapyrgites from the lower Cambrian of South China: growth pattern, post-embryonic development, and affinity. Chin. Sci. Bull. 59 (31), 4086–4095. Liu, Y.H., Qin, J.C., Wang, Q., Maas, A., Duan, B.C., Zhang, Y.N., Zhang, H., Shao, T.Q., Zhang, H.Q., 2019. New armoured scalidophorans (Ecdysozoa, Cycloneuralia) from the Cambrian Fortunian Zhangjiagou Lagerstätte, South China. Pap. Palaeontol. 5, 241–260. Liu, Y.H., Xiao, S.H., Shao, T.Q., Broce, J., Zhang, H.Q., 2014a. The oldest known priapulid-like scalidophoran animal and its implications for the early evolution of cycloneuralians and ecdysozoans. Evol. Dev. 16 (3), 155–165. Liu, Z., Zhang, H.Q., 2017. A review of progress on Cambrian Orsten-type fossils in South China. Acta Micropalaeont. Sin. 34 (1), 1–15 (in Chinese with English abstract). Ma, X.Y., Aldridge, R.J., Siveter, Da.J., Siveter, De.J., Hou, X.G., Edgecombe, G.D., 2014. A new exceptionally preserved Cambrian priapulid from the Chengjiang Lagerstätte. J. Paleontol. 88 (2), 371–384. Maas, A., 2013. Gastrotricha, Cycloneuralia and Gnathifera: the fossil record. In: SchmidtRhaesa, A. (Ed.), Handbook of Zoology 2: Nematomorpha, Priapulida, Kinorhyncha, Loricifera. De Gruyter, Berlin, pp. 11–28. Maas, A., Braun, A., Dong, X.P., Donoghue, P.C.J., Müller, K.J., Olempska, E., Repetski, J.E., Siveter, D.J., Stein, M., Waloszek, D., 2006. The ‘Orsten’: more than a Cambrian Konservat-Lagerstätte yielding exceptional preservation. Palaeoworld 15 (3), 266–282. Maas, A., Waloszek, D., Haug, J.T., Müller, K.J., 2007a. A possible larval roundworm from the Cambrian ‘Orsten’ and its bearing on the phylogeny of Cycloneuralia. In: Memoirs
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New macrobenthic cycloneuralians from the Fortunian (lowermost Cambrian) of South China ⁎
T.Q. Shaoa, J.C. Qina, Y. Shaoa, Y.H. Liua, , D. Waloszekb, A. Maasc, B.C. Duand, Q. Wanga, Y. Xua, ⁎ H.Q. Zhange, a
School of Earth Science and Resources, Chang’an University, Xi’an 710054, China University of Lund, Sölvegatan 12, SE-22362 Lund, Sweden c Galgenackerweg 25, 89134 Blaustein, Germany d Research Center for Islands and Coastal Zone, First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China e State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Nanjing 210008, China b
A R T I C LE I N FO
A B S T R A C T
Keywords: Scalidophora Cycloneuralia Ecdysozoa Cambrian Fortunian stage South China
Although morphology-based phylogenetic analyses and molecular data suggested that the cycloneuralians might have emerged in the Ediacaran Period, the oldest known fossil remains of cycloneuralians were first reported from the Cambrian Fortunian Stage of South China, and to date four genera and species as well as nine indeterminate forms have been described. Here, we report the latest discoveries of cycloneuralians from the Fortunian Kuanchuanpu Formation at Zhangjiagou Lagerstätte, Dahe Village, Xixiang County, southern Shaanxi Province, South China. A new genus and species Dahescolex kuanchuanpuensis n. gen. n. sp. is described, and a previously reported genus and species Eopriapulites sphinx is re-described. Dahescolex kuanchuanpuensis n. gen. n. sp. is suggested to be a stem-lineage derivative of Scalidophora, whereas E. sphinx may represent a stem-lineage derivative of Cycloneuralia. From the fragments discovered, the new specimens are suggested to have reached millimeters in dimension, and the original individuals are estimated to have dimensions in centimeter, hence falls within the size range of macrobenthos. Therefore, at least some of the Fortunian cycloneuralians can be considered macrobenthic, and it is suggested here that the Cycloneuralia may have originated in the Fortunian macrobenthos.
