Three head-larvae of Hesslandona angustata (Phosphatocopida, Crustacea) from the Upper Cambrian of western Hunan, South China and the phylogeny of Crustacea

Gondwana Research 21 (2012) 1115–1127

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Three head-larvae of Hesslandona angustata (Phosphatocopida, Crustacea) from the Upper Cambrian of western Hunan, South China and the phylogeny of Crustacea Huaqiao Zhang a, b, Xi-ping Dong a, b,⁎, Shuhai Xiao c a b c

School of Earth and Space Sciences, Peking University, Beijing 100871, PR China State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, PR China Department of Geosciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061, USA

a r t i c l e

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Article history: Received 13 March 2011 Received in revised form 16 June 2011 Accepted 1 July 2011 Available online 14 July 2011 Handling Editor: P. Eriksson Keywords: ‘Orsten’-type Phosphatocopida Ontogeny Phylogeny Upper Cambrian South China

a b s t r a c t We describe three head-larvae of the phosphatocopid Hesslandona angustata of ‘Orsten’-type preservation from the Upper Cambrian Bitiao Formation in Wangcun section, western Hunan, South China. The head-larvae are small (around 300 μm long) and bear four pairs of functional limbs, presumably representing the first ontogenetic stage. A comparison with the head-larvae of Vestrogothia spinata from the same locality and horizon indicates that these head-larvae are identical in terms of appendage design. These head-larvae allow further comparison with phosphatocopids from other ontogenetic stages and other localities. We take these two species as representatives of Euphosphatocopida and include their ontogenetic information, combined with other ‘Orsten’-type stemlineage crustaceans and crown-group crustaceans, into a computer-based cladistic analysis to explore the relationships of early crustaceans. The phylogeny of the Crustacea sensu lato is reconstructed and the autapomorphies of each node on the phylogenetic tree are given. The occurrence and development of the proximal endite (and its derivatives) can be used to trace the evolution of crustaceans. The evolutionary path from the origin of crustaceans to crown-group crustaceans consists of five steps. These steps are (1): the proximal endite occurred but only on the third pair of limbs and only in later larval stages, (2): the proximal endite occurred on the third pair of limbs since the first ontogenetic stage and later also on the second pair of limbs, (3): the proximal endite occurred on all the post-antennular limbs simultaneously since the first ontogenetic stage, (4): the proximal endites on the second and third pairs of limbs were enlarged to form a coxa and (5): the proximal endites on post-mandibular limbs were enlarged to form a coxa in the malacostracan eucrustaceans. © 2011 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved.

1. Introduction Exceptionally preserved Lagerstätten (e.g. the Doushantuo-type fossils, the Burgess Shale-type fossils and the ‘Orsten’-type fossils, see Butterfield, 2003) from Neoproterozoic and early Paleozoic rocks have contributed significantly to elucidate the early evolution of metazoans, (e.g. Xiao et al., 1998; Chen, 2004; Maas et al., 2006). The Crustacea, representing the third most diverse arthropod class (Brusca and Brusca, 2003), may have originated in the Neoproterozoic based on molecular studies (Regier et al., 2005). Although arthropods are abundant and diverse in the Lower Cambrian Chengjiang biota, the occurrence of crustaceans has been controversial (Hou and Bergström, 1997; Chen, 2009). In contrast, Cambrian ‘Orsten’-type assemblages contain a great number of crustaceans and provide an excellent record of the origin and early evolution of arthropods and crustaceans (Maas et al., 2006). ‘Orsten’-type preservation is a special mode of taphonomy. It selectively preserves cuticle-bearing animals and generally the ⁎ Corresponding author at: School of Earth and Space Sciences, Peking University, Beijing 100871, PR China. Tel.: + 86 10 6275 3604; fax: + 86 10 6275 1187. E-mail address: [email protected] (X. Dong).

preserved specimens are b2 mm in size. Typically, the cuticle is impregnated or encrusted by calcium phosphate, but internal organs were decomposed, so that the fossils are in most cases hollow or secondarily filled with amorphous phosphate. But in rare circumstances, musculature and possible digestive tracts can be preserved (Müller and Walossek, 1985; Andres, 1989). ‘Orsten’type fossils are three-dimensionally preserved with little diagenetic deformation. As such, they provide high-resolution (~ 0.5 μm) anatomical information about cuticular structures such as setae and glandular openings. In addition, specimens representing different developmental stages of the same species can be preserved, allowing ontogenetic reconstructions (Maas et al., 2006). ‘Orsten’-type fossils have been reported from a very limited number of localities in the world, ranging in age from the Lower Cambrian (Hinz, 1987; Siveter et al., 2001, 2003; Zhang et al., 2007, 2010) to the Lower Ordovician (e.g. Andres, 1989; Roy and Fåhræus, 1989). The dominant fossils in ‘Orsten’-type Lagerstätten are (pan) arthropods (Maas et al., 2006). In combination with arthropods from Burgess Shale-type Lagerstätten, these fossils offer important insight into the early evolution of arthropods (Walossek and Müller, 1998a,b; Waloszek et al., 2005, 2007).

1342-937X/$ – see front matter © 2011 International Association for Gondwana Research. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.gr.2011.07.003

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Phosphatocopids are the most abundant and diverse arthropod fossils in ‘Orsten’-type Lagerstätten (Maas et al., 2006). They are widely accepted as representing the sister-taxon of extant crustaceans or the Eucrustacea (Maas et al., 2003; but see Hinz-Schallreuter, 2000 for different opinions). Their hollow shields or isolated valves have been reported from many localities in Scandinavia (Müller, 1964), North America (Siveter and Williams, 1997), Britain (Williams and Siveter, 1998), and Siberia (Müller et al., 1995), but specimens with soft parts are rare and have been discovered mainly from the Upper Cambrian of southern Sweden (Müller, 1979, 1982; Maas et al., 2003) and South China (Dong et al., 2005). In addition, sporadic material with soft part anatomy has been reported from the Lower Cambrian of Britain (Hinz, 1987; Siveter et al., 2001, 2003), the Middle Cambrian of Australia (Walossek et al., 1993), and the Upper Cambrian of Poland (Maas et al., 2006). Very recently, new specimens of phosphatocopids with soft part anatomy have been recovered from the Lower Cambrian Comley limestone in England (Thomas Harvey, pers. comm., 2010). ‘Orsten’-type fossils have been known for more than 30 years (Müller, 1979), but it was not until 2005 when similarly preserved fossils as represented by the Phosphatocopida and Skaracarida were reported from China (Dong et al., 2005). The Chinese material was collected from the Upper Cambrian Bitiao Formation at the Wangcun section in Yongshun County, western Hunan (Dong et al., 2005). The Wangcun phosphatocopid specimens are typically b400 μm in size, representing the earliest ontogenetic stages, including what are known as head-larvae. The term “head-larva” of Walossek and Müller (1990) refers to a euarthropod larva that consists of the same number of segments as the head of its adult stage. Liu and Dong (2009) described two head-larvae of Vestrogothia spinata Müller, 1964 from Wangcun section and assigned them to the first ontogenetic stage. V. spinata is a representative species of the suborder Vestrogothiina Müller, 1982. Here we describe new material of Hesslandona angustata Maas et al., 2003, a representative of suborder Hesslandonina Müller, 1982, from the same locality and horizon. H. angustata was first reported from southern Sweden but only one specimen was preserved with soft part anatomy (Maas et al., 2003). Our material consists of three head-larvae of H. angustata with soft part preservation and allows a comparative analysis with the head-larvae of V. spinata to elucidate the ground pattern of the Phosphatocopida and Euphosphatocopida. We incorporated the new developmental information in a computer-based cladistic analysis to illuminate the phylogenetic relationships and early evolution of crustaceans. 2. Material and methods The three head-larvae were liberated from limestone samples collected from the Bitiao Formation at Wangcun, western Hunan, South China. The horizon yielding the ‘Orsten’-type fossils is stratigraphically dated to the Westergaardodina cf. calix–Prooneotodus rotundatus Zone (conodonts), Paibian Stage, Furongian Series (Dong et al., 2004). The samples were processed following the acetic acid etching procedures as suggested by Müller (1985). Fossils were handpicked from residues and examined under a scanning electron microscope. All scanning electron micrographs were processed using Adobe Photoshop CS. Four specimens were analyzed using synchrotron radiation X-ray tomographic microscopy (SRXTM; see Donoghue et al., 2006 for its application to paleontology) and one of them is shown in Fig. 1. SRXTM was carried out at the Swiss Light Source at the Paul Scherrer Institute, Villigen, Switzerland. Cladistic analysis was carried out using PAUP (Swofford, 2002), and the cladograms and phylogenetic trees derived from PAUP were redrawn using Adobe Illustrator CS2. 3. Description All the specimens illustrated in this paper are deposited in the Geological Museum of Peking University (repository number with

