The appendicular morphology of Sinoburius lunaris and the evolution of the artiopodan clade Xandarellida (Euarthropoda, early Cambrian) from South China

Abstract

Background: Artiopodan euarthropods represent common and abundant faunal components in sites with exceptional preservation during the Cambrian. The Chengjiang biota in South China contains numerous taxa that are exclusively known from this deposit, and thus offer a unique perspective on euarthropod diversity during the early Cambrian. One such endemic taxon is the non-trilobite artiopodan Sinoburius lunaris, which has been known for approximately three decades, but few details of its anatomy are well understood due to its rarity within the Chengjiang, as well as technical limitations for the study of these fossils. Furthermore, the available material does not provide clear information on the ventral organization of this animal, obscuring our understanding of phylogenetically significant details such as the appendages.

Results: We employed X-ray computed tomography to study the non-biomineralized morphology of Sinoburius lunaris. Due to the replacement of the delicate anatomy with pyrite typical of Chengjiang fossils, computed tomography reveals substantial details of the ventral anatomy of Sinoburius lunaris, and allow us to observe in detail the three-dimensionally preserved appendicular organization of this taxon for the first time. The dorsal exoskeleton consists of a crescent-shaped head shield with well-developed genal spines, a thorax with seven freely articulating tergites, and a fused pygidium with lateral and median spines. The head bears a pair of ventral stalked eyes that are accommodated by dorsal exoskeletal bulges, and an oval elongate ventral hypostome. The appendicular organization of the head is unique among Artiopoda. The deutocerebral antennae are reduced, consisting of only five podomeres, and bear an antennal scale on the second podomere that most likely represents an exite rather than a true ramus. The head includes four post-antennal biramous limb pairs. The first two biramous appendages are differentiated from the rest. The first appendage pair consists of a greatly reduced endopod coupled with a greatly elongated exopod with a potentially sensorial function. The second appendage pair carries a more conventionally sized endopod, but also has an enlarged exopod. The remaining biramous appendages are homonomous in their construction, but decrease in size towards the posterior end of the body. They consist of a basipodite with ridge-like crescentic endites, an endopod with seven podomeres and a terminal claw, and a lamellae-bearing exopod with a slender shaft. Contrary to previous reports, we confirm the presence of segmental mismatch in Sinoburius lunaris, expressed as diplotergites in the thorax. Maximum parsimony and Bayesian phylogenetic analyses support the monophyly of Xandarellida within Artiopoda, and illuminate the internal relationships within this enigmatic clade. Our results allow us to propose a transformation series explaining the origin of archetypical xandarellid characters, such as the evolution of eye slits in Xandarella spectaculum and Phytophilaspis pergamena as derivates from the anterolateral notches in the head shield observed in Cindarella eucalla and Luohuilinella species. In this context, Sinoburius lunaris is found to feature several derived characters within the group, such as the secondary loss of eye slits and a high degree of appendicular tagmosis. Contrary to previous findings, our analyses strongly support close affinities between Sinoburius lunaris, Xandarella spectaculum and Phytophilaspis pergamena, although the precise relationships between these taxa are sensitive to different methodologies.

Conclusions: The revised morphology of Sinoburius lunaris, made possible through the use of computed tomography to resolve details of its three-dimensionally preserved appendicular anatomy, contributes towards an improved understanding of the morphology of this taxon and the evolution of Xandarellida more broadly. Our results indicate that Sinoburius lunaris possesses an unprecedented degree of appendicular tagmosis otherwise unknown within Artiopoda, with the implication that this iconic group of Palaeozoic euarthropods likely had a more complex ecology and functional morphology than previously considered. The application of computer tomographic techniques to the study of Chengjiang euarthropods holds exceptional promise for understanding the morphological diversity of these organisms, and also better reconstructing their phylogenetic relationships and evolutionary history.

Keywords: Antennal scale; Computed tomography; Dorsoventral segmental mismatch; Euarthropoda; Exceptional preservation; Konservat-Lagerstätte; Pyritization; Tagmosis.