1. Introduction Morphology-based phylogenetic analyses propose that the Scalidophora (Priapulida, Loricifera and Kinorhyncha) and Nematoida (Nematoda and Nematomorpha) are sister taxon to each other, and they constitute the monophyletic Cycloneuralia (Ax, 2003; Nielsen, 2012; Giribet and Edgecombe, 2017). Cycloneuralians might have emerged in the Ediacaran Period and diversified in the early Cambrian (RotaStabelli et al., 2013). Although some trackways from the Ediacaran Period may have possibly been produced by some cycloneuralians or appendage-bearing bilaterians (Chen et al., 2018), the oldest known unambiguous fossils of cycloneuralians occurred in the Cambrian Fortunian Stage (Liu et al., 2014a; Zhang et al., 2015). As cuticle-bearing animals, cycloneuralians have relatively strong fossilisation potential relative to other taxa with simple epidermis, and thus not surprisingly left abundant fossils in the Cambrian Konservat-Lagerstätten (Maas,
⁎
2013). Previously reported Cambrian cycloneuralians occur mainly in Stage 3 and younger strata (Maas, 2013), such as the typical Burgess Shale-type Lagerstätten (Conway Morris, 1977; Briggs et al., 1994; Hou et al., 2017) and the Orsten-type Lagerstätten (Liu et al., 2014a, 2019; Maas et al., 2007a; 2009; Shao et al., 2018; Zhang et al., 2015, 2018), with minor occurrences as Small Carbonaceous Fossils (Harvey and Butterfield, 2017; Slater et al., 2018). In Stage 2, only a single species, known exclusively from embryos, was reported (Bengtson and Yue, 1997). In the Fortunian Stage, the cycloneuralians were not reported until 2014, and to date four genera and species as well as nine indeterminate forms have been described (Liu et al., 2014a, 2019; Shao et al., 2016, 2018; Zhang et al., 2015, 2018). Because of their occurrence close to the origin and early diversification of the cycloneuralians, the Fortunian cycloneuralians provide the possibility of helping to reconstruct the last common ancestors of Cycloneuralia and its ingroups Nematoida and Scalidophora.
Corresponding authors. E-mail addresses: [email protected] (Y.H. Liu), [email protected] (H.Q. Zhang).
https://doi.org/10.1016/j.precamres.2019.105413 Received 5 March 2019; Received in revised form 18 June 2019; Accepted 8 August 2019 0301-9268/ © 2019 Elsevier B.V. All rights reserved.
Please cite this article as: T.Q. Shao, et al., Precambrian Research, https://doi.org/10.1016/j.precamres.2019.105413
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Fig. 1. Location map and stratigraphic column of the Zhangjiagou section in southern Shaanxi Province, South China. The key horizon yielding the current specimens is denoted by an arrow.
Geology and Palaeontology. In order to detect possible internal biologic structures, selected specimens were scanned using Micro-CT at Nanjing Institute of Geology and Palaeontology, and the Micro-CT data were analyzed using Amira 5.3. The current specimens are deposited at the University Museum of Chang’an University (UMCU), Xi'an.
Here, we describe new material of cycloneuralians from the Fortunian Zhangjiagou Lagerstätte in southern Shaanxi Province, South China. Although fragmentarily preserved, the new material suggests that these specimens have reached several millimeters in dimensions, and the original individuals may be at a centimeter scale, thus falling within the size range of the macrobenthos.
