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Gondwana Research 14 (2008) 277–283 www.elsevier.com/locate/gr

Origin, diversification, and relationships of lobopods ⁎ Jianni Liu a, , Degan Shu a,b, Jian Han a, Zhifei Zhang a, Xingliang Zhang a

a Early Life Institute, The Key Laboratory of Continental Dynamics, Northwest University, Xi'an, 710069, PR b School of Earth Sciences and Resources, China University of Geosciences (Beijing), 100083, PR China

Received 30 April 2007; received in revised form 25 September 2007; accepted 9 October 2007 Available online 25 October 2007

Abstract

As an extinct group, the origin, diversification and relationships of Cambrian lobopods have long been one of the most hotly-debated subjects. Lobopods used to be regarded as closely related to modern onychophorans and tardigrades, but the similarities are based on the few species of Cambrian lobopods and often on a fairly general level. With the discovery of new creatures and based on new observations on fossil lobopods, we consider that Cambrian lobopods show great diversity and reveal a close relationship between Cambrian lobopods and . In addition, comparison between the dorsal spines of Cambrian lobopods and small shelly fossils suggest that Cambrian lobopods might have originated from the Meishucun radiation and diversified in the Qiongzhusi radiation. © 2007 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.

Keywords: Cambrian lobopods; Arthropods; Small shelly fossils; Origin; Diversification

1. Introduction Conway Morris (1977) described a second lobopod, sparsa (see Ramsköld and Chen, 1998, Fig. 3.1), from the The supercontinent of Rodinia is described as tectonically . As the two undisputed lobopods discovered in the stable and coherent between 1000 and about 750 Ma (Hoffman, Middle Cambrian, these two taxa have been widely cited and 1991). The configuration of Rodinia has been vigorously discussed (Ramsköld, 1992; Hou and Bergström, 1995; Rams- examined by scientists around the world and numerous alternative köld and Chen, 1998; Bergström and Hou, 2001; Hou et al., 2004; models have been proposed (Yoshida et al., 2003; Maruyama Zhang and Aldridge, 2007). et al., 2007). It is generally accepted that the Laurentian, Baltica, Since the Lower Cambrian Chengjiang fauna was discov- Siberia and Gondwana blocks were certainly separated by the ered in 1984 (Hou et al., 1991), Hou et al. have described split-up of Rodinia in the Neoproterozoic and moving apart six species of lobopods before the end of last century, during the Ediacaran–Early Cambrian interval (McKerrow et al., they are sinicum (Fig. 1a) Chen et Hou 1992). The geographic distribution of lobopods in the Cambrian 1989; Luolishania longicruris (Fig. 1i) Hou et Chen 1989; including south China, Siberia, Greenland and North America, ferox (Fig. 1d) Hou, Ramsköld et Bergström indicates that this type of faunal community had dispersed 1991; Cardiodictyon catenulum (Fig. 1b) Hou, Ramsköld et worldwide in the interval from the Late Tommotian through the Bergström, 1991; Hallucigenia fortis (Fig. 1c) Hou et Atdabanian. The first lobopod to be described from the Cambrian Bergström 1995 and inermis (Fig. 1e) Chen, was pedunculata (see Briggs et al., 1994, Fig. 87, 88, Zhou et Ramsköld 1995; together with the other four 89) from the Burgess Shale, named by Walcott (1911).Later, lobopods auerswaldae (see Dzik and Krumbiegel, 1989, Fig. 1, 4) Pompeckj (1927) from the Lower Cambrian of northern Europe; whittingtoni (see Budd, 1997, ⁎ Corresponding author. Early Life Institute and Department of Geology, Northwest University, 229#, Taibai Road, Xi'an, 710069, PR China. Tel.: +86 Fig. 11.3, 11.4) Budd, 1997, kierkegaardi (see 29 88303706; fax: +86 29 88302128. Budd, 1993, Fig. 1, 2, 3) Budd, 1993 and Hadranax augustus (see E-mail addresses: [email protected], [email protected] (J. Liu). Budd and Peel, 1998, plate I, II and text-fig. 2) Budd and Peel,

1342-937X/$ - see front matter © 2007 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.gr.2007.10.001 278 J. Liu et al. / Gondwana Research 14 (2008) 277–283

Fig. 1. Early Cambrian lobopods from Chengjiang Fauna. a) Microdictyon sinicum ELI-JSMS0001; b) Cardiodictyon catenulum ELI-JSC0002A; c) Hallucigenia fortis ELI-JSH0007A; d) Onychodictyon ferox ELI-JSO0011A; e) Paucipodia inermis ELI-JSP0025A; f) Megadictyon cf. haikouensis Holotype ELI-JSMH008;g) decora Holotype ELI-J007; h) Miraluolishania haikouensis Holotype ELI-JSM0020A; i) Luolishania longicruris, the Camera Lucida drawing of ours. Note that the smallest units in scale bar represent 1 mm.