prefix GMPKU). The terminology and abbreviations used in this paper follow Maas et al. (2003). 3.1. Systematic paleontology Class Crustacea Brünnich, 1772 Order Phosphatocopida Müller, 1982 Suborder Hesslandonina Müller, 1982 Family Hesslandonidae Müller, 1964 Genus Hesslandona Müller, 1964 Type-species Hesslandona necopina Müller, 1964 Hesslandona angustata Maas et al., 2003 (Figs. 1–4) 2003 Hesslandona angustata Maas, Waloszek and Müller, pp. 89–101, plates 26–27, text fig. 39. 2009 Hesslandona angustata Liu and Dong, pp. 18–26, figs. 1, 3, 4(a), (b). 2011 Hesslandona angustata Zhang, Dong and Maas, pp. 157–175, figs. 1–6. 3.1.1. Material examined Three specimens of ‘Orsten’-type preservation with dimensions no larger than 308 μm, all bearing four pairs of limbs and representing the head-larvae and the first ontogenetic stage. 3.1.2. Occurrence Westergaardodina cf. calix–Prooneotodus rotundatus Zone (conodonts), Upper Cambrian Bitiao Formation, Paibian Stage, Furongian Series from Wangcun section, Yongshun county, western Hunan, South China. 3.1.3. Description The specimens on hand and their valves and limbs are reconstructed in Fig. 4. The shields are bivalved, and the bivalved shield is amplete (i.e., maximum valve height located at the anterior–posterior midpoint) and the maximum valve length is located between the dorsal rim and the dorsal–ventral midline. The valve is semicircular in outline and the central part is convex. The valve surface is smooth without any lobes or spines or any ornament (Fig. 4D, E). The two valves are fused dorsally with each other through a relatively narrow interdorsum (Fig. 1F). The doublure is continuous from anterior to posterior, narrowest ventrally, wider anteriorly and widest posteriorly (Figs. 1A, 2A, 3D). The inner lamella is well preserved in one specimen (Fig. 2A). The body proper is completely enveloped in the bivalved shield, fused with the head shield dorsally. The segmentation of the body proper is deduced from the limb insertions. The anterior part is the hypostome/labrum complex, followed by the hind body. The hypostome (Figs. 2B, 3B) is a strongly sclerotized structure and it provides the insertion area for the antennulae and antennae. It is followed by the three-cupped median eyes ventrally, but in the specimens on hand the median eyes are not preserved well. Posterior to the possible median eyes, the hypostome protrudes into a long and rotund structure, the labrum. The labrum protrudes like a funnel well covering the atrium oris. The hind body following the labrum is triangular in outline and tapers into its end, where the possible furcal rami and possible terminal anus are not observed. The antennulae can be studied in two specimens (Figs. 2, 3). They are uniramous and arise from the antero-lateral edges of the hypostome, short and peduncle-shaped, weak in segmentation and setation. Their tips are smooth without any setae. The weak segmentation and setation is, however, a preservational artifact. The antennae (Figs. 1B, 2B, 3B) arise from the medio-lateral edges of the hypostome. They are biramous and consist of the limb stem, the endopod and the exopod. The limb stem is un-divided, antero-posteriorly flattened and proximally drawn into a strong gnathobase with several strong setae inserting on its inner edge and pointing to the labrum. The endopod is two-divided, inserting

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Fig. 1. Hesslandona angustata Maas et al., 2003 from Wangcun section, GMPKU2397, about 211 μm long. A–D, scanning electron micrographs; E–F, SLS (Swiss Light Source) surface models. A, overall view of head-larva; B, close-up of A, showing the right antennae and mandibles; C, close-up of A, showing the left antennae and mandibles; D, close-up of A, a comparison of the design between the right and left mandibles; E, ventral reconstruction; F, dorsal reconstruction, showing the relatively narrow interdorsum. Abbreviations: am, arthrodial membrane; anl, annulus; a1, antennula; a2, antenna; bas, basipod; cox, coxa; en, endopod; en1 and en2, first and second segments of endopod; ex, exopod; gnb, gnathobase; hb, hind body; id, interdorsum; lbr, labrum; lst, limb stem; mdb, mandible; mx1, first post-mandibular limbs; pe, proximal endite; pgn: paragnath; set, setae; ste, sternum. Scale bar: A, 48 μm; B, 23 μm; C, 17 μm; D, 26 μm; E, 38 μm; F, 37 μm.

on the inner terminal edge of the limb stem. Each segment protrudes medially into an endite with several spine-like setae on its medial margin. The distal segment bears a long seta on its distal face and it is directed parallel to the long axis of the endopod. The exopod is a little longer than the endopod and is inserted on the outer distal edge of the limb stem. It is multi-annulated, estimated to have about ten annuli in this ontogenetic stage, and each annulus bears a seta at its medial edge facing the endopod. The mandibles (Figs. 1D, 3D) are basically of the same design as the antennae, consisting of the limb stem, the endopod and the exopod, and the endopod and the exopod are also like those of the antennae. However, the mandibular limb stem consists of two segments, the proximal coxa and the distal basipod. The coxa articulates with the main body and arises postero-laterally to the hypostome,

proximally drawn into a strong gnathobase bearing several setae. The first post-mandibular limbs can be studied in two specimens (Figs. 2, 3). They are composed of a basipod, an endopod and an exopod, and there is a wedge-shaped structure inserting at the medio-proximal base of the basipod. This wedge-shaped structure is the so-called proximal endite. The proximal endite is inverse-triangular in shape and bears several setae on its medio-proximal edge. The endopod and exopod are not well-preserved and their segmentation is unclear. 3.2. Discussion Hesslandona angustata is phylogenetically more primitive than other species of the suborder Hesslandonina due to its simple valve

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Fig. 2. Scanning electron micrographs of Hesslandona angustata Maas et al., 2003 from Wangcun section, GMPKU2363, about 225 μm long. A, overall morphology of the head-larva, revised from Liu and Dong (2010, Fig. 4b); B, anterior view of the hypostome/labrum complex, showing well preserved antennulae; C, close-up of A, showing the antennulae, antennae and labrum; D, close-up of A, showing the right first post-mandibular limb. See Fig. 1 for abbreviations. Scale bar: A, 34 μm; B, 23 μm; C, 20 μm; D, 8 μm.