3. Systematic palaeontology 2. Materials and methods
Cycloneuralia Ahlrichs, 1995
The current specimens were extracted from the lower part of the second member of the Kuanchuanpu Formation at the Zhangjiagou Lagerstätte (Shao et al., 2018), Dahe Village, Xixiang County, southern Shaanxi Province, South China (Fig. 1). They are three-dimensionally phosphatized and soft-bodied, i.e., with Orsten-type preservation (Müller and Walossek, 1991; Waloszek, 2003; Maas et al., 2006). The key horizon that yielded the present material has previously been constrained to be part of the small shelly fossils Anabarites trisulcatus–Protohertzina anabarica Assemblage Zone (Li, 1984; Liu et al., 2014b, 2014a; Shao et al., 2018; Steiner et al., 2014; Zhang et al., 2015), and has an estimated age of about 535 Ma (Steiner et al., 2007, 2014), within the Fortunian Stage of the Cambrian Period (Peng et al., 2012). As in the previous studies (Liu et al., 2014b, 2014a, 2019; Shao et al., 2018; Zhang et al., 2015), rock samples from the key horizon at the Zhangjiagou section were processed through a routine etching method with diluted acetic acid (10%) at the Chang’an University. Undissolvable residues were dried naturally and then handpicked under a binocular microscope. Microfossils were picked out and mounted on aluminum stubs for observation under an LEO 1530VP field-emission environmental scanning electron microscope at the Nanjing Institute of
Genus Dahescolex Zhang HQ, Shao TQ, and Liu YH new genus
Type and single species.—Dahescolex kuanchuanpuensis Zhang HQ, Shao TQ, and Liu YH new genus and new species, by monotypy. Diagnosis.—As for the type species. Occurrence.—Kuanchuanpu Formation, Zhangjiagou section, southern Shaanxi Province, South China; Anabarites trisulcatus–Protohertzina anabarica Assemblage Zone, Fortunian Stage, Cambrian. Etymology.—From Dahe, with reference to its occurrence in Dahe Village, and scolex, Greek, worm. Dahescolex kuanchuanpuensis Zhang HQ, Shao TQ, and Liu YH new genus and new species Figs. 2–4, Supplementary data set 1. Holotype and single specimen.—UMCU 13CHD0718-006, a possible juvenile or young adult, from the Fortunian Kuanchuanpu Formation at Zhangjiagou section, southern Shaanxi Province, South China. Diagnosis.—Body bi-partite, composed of an anterior part, the 2
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Fig. 2. Dahescolex kuanchuanpuensis n. gen. n. sp. from the Cambrian Fortunian Zhangjiagou Lagerstätte. (1) holotype, UMCU 13CHD0718-006; (2) left lateral view of (1); (3) opposite side of (1), showing the preserved trunk part, A1–A6 refer to the first to the sixth annuli; (4) right lateral view of (1). Scale bar represents 1 mm.
arranged in longitudinal rows (Fig. 3.1). Between every two longitudinal rows of scalids, there are additional two longitudinal rows of relatively small scalids, extending only from the second to the fifth circlets (Fig. 3.1). The trunk is demarcated off from the proboscis by the beginning of the first trunk annulus (Fig. 2). The trunk portion of the specimen at hand indicates that the species had at least six annuli, each with an annular ring of five to seven spinose sclerites (Fig. 2.3). The lengths of the annuli are more or less the same. Spinose sclerites are positioned at the anterior part of each annulus, and take up two-thirds or three-quarters of the annular length. The anterior margin of the spinose sclerites is aligned with the anterior margin of the annulus. The spinose sclerites have an expanded and long elliptic base and a spine antero-centrally. The bases of the sclerites do not contact with those of the adjacent ones, with membranous cuticle in between. There is a large spinose sclerite straddling on the fifth and sixth annuli. The large spinose sclerite has an expanded, round base and a central spine. The posterior part of the trunk is unknown in the specimen at hand. Etymology.—From kuanchuanpu, with reference to its occurrence in the Kuanchuanpu Formation. Comparisons.—Dahescolex kuanchuanpuensis n. gen. n. sp. differs