1998 from the Lower Cambrian of Greenland. These are With the new century coming, three distinct forms regarded as closely related with each other and they have certain Miraluolishania haikouensis (Fig. 1h) Liu et Shu 2004; similarities to modern onychophorans, tardigrades and arthropods Jianshanopodia decora (Fig. 1g) Liu et Shu 2006 and (Hou and Bergström, 1995; Budd, 1993, 1997). Megadictyon cf. haikouensis (Fig. 1f) Liu et Shu 2007 have been J. Liu et al. / Gondwana Research 14 (2008) 277–283 279 discovered by the Early Life Institute (abbreviated ELI) team, and (iv) as in the rare lobopod Miraluolishania, each appendage adding significant data to the group. This is not only because of a of Facivermis bears two rows of setae on its anterior and posterior larger number of specimens and species, but in particular because margins. Besides the affinities of Facivermis with lobopods, if we these three taxa bear mosaic features of both lobopods and turn F.yunnanicus upside down and interpret the pear-shaped end arthropods. Consequently, these Cambrian lobopods are now as the anterior of F. yunnanicus rather than the posterior, it is very regarded as the intermediate creatures between lobopods and similar to the pear-shaped anterior proboscis of priapulid arthropods (Xiao, 2004; Liu et al., 2004, 2006a, 2007). Xishania longiusula (Hu, 2001). The similarities are: (i) the The possible origin of the extinct lobopods has rarely been same ratio of width/length, about 1/20; (ii) the pear-shaped discussed (Dzik and Krumbiegel, 1989; Budd, 2001a,b). Dzik anterior proboscis; (iii) two or three circles of hooks which are and Krumbiegel (1989) suggested an origin from priapulid– located in the same place; (iv) the anterior projection of proboscis; palaeoscolecid-like worms through the development of seg- (v) the clear annulations and thin spines of the body. Furthermore, ments and limbs with, at the same time, a change in the mode of the mode of life of F. yunnanicus is intermediate between life from priapulid-style burrowing within the bottom sediment burrowing and crawling. We think that most part of the body of to the crawling on the sea bottom of lobopods. Budd also F. yunnanicus rested in the sediment, and that the anterior body discussed the relationship of , lobopods and and appendages protruded out above the sea floor to catch prey. Euarthropoda based on the segmentation and concept And in terms of the posterior morphology of Facivermis,we (Budd, 2001a,b). Although both hypotheses offer hope that conceive that the enlarged pear-shaped trunk ends with two or lobopods have a close relationship with priapulid–palaeoscole- three circles of hooks could have helped to fix the like an cid-like worms, no intermediate creatures have been discovered to anchor of a ship when it protruded the five pairs of appendages support this idea. Fortunately, the discovery of complete specimens and made purchase to allow it to prey upon its victim. of Facivermis yunnanicus gives direct fossil evidence for this As noted above, there are certain taxa of small shelly fossils hypothesis (Liu et al., 2006b). F.yunnanicus, not only possesses the such as Microdictyon that are now regarded as lobopod plates. characters of a priapulid, but also bears features typical of lobopods. One of these, Zhijinites,asQian et al. (2000) indicated, has features ThemodeoflifeofF. yunnanicus is also just between burrowing in common with the plates and spines of both Hallucigenia and crawling. Therefore, we considered that lobopods might have (Conway Morris, 1977)andOnychodictyon (Ramsköld and Hou, originated from priapulid–palaeoscolecid-like worms. Besides, 1991). These similarities include: (1) in gross morphology, both there are some lobopod plates discovered from the Meishucun structures are composed of a sub-round plate as a base and a spine; Stage of Cambrian, such as Zhijinites (Qian, 1984, 1989)and (2) as with Zhijinites, the outer surface of spines of Hallucigenia Cambroclavus (Qian, 1984, 1989), which are probably the plates of are finely granulated; (3) especially, there usually occurs in the lobopods (Qian et al., 2000). And the similarity between small same number and symmetry of plates in one sample, and this shelly fossils and lobopods plates are hotly discussed these years situation is in accord with those of dorsal spines of Hallucigenia (Dzik, 2003; Hou and Aldridge, 2007). Thus, we suggest that the and Onychodictyon. Therefore, we are inclined to regard Zhijinites lobopods originate as early as the Meishucun radiation or even in as likely isolated dorsal plates of lobopods; if accepted, then there is the and then diversify in the Cambrian. evidence that lobopods originated during or before the early Meis- hucun Stage. 