structures (Fig. 4D, E) and soft body anatomies (Zhang et al., 2011). It is hitherto known only from two localities, the southern Sweden orsten (Maas et al., 2003) and Wangcun section (Zhang et al., 2011; this paper). Maas et al. (2003) reported thirty-one specimens, but only one of them is preserved with soft part anatomy. Zhang et al. (2011) described H. angustata and established the first and second ontogenetic stages based on the western Hunan material that preserves soft-body anatomical information. The material in this paper (221 μm, 225 μm and 308 μm long respectively) is smaller compared with specimens illustrated in Zhang et al. (2011) (N298 μm or larger), potentially representing still earlier ontogenetic stages. Therefore they are useful for character polarization in phylogenetic analysis and in discussion of character evolution. Liu and Dong (2009) described two head-larvae of Vestrogothia spinata from the Wangcun section. They are extremely small and measured 176 μm and 247 μm in size respectively, nearly matching the smallest phosphatocopids ever reported (Maas et al., 2003, pl. 45, a head-larva of V. spinata measured 170 μm long). A detailed description of these two head-larvae of V. spinata can be found in Liu and Dong (2009). A comparison of the head-larvae between H. angustata and V. spinata shows that they are identical in terms of appendage design in spite of minor difference in size. Their identical appendage design may underlie the ground pattern of the Euphosphatocopida (see Section 5). 4. Phylogenetic implications The Phosphatocopida was traditionally regarded as being closely related to the Bradoriida or to the Ostracoda (Müller, 1964, 1979, 1982) and this is still followed by some researchers, e.g. Hinz-Schallreuter (1998, 2000). Phosphatocopids, bradoriids and ostracods look alike in valve morphology. However, this superficial similarity likely represents

convergent evolution and their systematic positions are different. The Bradoriida is a marine bivalved arthropod group ranging from the Lower Cambrian to Middle Ordovician. The Bradoriida sensu stricto comprises seven families and might represent a natural group (Williams et al., 2007). The soft part anatomy of the most derived bradoriid Kunmingella douvillei (Mansuy, 1912) from the Chengjiang biota indicates that the bradoriids are not crown-group crustaceans, and they are probably an early offshoot on the evolutionary path towards the Crustacea (Hou et al., 1996; Shu et al., 1999; Williams et al., 2007; Hou et al., 2010). The Ostracoda is a prolific bivalved eucrustacean group and the earliest unambiguously identified ostracode occurs in the Lower Ordovician Tremadoc Stage; some Cambrian bradoriids might possibly be ostracodes but their interpretation is uncertain due to the lack of soft body preservation (Williams et al., 2007). The Phosphatocopida has been reinterpreted as a sister-taxon to the Eucrustacea (Walossek, 1999; Maas et al., 2003; Siveter et al., 2003; Waloszek, 2003; Maas and Waloszek, 2005) and this interpretation has been confirmed in more recent analysis (e.g. Zhang et al., 2007). The sister-taxon relationship of the Phosphatocopida and Eucrustacea is supported by several synapomorphies, e.g. a cephalon incorporating five limb-bearing segments in late larval stages, occurrence of labrum, atrium oris, paragnath on the mandibular sternite, limb stem of antennae and mandibles originally composed of separate coxa and basipod, a single sternum derived from the fusion of anterior three sternites, and fine hairs on the structures around the mouth opening and enditic surfaces of all head limbs and also on the setae and spines. The specimens of H. angustata illustrated in this paper are very small, around 300 μm or even smaller in size. They have developed four pairs of functional limbs, presumably representing the first postembryonic stage or the so-called “head-larva” described by Walossek and Müller (1990). In phosphatocopid larvae, a typical labrophoran cephalon (i.e. a cephalon incorporating five limb-bearing

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Fig. 3. Scanning electron micrographs of Hesslandona angustata Maas et al., 2003 from Wangcun section, GMPKU2398, about 308 μm long. A, overall morphology of head-larva, anterior to the left; B, anterior view of the hypostome/labrum complex, showing the hypostome and antennulae; C, close-up of A, showing the right antenna and mandible; D, close-up of A, showing the left mandible and first post-mandibular limb; E, close-up of A, showing the right mandible and antenna; F, close-up of A, showing the left first post-mandibular appendage. See Fig. 1 for abbreviations. Scale bar: A, 43 μm; B, 26 μm; C, 24 μm; D, 31 μm; E, 28 μm; F, 23 μm.

segments) forms when the second post-mandibular limbs are inserted into the head ontogenetically after the head-larval stage. The head-larva is phylogenetically a primitive character derived from the ground pattern of the Euarthropoda or even earlier and is inherited by stemlineage crustaceans (Waloszek, 2003; Waloszek et al., 2005). The Phosphatocopida, as illustrated in this paper, starts its first postembryonic stage with a presumed head-larva with four pairs of functional limbs, different from the eucrustacean orthonauplius. Among the extant crustaceans, the first postembryonic stage starts with a shorter larva with only three appendage-bearing segments and each segment has a pair of functional limbs, i.e. the antennulae, antennae and mandibles from anterior to posterior, and this larva is the so-called ‘short-headlarva’ or orthonauplius (Walossek and Müller, 1990). An orthonauplius

characterizes the last common ancestor of Eucrustacea although many derived eucrustaceans pass their nauplius period in the embryonic stage and hatch as a metanauplius or even more advanced stages (Brusca and Brusca, 2003). Therefore, the head-larva is a key character (plesimorphic status) distinguishing phosphatocopids and other stem-lineage crustaceans from the Eucrustacea (Maas and Waloszek, 2005). 5. Comparison with other phosphatocopid head-larvae Phosphatocopida consists of two sub-groups, the univalved Klausmuelleria salopensis Siveter et al., 2003 from the Lower Cambrian of England and the bivalved Euphosphatocopida from the Upper Cambrian (Siveter et al., 2003). It is proposed that K. salopensis is closely related to

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Fig. 4. Reconstructions of Hesslandona angustata Maas et al., 2003, not to scale. A is based on specimen GMPKU2397 (Fig. 1), B on specimen GMPKU2363 (Fig. 2), and C on specimen GMPKU2398 (Fig. 3). Some limbs are omitted for clarity and their insertion areas are denoted with hatched circles. D, lateral external view of left valve, smooth without any lobes, nodes, sulci or any ornament; E, laternal internal view of right valve showing the inner surface. F–H, post-antennular limbs showing their basic design. F, antennae, consisting of an undivided limb stem, a two-divided endopod and a multi-annulated exopod with ten annuli; G, mandible, consisting of a two-divided limb stem with separate coxa and basipod, a two-divided endopod and a multi-annulated exopod with about ten annuli; H, first post-mandibular limb, consisting of a proximal endite, a basipod, a three-divided endopod and a multi-annulated exopod with about nine annuli. The proximal endite is wedge-shaped inserting at the medio-proximal edge of the basipod. See Fig. 1 for abbreviations.

the univalved Dabashanellidae from the Lower Cambrian of Southwest China, but uncertainties still exist due to lack of soft body information of dabashanellids (Hou et al., 2001; Maas et al., 2003). Walossek et al. (1993)

reported isolated appendages from the Middle Cambrian of Australia and considered them as possible phosphatocopid limbs. These appendages lack exopods and might represent a specialized lifestyle, but their true

Fig. 5. A–C, three shortest cladograms (of thirty-three) derived from PAUP. They differ in the internal relationships within the clade (Oelandocaris oelandica + Sandtorpia vestrogothiensis + Henningsmoenicaris scutula) and the monophyly of (Martinssonia elongata+ Musacaris gerdgeyeri + Labrophora). D, 50% majority rule tree of 33 shortest trees. Numbers adjacent to nodes represent support values: the upper value is the Bremer Support (computed to extra 10 steps), and the lower value is the Bootstrap Support (only values≥ 50% are shown).