proboscis and a posterior part, the trunk; proboscis composed of an anterior region, the teeth-bearing pharynx, and a tubular posterior region, the introvert, with at least eight circlets of spine-shaped, internally hollow scalids; scalids arranged in longitudinal rows; between every two rows of scalids there are additional two longitudinal rows of relatively small scalids, extending only from the second to the fifth circlets; trunk with at least six annuli, each with an annular ring of spinose sclerites. Occurrence.—Kuanchuanpu Formation, Zhangjiagou section, southern Shaanxi Province, South China; Anabarites trisulcatus–Protohertzina anabarica Assemblage Zone, Fortunian Stage, Cambrian. Description.—The body of Dahescolex kuanchuanpuensis n. gen. n. sp. is composed of two major body regions (Fig. 2). The anterior part is the proboscis, and it is subdivided into the pharynx, as the expandable and intrudible anterior end of the esophagal part of the gut, and a posterior more or less tubular region, called introvert. The pharynx and its teeth are unknown in the specimen at hand. The introvert bears at least eight circlets of cuticular scalids (Fig. 3.1). The scalids are long, spine-shaped (Figs. 2.1, 3.1, 3.3) and internally hollow (Figs. 2.2, 3.2), and are
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Fig. 3. Dahescolex kuanchuanpuensis n. gen. n. sp. from the Cambrian Fortunian Zhangjiagou Lagerstätte. (1) close-up of the introvert of the holotype UMCU 13CHD0718-006 (Fig. 2.1), sc1–sc8 refer to the first to the eighth circlets of scalids, numbers and white arrows denote the scalids in each circlet, and black arrows denote the relatively small scalids; (2) right lateral view of (1), arrows indicate the internally hollow scalids; (3) left lateral view of (1), arrow indicates a spine-shaped scalid. Scale bar represents 500 μm.
considered embryonic, because the worm-like forms were found embedded in an egg case, though completely annulated and with anterior and posterior spine structures preserved, is Markuelia, found in the middle Cambrian rocks in Australia and middle and upper Cambrian rocks of South China (Haug et al., 2009; Dong et al., 2010). Also here, there are clear differences to D. kuanchuanpuensis gen. et sp. nov., e.g. in the arrangement pattern of the introvert scalids, or the presence/absence of sclerites on the trunk. Measurements.—The holotype UMCU 13CHD0718-006 (Fig. 2.1) is about 3.73 mm long and 1.58 mm wide. The proboscis is about 2.99 mm long, and 1.01 mm wide at its basal part, whereas the trunk part is about 3.40 mm long and 1.49 mm wide. Because the specimen is flattened, the original diameter of the proboscis and the trunk part is about 643 μm and 949 μm, respectively. The scalid in the second circlet (Fig. 3.1) is about 555 μm long and 160 μm wide at the base, and a relatively small scalid beside it is about 262 μm long, and 52 μm wide at its base. The base of the large spinose sclerite is about 500 μm in diameter, and the base of each spinose sclerite is about 430 μm long and 170 μm wide. Each annulus is about 650 μm long. Reconstruction.—An artistic reconstruction of Dahescolex kuanchuanpuensis n. gen. n. sp. is presented in Fig. 4. Remarks.—Micro-CT analysis suggests that the holotype of Dahescolex kuanchuanpuensis n. gen. n. sp. is internally solid (Supplementary data set 1).
from the co-occurring Eopriapulites sphinx Liu and Xiao in Liu et al., 2014a (Liu et al., 2014a; Shao et al., 2016, 2018) in the arrangement pattern of the introvert scalids and also in the presence/absence of sclerites on the trunk. Dahescolex kuanchuanpuensis n. gen. n. sp. differs from the coeval Eokinorhynchus rarus Zhang et al., 2015 in that E. rarus has annular rings of closely-spaced rectangular plates without spines, randomly distributed spines, and bilaterally positioned large spinose sclerites, and also in that E. rarus has pentaradially arranged introvert scalids. Dahescolex kuanchuanpuensis n. gen. n. sp. differs from the Qinscolex and Shanscolex (Liu et al., 2019) in the arrangement pattern of the introvert scalids and also in the shape and arrangement of the spinose sclerites on the trunk. Dahescolex kuanchuanpuensis n. gen. n. sp. differs from the palaeoscolecids in that the latter forms have long and slender trunks with annular ring(s) of plates with nodes, platelets, or microplates (Müller and Hinz-Schallreuter, 1993; Zhang and Pratt, 1996; Duan et al., 2012; Liu et al., 2018). Assuming that D. kuanchuanpuensis n. gen. n. sp. lacks loricae at this ontogenetic stage, it is