2. Origin of lobopods 3. Diversification As noted above, the origin of lobopods is still obscure. Dzik and Krumbiegel's (1989) hypothesis of an origin from During the last few years, data on the range of Lower Cambrian priapulid–palaeoscolecid-like worms through the development lobopods has been greatly increased (Budd, 1993, 1997; Hou and of segments and limbs is the main contender. In lobopod Bergström, 1995; Budd and Peel, 1998; Ramsköld and Chen, evolution, whatever the origin, the mode of life changed from 1998; Liu et al., 2004, 2006a, 2007), while a few additional Middle priapulid burrowing to lobopod-style crawling. Conway Morris and Upper Cambrian taxa are now known (Collins, 1986; Maas (1997) thought that this transformation would have been and Waloszek, 2001). All these forms and the living onychophor- difficult to complete; however, it has its own reason based on ans are generally included in the taxon Lobopoda, following the the Ecdysozoa concept. Similar to the ideas of Dzik and suggestions of Simonetta and Delle Cave (1981). Although the Krumbiegel, Budd also offers hope that lobopods have a close majority of Cambrian lobopods sport spines or other , relationship with priapulid–palaeoscolecid-like worms based on however, as several authors indicated (Briggs, 1994; Wills et al., the segmentation and the Ecdysozoa concept (Budd, 2001a,b). 1994; Delle Cave et al., 1998), there is a fairly large morphological Furthermore, the discovery of complete specimens of variation within the group, even within a single Lagerstätte. F. yunnanicus gave direct fossil support to this hypothesis. Indeed, all the Cambrian forms were probably already strongly F. yunnanicus, not only possesses the characters of priapulid, but derived, although more or less closely related, radiating from a also bears features of typical lobopods. The affinity of Facivermis common source and this trend can be easily recognized: Pauci- with the lobopods is supported by (i) the lobe-like appendages; (ii) podia (Chen et al., 1995a) is the simplest lobopod with six pairs of the appendages having strong attachment with the trunk and appendages and a proboscis-like head area. Microdictyon attachment areas forming a round plate at a base; (iii) a fine canal (Ramsköld and Hou, 1991) bears pairs of sclerites with a series running centrally through the entire length of the each appendage; of perforated platelets; Hallucigenia (Conway Morris, 1977), with 280 J. Liu et al. / Gondwana Research 14 (2008) 277–283 long dorsal spines on the trunk and three pairs of appendages at the et al. that the association between Microdictyon and occa- anterior end of the trunk, is regarded as a typical ‘armored lobopod’ sionally occurs because of transportation. (Budd, 1997); Cardiodictyon (Hou and Bergström, 1995)bears25 Most of the lobopods, such as Hallucigenia, Onychodictyon, pairs of appendages on the trunk and pairs of unique triangular- Miraluolishania, bear pairs of strong and sharp spines on their shaped plates; Onychodictyon (Ramsköld and Hou, 1991), with trunk, which not only could be used to protect themselves, but also large papillae, has a strange appearance; Luolishania (Hou and could be actively used against prey. Besides, Miraluolishania each Chen, 1989a) is of generalized appearance, without specialized possesses a pair of eyes, which is significant for predators. In head structures; Miraluolishania (Liu et al., 2004) is much more addition, the claws of the lobopods would help them to get a firm derived, with pairs of eyes and antennae on the head and the trunk hold on the prey they were interested in. showing primitive tagmosis; Aysheaia (Whittington, 1978)is The large lobopods, Jianshanopodia and Megadictyon bear unique, without antennae but with a pair of grasping appendages in pairs of frontal appendages similar to those of front of the first pair of trunk appendages; Xenusion (Dzik and (Chen et al., 1994), together with a strong body and the Krumbiegel, 1989) is a large lobopod with pairs of dorsal plates; ‘Peytoia’ mouthparts of Megadictyon. We thus suppose that they Hadranax (Budd and Peel, 1998) is an incomplete animal bearing were predators. The branched lobe-like limbs of Jianshanopodia strong appendages and dorsal tubercles; Kerygmachela suggest that it could swim for only a short time when not crawling (Budd, 1993), a gilled lobopod, bears lateral lobes on the trunk; on the bottom. The other large lobopods such as Kerygmachela Pambdelurion (Budd, 1997), a typical lobopod, possesses lateral and Pambdelurion, which come from Sirrus Passet in