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Fig. 6. Simplified phylogeny of Crustacea sensu lato derived from thirty-three shortest trees and the 50% majority rule, showing the relationships of stem-lineage crustaceans. Numbers in boxes denote the autapomorphies of each node. Box 1: the second and third pairs of limbs specialized and different from the succeeding ones; exopods of (at least) the second and third pairs of limbs being multi-annulated with setae on the outer and distal margin. Box 2, Crustacea sensu lato: proximal endite occurring only on the third pair of limbs and only in larger individuals; the exopods of the second and third pairs of limbs specialized, being multi-annulated with setae on the medial margin facing the endopods. Box 3, Oelandocarididae: exopods of the second and third pairs of limbs in early stages with three setae on the terminal article and two on the sub-terminal article; exopods since the fourth limbs composed of two articles, with proximal part joining to the proximal endopod portion; cephalon consisting of five limb-bearing segments in late larval stages. Box 4: proximal endites occurring on the third pairs of limbs since the first ontogenetic stage and also on the second pair of limbs in later larval stages; the fourth pair of limbs also specialized and different from the following trunk limbs. Box 5, Cambropachycopidae: a single compound eye inserted anterior to the head; uniramous paddle-shaped trunk limbs. Box 6: proximal endites occurring on all the post-antennular limbs since early ontogeny; the exopods of the anterior five pairs of limbs are specialized. Box 7, Labrophora: cephalon incorporating five limb-bearing segments in late larval stages; limb stem of antennae and mandibles two-divided since early ontogeny, composed of separate coxa and basipod; labrum, paragnath, fine hairs and a single sternum are present; anus terminally positioned. Box 8, Eucrustacea: first post-mandibular limbs specialized as maxillulae; first post-embryonic stage starts as an orthonauplius; epipodites occurred on post-maxillulary limbs. Box 9, Phosphatocopida: shields with special doublure; dorsal rim long and straight; antennulae short and thin, weak in segmentation and setation; endopods of biramous limbs three-divided. Box 10, Euphosphatocopida: an all-embracing bivalved shield with a single dorsal furrow; limb stem of antennae un-divided since early ontogeny; limb stem of mandibles un-divided in late larval stages; antennal and mandibular endopods two-divided. Type-C larva and C. baltica were not included in this cladistic analysis but their possible positions are denoted with dashed line. In addition, a cephalon incorporating five limb-bearing segments in late larval stages might possibly characterize Box 6 on the condition that Mu. gerdgeyeri possessed such a cephalon.

affinity is still uncertain. Phosphatocopid head-larvae are reported from many species but only a few of them preserve information about appendage design especially of the antennae and the mandibles (Maas et al., 2003; Siveter et al., 2003). Below we compare the Hunan specimens with other phosphatocopid head-larvae. Klausmuelleria salopensis was established on the basis of three headlarvae (Hinz, 1987; Siveter et al., 2003). Its antennulae are not well preserved, but they are possibly short and thin, and have weak segmentation and setation, and may have a tuft of distal setae like those of other phosphatocopids (Siveter et al., 2001, 2003). The endopods of the antennae, mandibles and the first post-mandibular limbs are all threedivided, and the limb stems of the antennae and mandibles are composed of two separate segments, the coxa and the basipod, whereas the limb stem of the first post-mandibular limbs is composed of the basipod and the proximal endite (Siveter et al., 2001, 2003). K. salopensis is resolved as the sister-taxon to the Euphosphatocopida, because the basic design of the antennae and the mandibles of K. salopensis is different from that of the Euphosphatocopida. Additionally, a univalved head shield is a plesiomorphic state inherited from the ground pattern of Euarthropoda, and it is different from the bivalved condition of Euphosphatocopida. Compared with other stem-lineage crustaceans, the apomorphies of the last common ancestor of Phosphatocopida (=K. salopensis +Euphosphatocopida) in

the head-larval stage include at least 1) the antennulae short and thin, weak in segmentation and setation; 2) the antennal and the mandibular limb stem composed of separate coxa and basipod; 3) the endopods of the antennae, the mandibles and the first post-mandibular limbs are all threedivided; and 4) other apomorphies, e.g. the occurrence of labrum, paragnath, single sternum and fine hairs. A detailed discussion on the autapomorphies of the Phosphatocopida and Labrophora is presented in Section 7. As exemplified by head-larvae of H. angustata (Figs. 1–4) and Vestrogothia spinata (Liu and Dong, 2009), the Upper Cambrian phosphatocopids (Euphosphatocopida) are all bivalved and the antennal and mandibular endopods are two-divided. The antennal limb stem is un-divided, possibly resulted from the fusion of a coxa and a basipod (Maas et al., 2003). The mandibular limb stem is variable; some are two-divided since the first ontogenetic stage whereas others are un-divided. A two-divided mandibular limb stem consisting of separate coxa and basipod is phylogenetically more primitive and is reported in V. spinata from the Upper Cambrian of Sweden and the Upper Cambrian of Hunan (Maas et al., 2003; Liu and Dong, 2009), in Hesslandona suecica Maas et al., 2003 from the Upper Cambrian of Sweden (Waloszek and Maas, 2005), in H. angustata and Hesslandona necopina Müller, 1964 from the Upper Cambrian of Hunan (Zhang et al., 2011; this paper) and

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also in Hesslandona sp. sensu Dong et al., 2005 from the Upper Cambrian of Hunan (Zhang et al., 2011). Compared with the apomorphies of the last common ancestor of Phosphatocopida analyzed above, the autapomorphies of the last common ancestor of Euphosphatocopida in head-larval stage include at least 1) an all-embracing bivalved shield with a long and straight dorsal rim; 2) the endopods of the antennae and mandibles two-divided; and 3) the antennae composed of an undivided limb stem since the first ontogenetic stage. A two-divided mandibular limb stem in head-larval stage characterizes the ground pattern of the Euphosphatocopida but is a plesiomorphic state inherited from the ground pattern of Labrophora (see Section 7). It is possible that most euphosphatocopid species start their first post-embryonic stage with an undivided antennal limb stem and a two-divided mandibular limb stem. 6. Comparison with euphosphatocopids in later larval stages Most fossils in ‘Orsten’-type preservation, with the exception of Skara (Müller and Walossek, 1985), are preserved with only larval stages; our discussion is restricted to the larval stages. Klausmuelleria salopensis is known only from three univalved head-larvae and lacks information about its later ontogenetic stages (Hinz, 1987; Siveter et al., 2003). Whether the antennal and mandibular coxa and basipod would be fused in a later ontogenetic stage to form an undivided limb stem is uncertain. This results in uncertainties about the autapomorphies of the last common ancestor of Phosphatocopida especially about its appendage design. However, an ontogenetic change from a univalved to a bivalved head-shield has not been known from any phosphatocopid species yet and thus a univalved head-shield (a plesiomorphic state) seems to characterize the ground pattern of the Phosphatocopida. Most euphosphatocopids are known from later larval stages. A typical euphosphatocopid in later larval stages possesses antennulae, antennae and first post-mandibular limbs of the same design as they are in their head-larval stage, but the mandibles show ontogenetic changes. The mandibular limb stem in later larval stages is undivided, evidently derived from fusion of the coxa and the basipod. In some euphosphatocopids in earlier ontogenetic stages, the mandibular limb stem is undivided, but the endopod is seemingly three-divided, with a wedgeshaped structure inserted between the two-divided endopod and the underlying limb stem. This structure is interpreted as the remaining part of the basipod, the so-called basipodal endite. The occurrence of basipodal endite has been reported in many species, such as Hesslandona unisulcata Müller, 1982, H. suecica, Hesslandona ventrospinata Gründel in Gründel and Buchholz, 1981 and Vestrogothia spinata (Maas et al., 2003). The occurrence of basipodal endite implies that in even earlier stages that are unknown to us the mandibular limb stem is also two-divided, consisting of separate coxa and basipod. To summarize, the autapomorphies of Euphosphatocopida in later larval stages possibly include at least 1) an all-embracing bivalved shield with long and straight dorsal rim; 2) the endopods of the antennae and the mandibles two-divided; 3) the limb stem of the antennae undivided; and 4) the mandibular limb stem undivided. 7. Phylogenetic analysis of Crustacea sensu lato Hesslandona angustata and Vestrogothia spinata head-larvae from the Upper Cambrian at the Wangcun section provide detailed information about the earliest head-larval stage of these two species (Liu and Dong, 2009; Zhang et al., 2011; this paper). Combined with anatomical information of their later larval stages (Maas et al., 2003), their early ontogeny especially the development of their appendages can be reconstructed. These two species are representatives of two traditional sub-lineages of the Euphosphatocopida, i.e. Hesslandonina and Vestrogothiina. Combined with other ‘Orsten’-type stem-lineage crustaceans, we can explore the relationships of early crustaceans by means of phylogenetic systematics (Hennig, 1950). To shed light on the