different from the loricate Eolorica deadwoodensis Harvey and Butterfield, 2017. Shergoldana australiensis Maas et al., 2007a from the middle Cambrian of Australia is known only from its small, possibly earliest larval semaphoront/larval stage, measuring no more than 120 µm in length. Its subdivision into (intruded) pharynx and four more body regions sets it off until now from the new species and all other described Cambrian fossils assigned to Cycloneuralia, but its shared features like the sclerites with spines and bifid trunk end make it clearly an interesting form for future discussions of the basic set of features of this group and further evolutionary developments of its ingroup taxa. Orstenoloricus shergoldii Maas et al., 2009 from the middle Cambrian of Australia was also established on larval forms. They possess a trunk region made of 20 plates, thus representing a lorica, and, accordingly, were clearly assignable to the taxon Vinctiplicata (sister taxon to Kinorhyncha; Ax, 2003) within Scalidophora. Therefore, closer systematic relationships of the two Australia species with D. kuanchuanpuensis gen. et sp. nov. are currently ruled out. Another taxon, based on larval stages, often
Genus Eopriapulites Liu and Xiao in Liu et al., 2014a
Type and single species.—Eopriapulites sphinx Liu and Xiao in Liu et al., 2014a from the Fortunian Zhangjiagou section, southern Shaanxi Province, by original designation. Diagnosis.—As for the type species. Occurrence.—Kuanchuanpu Formation, Zhangjiagou section, southern Shaanxi Province, South China; Xinli Member, Dengying Formation, Xinli section, northern Sichuan Province, South China; Anabarites trisulcatus–Protohertzina anabarica Assemblage Zone, Fortunian Stage, Cambrian. Eopriapulites sphinx Liu and Xiao in Liu et al., 2014a
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Fig. 5. Eopriapulites sphinx Liu and Xiao in Liu et al., 2014a from the Cambrian Fortunian Zhangjiagou Lagerstätte. (1) UMCU 14CHD0816-007; (2) opposite side of (1); (3) UMCU 14CHD0816-008; (4) opposite side of (3); (5) UMCU 14CHD0816-009, lateral view; (6) posterior view of (5). Scale bar represents 1 mm.
proboscis, and a posterior part, the trunk; proboscis consisting of a pharynx with multiple circlets of pharyngeal teeth, 18 of which are present in the basal circlet, and each has a base and an apical cusp, an eversible collar with possibly 12 anteriorly directed coronal scalids, an eversible introvert with 12 circlets of nine scalids, each circlet alternates with the adjacent one(s), forming 18 longitudinal rows; coronal and introvert scalids spine-shaped and internally hollow; trunk densely annulated, with estimated several hundreds or even thousands of microannuli; pits distributed at random at the middle trunk part; posterior trunk part decreasing in diameter gradually toward the end; a sharp decrease of diameter before the terminal end; terminal end with longitudinal striations. Description.—The general morphology of Eopriapulites sphinx follows Liu et al. (2014a) and Shao et al. (2016), with only minor revisions to the trunk. The trunk is tube-shaped, with densely-spaced microannuli (Figs. 5.1–5.4, 6.1, 6.2). On the middle part of the trunk, there are some pits (Fig. 6.1, 6.2). The pits are situated on the microannuli or inserted in between two adjacent microannuli; they appear to be distributed at random. Each pit (Fig. 6.3) has a central hole housing a ball-shaped structure. The major part of the trunk has uniform diameter (Fig. 5.1, 5.2), but it decreases slightly and gradually toward the posterior end (Fig. 5.3, 5.4). Slightly before the terminal end, there is a sharp decrease in diameter (Fig. 5.3, 5.4). The trunk end bears not only microannuli but also longitudinal striations (Figs. 5.5, 5.6, 6.4, 6.5). At the terminal end, there are only longitudinal striations, and the cuticle recurves first interiorly then slightly backwards (Figs. 5.6, 6.5). The anus is situated terminally, and the backwardly recurved cuticle is lined with the posterior part of the assumed gut (Fig. 7.1–7.3; Supplementary data sets 2 and 3). Materials.—Three fragmentary specimens are examined, UMCU
Fig. 4. Reconstruction of Dahescolex kuanchuanpuensis n. gen. n. sp. The posterior trunk part is artfully blurred. Scale bar represents 1 mm.