north lobes and lobe-like limes on the trunk; Jianshanopodia (Liu et al., Greenland, also bear pairs of frontal appendages with long spines 2006a)andMegadictyon cf. haikouensis (Liu et al., 2007)areboth or ‘Peytoia’ mouthparts, indicating that they are also hunters. large lobopods within the Chengjiang Fauna, with a pair of grasping appendages. However, Jianshanopodia bears complex 5. Relationships branched appendages and a sucking pharyngeal mechanism, while Megadictyon cf. haikouensis possesses ‘Peytoia’ mouthparts and The Cambrian lobopods have repeatedly been supposed to caecae-like structures. have onychophoran and tardigrade affinities (Manton, 1977; Summing up, a striking variation in the number of morpho- Thompson and Jones, 1980; Bergström and Hou, 2001). logical characters indicates that Cambrian lobopods did undergo Robison (1985) concluded that Aysheaia is related to modern early diversification, and this may give us the impression that their onychophorans. However, although like those of onychophor- shared ancestor probably lived far back into the Precambrian. ans, the lobopods had strong terminal claws on their legs, other characters such as the location of mouth, the lobe-like limbs and 4. Mode of life the ornament of the trunk are all different from those of modern onychophorans. Besides, there is a reasonable number of It is generally held that lobopods crawled on other organisms lobopods and their morphologies show a range of diversity, but using their hook claws because of notable associations between onychophoran morphology does not show much diversification. certain lobopods and particular animals, such as Aysheaia,which Thus, we think that there is not close relationship between the is commonly found associated with sponges (Whittington, 1978) Cambrian lobopods and modern onychophorans. (see Briggs et al., 1994,Fig.89).Similarly,Microdictyon was A comparison between lobopods and tardigrades reveals described as associated with Eldonia (Chen et al., 1991). In numbers of differences, which we would contend to show that reconstructions they have been illustrated as clinging to sponges they are unrelated. As indicated by Bergström and Hou (2001), and eldoniids, and Aysheaia probably sucked the juice of the lobopods and tardigrades share the presence of a terminal mouth sponges (Whittington, 1978) and that Microdictyon was pelagic without jaws (at least in Aysheaia and Paucipodia), but Robison (Chen et al., 1995b). In terms of the morphology of Aysheaia,we (1985) stated that the location of mouth is different in differ- think that there exists this possibility. Besides, we agree that ent species of tardigrades; some species of lobopods, e.g. sucking predation is a possibility. Alternatively, we think that the M. haikouensis, H. fortis, are observed with an antero-ventrally association between Microdictyon and Eldonia does not indicate located mouth. Also, Bergström and Hou (2001) regarded that that Microdictyon was pelagic, because as Dzik et al. (1997) lobopods share similarities with tardigrades in the presence shown, eldoniids were shelled animals of bilateral organization of feet with several claws. Unfortunately, most lobopods bear that lived a gregarious life on the sea bottom. Deposition was only two claws at the end of their legs, such as Onychodictyon, sudden in the fossiliferous intervals and some animals most likely Miraluolishania, Hallucigenia, Microdictyon and Cardiodictyon; were transported. Hou and Bergström (1995) think that the small claws at the distal extremity of the legs are not observed in some and light xenusions were not likely to have been sorted along with species such as Xenusion, Jianshanopodia and Megadictyon. the fairly large-shelled eldoniids as a result of transport. However, Furthermore, as Robison (1985) stressed, the claws of Aysheaia and no association between Microdictyon and Eldonia occur in our 45 tardigrades are not comparable in structure and probably are not specimens. Indeed, Microdictyon, Paucipodia and Onychodictyon homologous. Bergström and Hou (2001) also indicted that both is often observed to be buried with burrowing worm priapulid lobopods and tardigrades lack antennae. However, Miraluolishania (Fig. 2), which suggests that they live in similar environment. is reported to bear a pair of dorsal antennae. It was noted that that Priapulids were burrowing under the sea bottom, whereas lobopods when moulting, Xenusion left its old cuticle through a mid-dorsal were crawling on the sea bottom. Therefore, we agree with Dzik split, while tardigrades do it anteriorly through the oral opening J. Liu et al. / Gondwana Research 14 (2008) 277–283 281