early evolution of crustaceans, we carried out a computer-based cladistic analysis of the Crustacea sensu lato. The taxa selected for the phylogenetic analysis are listed as follow. Phosphatocopida. This taxon has been resolved as a monophyletic group and comprises 19 species (Maas et al., 2003). However, most are known mainly from their shields; their soft part anatomy is poorly known and contributes little to interspecific differentiation (Maas et al., 2003). In this analysis, the Phosphatocopida is represented by three species, Klausmuelleria salopensis from the Lower Cambrian of England (Siveter et al., 2003), H. angustata and Vestrogothia spinata from the Upper Cambrian of Sweden and South China (Maas et al., 2003; Liu and Dong, 2009; Zhang et al., 2011; this paper). Eucrustacea. Bredocaris admirabilis Müller and Walossek, 1988 is adopted as a representative of entomostracan eucrustaceans (Müller and Walossek, 1988), and the extant species Euphausia superba Dana, 1852 is adopted as a representative of malacostracan eucrustaceans (Maas and Waloszek, 2001). Other stem-lineage crustaceans. Seven species are included and they are Cambropachycope clarksoni Walossek and Müller, 1990, Goticaris longispinosa Walossek and Müller, 1990, Henningsmoenicaris scutula Walossek and Müller, 1990, Martinssonia elongata Müller and Walossek, 1986a, Musacaris gerdgeyeri Haug et al., 2010b, Oelandocaris oelandica Müller, 1983 and Sandtorpia vestrogothiensis Haug et al., 2010a (Müller and Walossek, 1986a; Walossek and Müller, 1990; Stein et al., 2005, 2008; Haug et al., 2009, 2010a,b). Another possible stem-lineage crustacean Cambrocaris baltica Walossek and Szaniawski, 1991 is poorly documented and is not included in this analysis (Walossek and Szaniawski, 1991). Type-C larva from the Upper Cambrian of Sweden (Müller and Walossek, 1986b) is characterized by the lack of a distinct labrum, a cephalon incorporating five limb-bearing segments and exopods of all the four post-antennular limbs multiannulated with medial setae, indicating a close relationship with Ma. elongata. However, it is not included either, because of its unclear appendage design. Siveter et al. (2007) described an arthropod, Tanazios dokeron, with 3-D soft part preservation from the Herefordshire (Silurian) Lagerstätte and considered it as a possible stem-lineage crustacean. T. dokeron possesses a set of chimeric characters. For example, its differentiated mandibles with coxae, telson with furcal rami, and the development of labrum and epipodite indicate a derived position within the Labrophora (Siveter et al., 2003) or Eucrustacea (Maas et al., 2009). However, other characters such as the undifferentiated antennae without coxae and the sub-terminally situated anus imply a more primitive position outside the Labrophora (Walossek and Müller, 1990). Importantly, its endopodal segment number and the design of its exopods are unclear. Due to these uncertainties, T. dokeron is not included in the present analysis, either. Out-groups. Three non-crustacean euarthropods – Agnostus pisiformis (Wahlenberg, 1818), Kunmingella douvillei (Mansuy, 1912) and Eoredlichia intermedia (Lu, 1940) – and a stem-lineage arthropod, Shankouia zhenghei Chen, Wang, Maas and Waloszek in Waloszek et al., 2005 were included as out-groups of Crustacea sensu lato. A. pisiformis was traditionally regarded as a trilobite but its soft part anatomy indicates that it is more closely related to the Crustacea (Müller and Walossek, 1987; Walossek and Müller, 1990). K. douvillei is regarded as an early off-shoot towards the origin of Crustacea (Hou et al., 1996; Shu et al., 1999; Hou et al., 2010).

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However, the detailed morphology of K. douvillei is not fully understood, especially the limb stem of its biramous limbs, the setae on the outer rim of the exopods of its cephalic biramous limbs, and its mouth opening and anus. We prefer to interpret this species as a euarthropod. This interpretation implies that the presence of a basipod and setae on the outer rim of the exopod of cephalic biramous limbs, since these features are characteristics of the euarthropod ground pattern (Waloszek et al., 2005, 2007). The proximal endite characterizes only the Crustacea and thus the occurrence of a proximal endite beneath the medio-proximal edge of the basipod of K. douvillei is not expected. E. intermedia is a euarthropod and the oldest trilobite whose appendages are well documented (Ramsköld and Edgecombe, 1996; Hou et al., 2009). S. zhenghei is recovered from the Lower Cambrian Chengjiang biota and is regarded as a stemlineage arthropod (Waloszek et al., 2005). The character list and data matrix are provided in the Appendix. Forty characters are included. These characters are independently selected, focusing on soft part morphologies, especially on the appendage design and its variation. The data matrix was analyzed using PAUP (Swofford, 2002) and a branch-and-bound algorithm resulted in 33 shortest trees (Tree Length = 142 steps; CI = 0.8169; RI = 0.7937; RC = 0.6483). These 33 shortest trees are more or less identical in topology but differ only in the topology of two lineages, (Musacaris gerdgeyeri+Martinssonia elongata+Labrophora) and (Oelandocaris oelandica + Sandtorpia vestrogothiensis + Henningsmoenicaris scutula) (Fig. 5A, B, C). The 50% majority rule tree is derived (Fig. 5D), and the support values (Bremer and Bootstrap support values) are given. On the basis of the 50% majority rule (Fig. 5D), the simplified phylogeny of the Crustacea sensu lato is presented (Fig. 6). Due to insufficient developmental information of S. vestrogothiensis and Mu. gerdgeyeri, two lineages were collapsed, resulting in two polytomies and preventing a unambiguous reconstruction of the autapomorphies within the two clades represented by Box 3 and Box 6 in Fig. 6. We also added two stemlineage crustaceans, Type-C larva sensu Müller and Walossek, 1986b and C. baltica, to the phylogenetic tree of Crustacea sensu lato; their possible systematic positions are denoted with dashed lines. Type-C larva is tentatively considered as the sister-taxon of Ma. elongata if Mu. gerdgeyeri retains a cephalon with four limb-bearing segments all through; alternatively, it could form a polytomy with Ma. elongata and Mu. gerdgeyeri if Mu. gerdgeyeri develops a cephalon incorporating the fifth segment in late larval stage. C. baltica is supposed to be the sistertaxon of Labrophora based on its greatly enlarged coxa-like proximal endite in antennae and mandibles, which is quite similar to the coxa of Labrophora. The present analysis is consistent with the result of Haug et al. (2010b) but it is more comprehensive because more characters and more taxa are included. In addition, the phylogenetic positions of two possible stem-lineage crustaceans, Type-C larva sensu Müller and Walossek, 1986b and C. baltica, are discussed. The Phosphatocopida and Eucrustacea are represented by five actual species rather than coded using the ground pattern character sets as in Haug et al. (2010a,b). Importantly, phosphatocopid head-larvae of ‘Orsten’-type preservation from Hunan are included. Furthermore, two euarthropod taxa, Eoredlichia intermedia (Trilobita) and Kunmingella douvillei (Bradoriida), are included, and this is useful for the discussion on the origin of crustaceans. Below is a summary of the autapomorphies of each node on the evolutionary path towards the crown-group Crustacea or Eucrustacea and comments on the phylogeny of Crustacea sensu lato (Fig. 6). 7.1. The position of Kunmingella douvillei Our analysis supports the proposed systematic position of Kunmingella douvillei as an early off-shoot on the evolutionary path towards the