Figs. 5–7, Supplementary data sets 2 and 3
2014a 2016 2017 2018 2018
Eopriapulites sphinx Liu and Xiao in Liu et al., figs. 2, 3 Eopriapulites sphinx Liu and Xiao; Shao et al., figs. 2–6 Eopriapulites sphinx Liu and Xiao; Liu and Zhang, fig. 4.1, 4.2 unnamed form C; Zhang et al., fig. 6 Eopriapulites sphinx Liu and Xiao; Shao et al., fig. 7
Holotype.—A body fragment (UMCU No.CGM16) from the Fortunian Zhangjiagou section in southern Shaanxi, South China, now deposited at the University Museum of Chang'an University, Xi'an (Liu et al., 2014a, figs. 2, 3). Revised diagnosis.—Body bipartite, composed of an anterior part, the 5
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Fig. 6. Eopriapulites sphinx Liu and Xiao in Liu et al., 2014a from the Cambrian Fortunian Zhangjiagou Lagerstätte. (1) UMCU 14CHD0816-007, close-up of Fig. 5.1, arrows indicate pits; (2) UMCU 14CHD0816-007, close-up of Fig. 5.2, arrows indicate pits; (3) close-up of a pit; (4) UMCU 14CHD0816-008, close-up of Fig. 5.3, arrows indicate annuli with longitudinal striations; (5) UMCU 14CHD0816-008, close-up of Fig. 5.4, black arrow indicates the longitudinal striations, white arrow indicates the recurved cuticle. Scale bar under (3) represents 20 μm and is applied to (3) only. Scale bar between (1) and (2) represents 100 μm and applies to (1), (2), (4), and (5).
2012; Zhang et al., 2015), but they resulted in more conflicts, and this is largely because of the ambiguity of the ground pattern characters of the last common ancestors of the Cycloneuralia and its ingroups Scalidophora and Nematoida (Maas et al., 2007b). Here, a formal morphologybased phylogenetic analysis is not suggested, and instead we follow Maas et al. (2007b) and Maas (2013) that the Cambrian priapulid-like cycloneuralians represent stem-lineage derivatives of Cycloneuralia, or at most stem-lineage derivatives of Scalidophora. As to the current study, it is suggested that Dahescolex kuanchuanpuensis n. gen. n. sp. may represent a stem-lineage derivative of the Scalidophora, and we follow Shao et al. (2018) and regard Eopriapulites sphinx as a stemlineage derivative of the Cycloneuralia. Macrobenthic cycloneuralians in the Fortunian Stage.—The body length of the cycloneuralians in the Cambrian Stage 3 MaotianshanShale biota is generally in the centimeter range, with some smaller specimens of millimeter scale and some larger ones even of decimeter scale (Maas et al., 2007b). The current study demonstrates that some Fortunian cycloneuralians may have reached lengths of several millimeters or even centimeters, therefore being comparable in size with the cycloneuralians of the Maotianshan-Shale biota (Maas et al., 2007b). Here, we take the current material as an example. The not quite complete holotype of Dahescolex kuanchuanpuensis n. gen. n. sp. (Fig. 2.1) was apparently folded in the process of dying and subsequent fossilization. When unfolded and straightened during life time, as reconstructed in our Fig. 4, the holotype specimen would have reached a length of more than six mm and a trunk diameter of about one mm. If we suppose that the original animal had a body length-width ratio of 10–15, the original body length of this animal might have been between 9.5 mm and 1.4 cm. Specimen UMCU 14CHD0816-009 (Fig. 5.5) represents an animal with a trunk diameter of at least 1.84 mm. Based on the relatively long fragments at hand and the previously published material of this species (Liu et al., 2014a; Shao et al., 2016, 2018), the body length-width ratio of Eopriapulites sphinx is herein estimated to be 15–20, and the original animal may have had reached a body length between 2.8 and 3.7 cm. Therefore, it appears likely to us that these cycloneuralians were only temporary meiobenthic during their younger ontogenetic stages, but would have left the meiobenthos and joined the