Fig. 2. Lobopods are buried with priapulids. a) Paucipodia inermis is buried with priapulids; b) and c) Microdictyon sinicum is buried with priapulids; d) Onychodictyon ferox is buried with priapulids. Note that the smallest units in scale bar represent 1 mm. after they have expelled the cuticular elements of the buccal appa- mented limbs or lobe-like legs. The arthropodian features of ratus. Also, the diminutive size of tardigrades is strongly different Miraluolishania are its primary cephalization with paired eyes, from lobopods. Walossek and Müller (1994) described fossils of the paired antennae, and preliminary tagmosis. As is well known, the tardigrade Boeckelericambria pelturae discovered from the Middle primary cephalization and preliminary tagmosis are both nov- Cambrian and suggested that tardigrades evolved their diminutive elties of ‘arthropodation’. The occurrence of a pair of eyes and size at the beginning of the Cambrian or in the Precambrian. Taken antennae indicates (1): Both the protocerebrum and the together, the above differences strongly indicate that lobopods and deutocerebrum of Miraluolishania have had some degree of tardigrades are undoubtedly unrelated. development. (2): The antennae would be innervated not later Now we think that lobopods and arthropods are closely related. than the eye, which has been verified by developmental biology of Lobopods are probably the ancestor of the arthropods, and some living onychophorans (Eriksson et al., 2003). (3): The antennae of intermediate forms have been discovered. Miraluolishania,a Miraluolishania are probably the anterior-most limbs, creature with a mosaic of characters both lobopod and , which are different from the frontal limbs of other lobopods, gives strong support to the idea that arthropods should be rooted e.g. Kerygmachela (Budd, 1993), Pambdelurion (Budd, 1997) in the early lobopods. The lobopodian features of Miraluolishania and Aysheaia. On the other hand, the antennae of Miraluolishania are its worm-like body design, the dorsal spines, and non-seg- are quite like the antennae of the stem-group euarthropods, such 282 J. Liu et al. / Gondwana Research 14 (2008) 277–283 as Fuxianhuia, Naraoia, Xandarella (Bergström and Hou, 2001). the relationships of Cambrian lobopods to other phyla indicates The evidence strongly suggests that Miraluolishania represents a that lobopods have a much closer relationship with arthropods step in the evolutionary ladder leading to the euarthropods (Xiao, than and Tardigrada. This indication provides 2004). further evidence that arthropods may not be as closely related to Like Kerygmachela and Pambdelurion, Jianshanopodia the annelids as have been commonly thought. Furthermore, we and Megadictyon cf. haikouensis are the two big lobopods provide new evidences about the origin of lobopods, which not which have been found to bridge lobopods and arthropods. only suggests that lobopods might have originated from Jianshanopodia, with the complex branched appendages, throws priapulid–palaeoscolecid-like worms, but also breaks down the new light on the origin of biramous appendages. It is well known view that the phyla appeared abruptly in the Cambrian with no that the most obvious feature of arthropod diversity is manifested hints of their forebears under the weight of the similarities between in the number, morphology and function of their appendages. some small shelly fossils and the plates of lobopods. Antennae, mouthparts, walking legs, grasping and swimming appendages are all modifications of the basic jointed-leg structure Acknowledgments that defines the (Budd, 1996; Shubin et al., 1997). It is generally held that jointed legs evolved from simple unjointed This work was supported by the National Science Foundation appendages of Cambrian lobopods. Cambrian taxa with different of China (grants 40332016 and 30270207), the Program for types of “arthropodization” and limb morphology can be identified Changjiang Scholar and Innovative Research Team in the (Shu et al., 1995; Hou and Bergström, 1997; Zhang et al., 2003). Universities, and Ministry of Sciences and Technology of China Some paleontologists have hypothesized that fusion between the (PCSIRT, grant 2000077700). The authors are indebted to Dr. lateral lobes and ventral might have given rise to the Susan Turner for improving the English language; Yanbing Ji and biramous limb (Shubin et al., 1997; Budd, 1999). It is one Yanchun Yao for field work help. Special thanks are given to evolutionary possibility. 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