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origin of crustaceans (Shu et al., 1999; Hou et al., 2010). K. douvillei looks like Agnostus pisiformis or some stem-lineage crustaceans in the morphology of the antennulae. Their antennulae are all short and strong, with only a few annuli, for locomotion and food-intake. And this design of antennulae differs from that of the trilobite Eoredlichia intermedia, of which the antennulae are long and thin with more annuli for sensory purpose. But the anterior appendages of K. douvillei are not specialized in size or in design, and this is different from those of A. pisiformis and crustaceans. Therefore, K. douvillei is resolved as a stemgroup to the monophyletic group (A. pisiformis + Crustacea sensu lato) in this analysis. This is the result of insufficient inclusion of other bradoriids and euarthropods and it does not imply that K. douvillei is the sistertaxon of (A. pisiformis + Crustacea sensu lato). Undoubtedly, the serially similarly designed post-antennular appendages of K. douvillei and the paddle-shaped exopods with setae fringed on the outer margin accord well with the ground pattern of Euarthropoda (Waloszek et al., 2005, 2007), and they thus represent plesiomorphic states. This is true for the same characters in the trilobite E. intermedia, all inherited from the ground pattern of Euarthropoda. Although K. douvillei has a cephalon incorporating five limb-bearing segments, our analysis shows that this feature evolved at least four times independently in non-labrophoran arthropods, including K. douvillei, Oelandocarididae, the possible monophyletic group of (Type-C larva sensu Müller and Walossek, 1986b + Martinssonia elongate + Musacaris gerdgeyeri), and C. baltica; thus this feature likely represents an evolutionary convergence. 7.2. The origin and evolution of early crustaceans Crustaceans originated with the specialization of the first three pairs of limbs, i.e. the exopods being multi-annulated with setae on the medial margin facing the endopods and the occurrence of a proximal endite only on the third pair of limbs and only in later larval stages (Box 2). The setae fringed on the second and third pairs of limbs are transferred from the outer margin in Agnostus pisiformis to the medial margin among crustaceans. The proximal endite is a key novelty belonging exclusively to crustaceans (Walossek and Müller, 1990). The occurrence and development of proximal endite (and its derivatives) among different lineages denote the evolution of crustaceans towards the crown-group. Five steps leading to the evolution of the crown-group crustaceans have been recognized, and these are: 1) the proximal endite occurred only on the third pairs of limbs and only in later larval stages (Box 2); 2) the proximal endite first occurred on the third pairs of limbs and later in ontogeny also on the second pairs of limbs (Box 4); 3) the proximal endite occurred on all the post-antennular limbs simultaneously during early ontogeny (Box 6); 4) the proximal endites on the antennae and mandibles were enlarged to form a separate coxa, indicating the homology of proximal endite and the coxa (Box 7); and 5) the proximal endites on the post-mandibular limbs are enlarged to form a coxa, but this occurs only among malacostracan eucrustaceans (Walossek and Müller, 1998a). The specialization of the several anterior pairs of limbs, i.e. exopod being multi-annulated with setae fringed on the medial margin, distinguishes crustaceans from other euarthropods. The three anteriormost pairs of limbs are specialized to form a ‘naupliar set’, different from the succeeding limbs, and this specialization characterizes the autapomorphies of the last common ancestor of the Crustacea sensu lato (Box 2). Along the evolutionary path towards the Eucrustacea, progressively more pairs of limbs are specialized, for example, three pairs at Box 2, four pairs at Box 4, five pairs at Box 6 and eight or more pairs at Box 7. The data from H. unisulcata indicates that at least the anterior five post-mandibular limbs are serially designed and they all look like the first post-mandibular limbs in design (Maas et al., 2003). Therefore at least eight pairs of limbs are specialized at Box 7. However, such specialized appendages decrease in number from at least eight (Box 7) to three (Box 8). At the ground pattern level of the Eucrustacea (Box 8), only the first three pairs of limbs are specialized in design. Taking Skara anulata Müller, 1983 as an example, although the

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maxillulae are specialized as a mouthpart, they are still trunk limbshaped and the exopods are still paddle-shaped with setae fringed on the outer margin (Müller and Walossek, 1985). 7.3. The monophyly of (Martinssonia elongata + Musacaris gerdgeyeri+ Labrophora) Martinssonia elongata, Mu. gerdgeyeri and the Labrophora are not resolved and are collapsed, mainly due to lack of soft part information of late ontogenetic stages of Mu. gerdgeyeri. Mu. gerdgeyeri was established on the basis of several early ontogenetic stages, all being head-larvae. It is uncertain whether the cephalon would incorporate the fifth segment in later ontogenetic stages, and in this paper its cephalon is regarded as a fusion product of only four limb-bearing segments. This affects the ground pattern reconstruction of Box 6 and Box 7, and there are three possibilities: 1) if Mu. gerdgeyeri is resolved as the sister-taxon of Labrophora (Fig. 5A), a cephalon incorporating five limb-bearing segments in Ma. elongata would be an evolutionary convergence shared with Oelandocarididae and Labrophora; 2) if Ma. elongata is resolved as the sister-taxon of Labrophora (Fig. 5B), a cephalon incorporating five limb-bearing segments becomes the synapomorphy of Ma. elongata and Labrophora, also being an evolutionary convergence with Oelandocarididae; and 3) if Ma. elongata and Mu. gerdgeyeri form a clade to the exclusion of the Labrophora (Fig. 5C), the cephalon incorporating five segments in Ma. elongata is still an evolutionary convergence as in Labrophora and Oelandocarididae. Anyway, due to the lack of developmental information of the cephalon of Mu. gerdgeyeri, we tentatively conclude that a cephalon incorporating four segments characterizes Box 6 and five for Box 7. Of course, our interpretations hinge on the uncertain status of the cephalon of Mu. gerdgeyeri. If Mu. gerdgeyeri is proved to possess a cephalon being the fusion product of five limb-bearing segments, then this five limb-bearing cephalon characterizes the ground pattern of Box 6. Type-C larva sensu Müller and Walossek, 1986b has a cephalon incorporating five limbbearing segments, and the four post-antennular limbs are all specialized with multi-annulated exopods bearing setae on the medial margins, resembling Ma. elongata. Therefore, Type-C larva may form the sistertaxon of Ma. elongata. But since the late larval stages of Mu. gerdgeyeri are unclear, Type-C larva may also be collapsed with Ma. elongata and Mu. gerdgeyeri if Mu. gerdgeyeri incorporates the fifth segment into its head in later ontogenetic stages to form a cephalon with five limb-bearing segments. Martinssonia elongata and Mu. gerdgeyeri are tentatively resolved as the closest relatives of Labrophora. However, this topology might be revised if the stem-lineage crustacean C. baltica was included. All the post-antennular limbs of C. baltica are developed with a proximal endite beneath the medio-proximal edge of the basipod, and the proximal endites of the second and third pairs of limbs of C. baltica are greatly enlarged to form a coxa-like structure. The enlarged coxa-like proximal endites indicate that C. baltica is closely related to the Labrophora. However, other characters, e.g. specialization of the five anterior pairs of limbs and occurrence of proximal endites on all post-antennular limbs, imply morphological similarities between C. baltica and Ma. elongata (Walossek and Szaniawski, 1991) although such similarities may represent plesiomorphic states. Due to the insufficient information especially of the cephalon and appendage design, the sister-taxon relationship between C. baltica and the Labrophora cannot be tested at the present. 7.4. The sister-taxon relationship of Phosphatocopida and Eucrustacea The Phosphatocopida is resolved as the sister-taxon of the Eucrustacea on the basis of many shared apomorphies (Box 7), and this is consistent with results from previous studies (Maas et al., 2003; Siveter et al., 2003; Waloszek, 2003). With regard to the relationships within the Phosphatocopida, many previous studies have given detailed discussion (Maas et al., 2003; Zhang et al., 2011), and it is not the aim of