14CHD0816-007 (Fig. 5.1, 5.2), UMCU 14CHD0816-008 (Fig. 5.3, 5.4), and UMCU 14CHD0816-009 (Fig. 5.5, 5.6). Comparisons.—Specimens UMCU 14CHD0816-007 (Fig. 5.1, 5.2) and UMCU 14CHD0816-008 (Fig. 5.3, 5.4) are assigned to Eopriapulites sphinx based on co-occurrence and identical trunk morphology with the holotype. Specimen UMCU 14CHD0816-009 (Fig. 5.5, 5.6) is interpreted as the terminal trunk end of the same species based on co-occurrence and identical morphology with the trunk end of specimen UMCU 14CHD0816-008 (Fig. 5.3, 5.4). Measurements.—The specimen UMCU 14CHD0816-007 (Fig. 5.1) is slightly distorted and flattened. If straightened, it would be about 2.57 mm long and 566 μm wide; there are about seven annuli every 100 μm. The pits (Fig. 6.3) on the cuticle are each about 15 μm in diameter. The specimen UMCU 14CHD0816-008 (Fig. 5.3) is curved but not compressed; thus its width is equal to its diameter. If it were straightened, it would be about 2 mm long. Its anterior part has a diameter of about 436 μm; its posterior trunk part has a diameter of about 333 μm; the trunk end with longitudinal striations has a diameter of 232 μm and a length of 214 μm. There are about eight annuli every 100 μm, and about 15 longitudinal striations every 100 μm. The specimen UMCU 14CHD0816-009 (Fig. 5.5) has a diameter of about 977 μm, with six longitudinal striations every 100 μm. Reconstruction.—A revised reconstruction of Eopriapulites sphinx is presented (Fig. 7.4), showing that the estimated body length–width ratio is about 15 (see discussion below). Remarks.—The current diagnosis is emended from Liu et al. (2014a) and Shao et al. (2016), with new information added, i.e., the pits on the trunk and the narrowed trunk end based on the current material. 4. Discussion Affinities.—The affinity of the Cambrian cycloneuralians is a longterm debated topic, and it is beyond the scope of this paper to review this lengthy debate. Many morphology-based phylogenetic analyses have previously been proposed to probe the phylogenetic positioning of the Cambrian cycloneuralians (Dong et al., 2010; Harvey et al., 2010; Liu et al., 2014a; Ma et al., 2014; Shao et al., 2016, 2018; Wills et al., 6
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(Liu et al., 2014a, 2019; Zhang et al., 2015; this study), ancestral cycloneuralians should have occurred in the lowermost Cambrian. Among the Fortunian cycloneuralians, Eopriapulites sphinx has previously been proposed to be an ancestral cycloneuralian, or more exactly be close to the ancestral cycloneuralian (Liu et al., 2018; Shao et al., 2018), because it has priapulid-like trunk morphology and matches the reconstruction of an ancestral cycloneuralian (Budd, 2001, 2003; Webster et al., 2006). Here, we follow this suggestion that E. sphinx may represent an ancestral cycloneuralian, or more precise, close to the last common ancestor of modern cycloneuralians. In previous studies, mainly meiobenthos-sized specimens of E. sphinx were studied, thus it was proposed that ancestral cycloneuralians might have been microscopic, and that the taxon Cycloneuralia might have originated in the Fortunian meiobenthic community (Liu et al., 2018; Shao et al., 2018). The current study demonstrates that E. sphinx could reach a macrobenthic body size during later ontogenetic stages, therefore we propose herein that the last common ancestor of the Cycloneuralia may have been macroscopic, introvert-bearing, microannulated, and lacking trunk armatures such as cuticular sclerites and spines, that the Cycloneuralia may have originated in the Fortunian as part of the macrobenthos community, and that E. sphinx may be an ancestral representative of the Cycloneuralia. Acknowledgements This work was supported by the National Natural Science Foundation of