this paper. The traditional Eucrustacea is proposed to be a monophyletic group consisting of two sub-lineages, the Entomostraca and the Malacostraca (Waloszek, 2003), but this is challenged by recent molecular studies supporting that the Hexapoda originated within eucrustaceans and the traditional “Crustacea” is a paraphyletic group (Regier et al., 2005, 2010; Andrew, 2011; Strausfeld and Andrew, 2011). A detailed discussion on this phylogenetic hypothesis is evidently beyond the scope of this paper and we here restrict our discussion to the traditional monophyletic Crustacea. 7.5. Number of endopodal podomeres This analysis also shows that the podomere number of endopods may not be an appropriate character for the phylogenetic reconstruction of the Crustacea sensu lato or Arthropoda. Shu et al. (1999) proposed that the endopods of Kunmingella douvillei possessed five podomeres that match the ground pattern of Crustacea sensu lato. Our analysis shows that it is somewhat subjective to judge the affinity of an arthropod on the basis of its endopodal podomere number. The endopods of K. douvillei are supposed to have five podomeres, those of Eoredlichia intermedia all have seven podomeres, those of Agnostus pisiformis have six or seven podomeres, and endopods of some stem-lineage crustaceans have even fewer podomeres. An endopod consisting of no more than five podomeres was previously regarded as the autapomorphy of the last common ancestor of Crustacea sensu lato and all endopods of crustaceans are supposed to possess no more than five podomeres (Waloszek, 2003). However, according to the re-study by Haug et al. (2010b), the endopods of Ma. elongata probably have six or seven podomeres. In addition, Zhang et al. (2007, fig. 1i and j) illustrated a post-maxillulary appendage with seven podomeres in Yicaris dianensis Zhang et al., 2007, a Lower Cambrian entomostracan eucrustacean. Therefore, an endopod with more than 5 podomeres originated many times within the Euarthropoda and especially within the Crustacea sensu lato, indicating that the original hypothesis of an endopod with (at most) five podomeres as an autapomorphy of the Crustacea sensu lato (Walossek, 1999; Maas et al., 2003; Waloszek, 2003) needs to be reconsidered. 8. Conclusions We described three head-larvae of H. angustata of ‘Orsten’-type preservation from the Upper Cambrian of Wangcun section in Yongshun County, western Hunan, South China. They possess four pairs of functional limbs at the head-larval stage, and the fifth pair would develop in later larval stages to form a typical labrophoran cephalon (a fusion product of five limb-bearing segments). The antennulae are short and thin, weak in segmentation and setation. The antennae consist of an un-divided limb stem (with separate coxa and basipod), a twodivided endopod and a multi-annulated exopod with setae on the medial margin. The mandibles consist of a two-divided limb stem (with separate coxa and basipod), a two-divided endopod and a multiannulated exopod with setae on the medial margin. The first postmandibular limbs consist of a proximal endite, a basipod, an endopod and a multi-annulated exopod. A comparison with the head-larvae of Vestrogothia spinata from the same locality and horizon indicates that these head-larvae are identical in terms of appendage design. And a comparison with phosphatocopids of later larval stages indicates that the mandibular limb stem of H. angustata and V. spinata transitioned ontogenetically from two-divided to un-divided with the coxa and basipod being fused in later larval stages, and this condition possibly characterizes the Euphosphatocopida. To shed light on the relationships of stem-lineage crustaceans, we carried out a computer-based phylogenetic analysis of the Crustacea sensu lato. On the basis of this analysis, we reconstructed the phylogeny of the Crustacea sensu lato and enumerated the autapomorphies of each node along the phylogenetic tree. The analysis indicates that the origin of crustaceans is characterized by the

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occurrence of proximal endite only on the third pair of limbs and only in later larval stages, together with the specialization of the exopods on the second and third pairs of limbs. The occurrence and development of the proximal endite (and its derivatives) can be used to explore the evolution of crustaceans. The evolution of the proximal endite along the evolutionary path from the origin of crustaceans to crown-group crustaceans can be summarized as five steps. These steps are 1) the proximal endite occurred only on the third pair of limbs and only in later larval stages; 2) the proximal endite occurred on the third pair of limbs early in ontogeny and also on the second pair of limbs in later ontogeny; 3) the proximal endite occurred on all post-antennular limbs simultaneously in early ontogeny; 4) the proximal endites on the second and third pairs of limbs were enlarged to form a coxa inserting beneath the basipod; and 5) the proximal endites on post-mandibular limbs are enlarged to form separate coxa but only in the Malacostraca (Walossek and Müller, 1998a). Type-C larva sensu Müller and Walossek, 1986b is possibly a close relative of Ma. elongata and Mu. gerdgeyeri, whereas C. baltica may be the closest relative of Labrophora. Finally, our analysis indicates that the endopodal podomere number is not an appropriate criterion in phylogenetic analysis of the Arthropoda, because endopod with N5 podomeres evolved several times independently in the Arthropoda and especially in the Crustacea. Acknowledgements This work was supported by the National Natural Science Foundation of China (Grants 41072006 and 40772008 to XPD), the Research Fund for Doctoral Program of High Education (Grant 20060001059 to XPD), State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences (Grant 103102 to XPD), and China Postdoctoral Science Foundation (Grant 20100480103 to HZ). We thank Wei Guo for field assistance, Andreas Maas for his invaluable suggestions and Dieter Waloszek for communication. Bruce S. Lieberman, Pat Eriksson and an anonymous reviewer provided constructive comments on the manuscript. Appendix I. Character list Forty characters are selected for analysis, mainly including soft part morphology in addition to some shield characters. Shield: 1. shield type: univalved (0), bivalved (1); 2. dorsal hinge structure: not developed (0), a dorsal furrow (1), an interdorsum (2); Body proper: 3. in addition to the ocular segment, the cephalon (or cephalothorax) incorporates: 1 segment (0), 4 segments (1), 5 segments (2), 6 to 12 segments (3), 13 segments (4); 4. hypostome/labrum complex: hypostome only (0), labrum developed (1); 5. compound eyes type: two lateral compound eyes (0), a single compound eye inserted anterior to the head (1), compound eyes secondarily lost (2); 6. position of the mouth opening: on the rear of the hypostome (0), ventrally on the hypostome (1), covered by the labrum (2); 7. anterior sternites fused to form a single sternum: no (0), yes (1); 8. paragnath on the mandibular sternite: not developed (0), developed (1); 9. fine hairs on the structures around the mouth opening: no (0), yes (1);