China (grant numbers 41872014, 41572007 and 41572009), the Strategic Priority Research Program of Chinese Academy of Sciences (grant number XDB26000000), the State Key Laboratory of Paleobiology and Stratigraphy, Nanjing Institute of Geology and Paleontology, Chinese Academy of Sciences (grant number 193123), the Youth Innovation Promotion Association, Chinese Academy of Sciences (2016283), the Basic Research Plan of Natural Science of Shaanxi Province (grant number 2018JM4002), the Graduate Student Scientific Research Innovation Projects of Chang’an University (grant numbers 2019383 and 2019368). We thank two anonymous reviewers for their comments and suggestions, and we thank Dinghua Yang and Suping Wu for technical help during artistic reconstruction and Micro-CT scanning. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.precamres.2019.105413. References Ahlrichs, W.H., 1995. Ultrastruktur und Phylogenie von Seison nebaliae (Gruber 1859) und Seison annulatus (Claus 1876). Hypothesen zu phylogenetischen Verwandtschaftsverhältnissen innerhalb der Bilateria. Georg-August-University of Göttingen, Göttingen, pp. 1–310. Ax, P., 2003. In: Multicellular Animals: Order in Nature-System Made by Man. SpringerVerlag, Berlin Heidelberg, New York, pp. 317. Bengtson, S., Yue, Z., 1997. Fossilized metazoan embryos from the earliest Cambrian. Science 277 (5332), 1645–1648. Briggs, D.E.G., Erwin, D.H., Collier, F.J., 1994. The Fossils of the Burgess Shale. Smithsonian Institution Press, Washington, D.C., pp. 238. Budd, G.E., 1999. The morphology and phylogenetic significance of Kerygmachela kierkegaardi Budd (Buen Formation, Lower Cambrian N Greenland). Trans. R. Soc. Edinb.-Earth Sci. 89 (04), 249–290. Budd, G.E., 2001. Tardigrades as “stem-group arthropods”: the evidence from the Cambrian fauna. Zool. Anz. 240 (3–4), 265–279. Budd, G.E., 2003. Arthropods as ecdysozoans: the fossil evidence. In: Legakis, A., Sfenthourakis, S., Polmeni, R., Thessalou-Leggaki, M. (Eds.), The New Panorama of Animal Evolution. Proceedings of the XVIII International Congress of Zoology, Sofia, Pensoft, pp. 479–487 September 2000, Athens, Greece. Chen, Z., Chen, X., Zhou, C.M., Yuan, X.L., Xiao, S., 2018. Late Ediacaran trackways produced by bilaterian animals with paried appendages. Sci. Adv. 4 (6), 6691. Conway Morris, S., 1977. Fossil priapulid worms. Spec. Pap. Palaeontol. 20, 1–95. Dong, X.P., Bengtson, S., Gostling, N.J., Cunningham, J.A., Harvey, T.H.P., Kouchinsky, A., Val'kov, A.K., Repetski, J.E., Stampanoni, M., Marone, E., Donoghue, P.C.J., 2010.
Fig. 7. Eopriapulites sphinx Liu and Xiao in Liu et al., 2014a from the Cambrian Fortunian Zhangjiagou Lagerstätte. (1–3) Micro-CT images of UMCU 14CHD0816-008 (Fig. 5.3); (1, 2) longitudinal sections through the posterior trunk part, arrows denote the gut; (3) transverse section through the posterior trunk part, arrow denotes the gut; (4) reconstruction, with body length/width ratio of about 15. Scale bar below (1) applies to (1–3), and scale bar right to (4) applies to (4) only. Scale bar represents 1 mm.
macrobenthos subsequently when reaching larger body sizes. The last common ancestor of the Cycloneuralia.—It has previously been proposed that the last common ancestor of the Cycloneuralia may have been a macroscopic, microannulated, and introvert-bearing worm, and that the Cambrian palaeoscolecids may represent such ancestral cycloneuralians (Budd, 1999, 2001, 2003; Eriksson and Budd, 2000). This rather priapulid-like last common ancestor of the Cycloneuralia is also supported by mitogenomics and phylogenomics, which suggest extant priapulids as a model of the last common ancestors of the Cycloneuralia (Webster et al., 2006). Because the cycloneuralians have emerged in the Fortunian Stage 7
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