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Tail end: 10. tail end: conical or spine-like pieces with lateral flaps (0), spinose or plated non-metameric piece, possibly with marginal setae (1), telson with articulated uropods forming a tail fan (2); 11. anus position: sub-terminal (0), terminal (1); General morphology of the appendages: 12. the anterior (at least three) pairs of appendages: non-specialized, identical in size and basic design as the following pairs (0), different a little, either in size of the exopods and endopods or in basic design as in crustaceans (1); The antennulae (first antennae): 13. the antennulae: strong with only a few annuli (0), long and thin, with more annuli (1), much reduced in size, setation and segmentation (2); 14. setae positioned: without setae (0), mainly anteriorly (1), mainly medially (2), mainly posteriorly (3); The second appendages (antennae): 15. limb stem in first stage: a multi-segmented main stem (0), a basipod (1), a proximal endite + a basipod (2), a coxa+ a basipod (3), fusion product of coxa and basipod (4); 16. limb stem in later stages: a multi-segmented main stem (0), a basipod (1), a proximal endite + a basipod (2), a coxa+ a basipod (3), fusion product of coxa and basipod (4); 17. exopod design: flap-shaped without setae (0), paddle-shaped with setae on the outer margin (1), multi-annulated with setae on the outer and distal margin (2), multi-annulated with setae on the inner margin (3), an undivided, flat exopod, the scaphocerite (4); 18. in earlier larval stages, exopod with three setae on the terminal article and two on the sub-terminal article: no (0), yes (1); 19. segments of endopod: N7 (0), 7 (1), 6 (2), 5 (3), 4 (4), 3 (5), 2 (6), 1 (7), 0 (8); The third appendages (mandibles): 20. limb stem in first stage: a multi-segmented main stem (0), a basipod (1), a proximal endite + a basipod (2), a coxa+ a basipod (3), fusion product of coxa and basipod (4), basipod secondarily lost, a coxa only (5); 21. limb stem in later stages: a multi-segmented main stem (0), a basipod (1), a proximal endite+ a basipod (2), a coxa+ a basipod (3), fusion product of coxa and basipod (4), basipod secondarily lost, a coxa only (5); 22. exopod design: flap-shaped without setae (0), paddle-shaped with setae on the outer margin (1), multi-annulated with setae on the outer and distal margin (2), multi-annulated with setae on the inner margin (3), exopod absent (4); 23. in earlier larval stages, exopod with three setae on the terminal article and two on the sub-terminal article: no (0), yes (1); 24. segments of endopod: N7 (0), 7 (1), 6 (2), 5 (3), 4 (4), 3 (5), 2 (6), 1 (7), 0 (8); The fourth appendages (maxillulae): 25. specialized as maxillulae: no (0), yes (1); 26. limb stem in first stage: a multi-segmented main stem (0), a basipod (1), a proximal endite + a basipod (2), a coxa + a basipod (3), fusion product of coxa and basipod (4); 27. limb stem in later stages: a multi-segmented main stem (0), a basipod (1), a proximal endite + a basipod (2), a coxa + a basipod (3), fusion product of coxa and basipod (4); 28. exopod design: paddle-shaped, one article, without setae (0), paddle-shaped, one article, with setae on the outer margin (1), paddle-shaped, two articles, basal part joining to the endopod portion, with setae on the outer margin (2), multi-annulated

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with setae on the outer and distal margin (3), multi-annulated with setae on the inner margin (4), exopod largely reduced or totally absent (uniramous) (5); 29. segments of endopod: N7 (0), 7 (1), 6 (2), 5 (3), 4 (4), 3 (5), 2 (6), 1 (7), 0 (8); The fifth appendages (maxillae): 30. specialized as maxillae: no (0), yes (1); 31. limb stem in first stage: a multi-segmented main stem (0), a basipod (1), a proximal endite + a basipod (2), a coxa + a basipod (3), fusion product of coxa and basipod (4); 32. limb stem in later stages: a multi-segmented main stem (0), a basipod (1), a proximal endite + a basipod (2), a coxa + a basipod (3), fusion product of coxa and basipod (4); 33. exopod design: paddle-shaped, one article, without setae (0), paddle-shaped, one article, with setae on the outer margin (1), paddle-shaped, two articles, basal part joining to the endopod portion, with setae on the outer margin (2), multi-annulated with setae on the outer and distal margin (3), multi-annulated with setae on the inner margin (4), exopod largely reduced or totally absent (uniramous) (5); 34. segments of endopod: more than 7 (0), 7 (1), 6 (2), 5 (3), 4 (4), 3 (5), 2 (6), 1 (7), 0 (8); The sixth appendages (first thoracopods): 35. specialized as a maxilliped: no (0), yes (1); 36. limb stem in first stage: a multi-segmented main stem (0), a basipod (1), a proximal endite + a basipod (2), a coxa + a basipod (3), fusion product of coxa and basipod (4); 37. limb stem in later stages: a multi-segmented main stem (0), a basipod (1), a proximal endite + a basipod (2), a coxa + a basipod (3), fusion product of coxa and basipod (4); 38. exopod design: paddle-shaped, one article, without setae (0), paddle-shaped, one article, with setae on the outer margin (1), paddle-shaped, two articles, basal part joining to the endopod portion, with setae on the outer margin (2), multi-annulated with setae on the outer and distal margin (3), multi-annulated with setae on the inner margin (4), exopod largely reduced or totally absent (uniramous) (5); 39. segments of endopod: more than 7 (0), 7 (1), 6 (2), 5 (3), 4 (4), 3 (5), 2 (6), 1 (7), 0 (8); Larval type: 40. first larval type: a possibly very primitive larva (longer compared with head-larva) (0), head-larva (1), nauplius (2), metanauplius (3), a more advanced type (4). II. Data matrix

Taxon Agnostus pisiformis Bredocaris admirabilis Cambropachycope clarksoni Eoredlichia intermedia Euphausia superba Goticaris longispinosa Henningsmoenicaris scutula Hesslandona angustata Klausmuelleria salopensis Kunmingella douvillei Martinssonia elongata Musacaris gerdgeyeri Oelandocaris oelandica Sandtorpia vestrogothiensis Shankouia zhenghei Vestrogothia spinata

Character state 0010?0000??10211208112020113201131011311 0021?21112110333305333041225402214022143 001011000101032230322303011430115?0115?1 001000000??01011101111010111101111011111 0041021112112234408354081335713317033132 001011000101031230322303011430115?0115?1 0020000001010112316123160122401224012261 122122111??12044306343060224502245022451 00?122111??1203?3053?30502?450????0????1 1120?0000??0021110311103011130111301113? 00202000010102223032230302243022430221?1 00?020000101022230?2230?0224?0????0????1 0020200001010111314123140112501125011251 002020000101011?3151?31501?2?0?????????? 0000000000000000000000000000000000000000 112122111??12044306343060224502245022451

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