Fig. 1

The non-biomineralized artiopodan Sinoburius lunaris from the early Cambrian (Stage 3) Chengjiang. a YKLP 11407, dorsal view of specimen photographed under light microscopy. b Dorsal view of specimen photographed under fluorescence microscopy. c Dorsal view of three-dimensional computer model based on X-ray tomographic data rendered in Drishti [73]. d Ventral view of three-dimensional model based on X-ray tomographic data. Abbreviations: en, endopod; ex, exopod; gs, genal spine; hs, head shield; ls, lateral spine; ms, median spine; pg, pygidium; Tn, thoracic segment

Fig. 2

Detailed ventral morphology of Sinoburius lunaris, specimen YKLP 11407. a Specimen photographed under light microscopy. b Ventral view of three-dimensional computer model based on X-ray tomographic data rendered in Drishti [73] showing details of the well-preserved appendages concealed by the rock matrix. Abbreviations: ans, antennal scale; ant, antennae; en, endopod; ex, exopod; hs, head shield; hyp, hypostome; ls, lateral spine; ms, median spine; pg, pygidium; stn, sternite; tc, terminal claw; Tn, thoracic segment

Fig. 3

Cephalic and limb morphology of Sinoburius lunaris, specimen YKLP 11407. a Three-dimensional computer model of ventral view of anterior cephalic region based on X-ray tomographic data rendered in Drishti [73]. Arrowheads indicate podomere boundaries in antennae. b Three-dimensional computer model of virtually dissected ninth biramous appendage from right side of body. Abbreviations: ans, antennal scale; ant, antennae; ed., endite; en, endopod; ex, exopod; hyp, hypostome

Fig. 4

The non-biomineralized artiopodan Sinoburius lunaris from the early Cambrian (Stage 3) Chengjiang. a YRCP 0011, dorsal view of specimen photographed under light microscopy. b Dorsal view of specimen photographed under fluorescence microscopy. c Ventral view of three-dimensional computer model based on X-ray tomographic data rendered in Drishti [73]. d Close up of head region in ventral view. e Close-up of uniramous antennae with antennal scale. Arrowheads indicate podomere boundaries in antennae. Abbreviations: ans, antennal scale; ant, antennae; en, endopod; ex, exopod; ey, eye; gs, genal spine; gn, gnathobases; hs, head shield; hyp, hypostome; ls, lateral spine; ms, median spine; pg, pygidium; Tn, thoracic segment

Fig. 5

Morphology of biramous appendages in Sinoburius lunaris (YRCP 0011). a Third post-antennal limb pair. b Fourth post-antennal limb pair. Abbreviations: ba, basipodite; en, endopod; ex, exopod; lam, lamellae; pdn, podomere

Fig. 6

The non-biomineralized artiopodan Sinoburius lunaris from the early Cambrian (Stage 3) Chengjiang. a Hz-f-10-45, dorsal view of specimen photographed under light microscopy. b Dorsal view of specimen photographed under fluorescence microscopy. c Dorsal view of three-dimensional computer model based on X-ray tomographic data rendered in Drishti [73]. Abbreviations: ant, antennae; en, endopod; ex, exopod; ey, eye; gs, genal spine; ls, lateral spine; ms, median spine; pg, pygidium; Tn, thoracic segment

Fig. 7

Morphological reconstruction of Sinoburius lunaris based on specimen YKLP 11407. Sternites associated with diplotergites highlighted. Abbreviations: ans, antennal scale; ant, antennae; ed., endite; en, endopod; ex, exopod; ey, eye; gs, genal spine; hyp, hypostome; lam, lamellae; ls, lateral spine; ms, median spine; pdn, podomere; pg, pygidium; stn, sternite; tc, terminal claw; Tn, thoracic segment

Fig. 8

Evolution of anterolateral notches, eye slits and dorsal exoskeletal bulges in the head shield of Xandarellida. Xandarella mauretanica [27] is excluded since the dorsal exoskeleton is unknown

Fig. 9

Phylogeny of Xandarellida (highlighted) within Artiopoda. a Maximum parsimony with implied weights (k = 4), strict consensus of 2 most parsimonious trees (CI = 0.412, RI = 0.737); node support values expressed as Group present/Contradicted frequency differences. b Maximum parsimony with implied weights (k = 5), strict consensus of 2 most parsimonious trees (CI = 0.413, RI = 0.739); node support values expressed as Group present/Contradicted frequency differences. c Consensus tree resulting from Bayesian analysis in MrBayes. Mk model, four chains, 1000,000 generations, 1/1000 sampling resulting in 5000 samples, 25% burn-in resulting in 3750 samples retained. Numbering denotes node posterior probability values. Internal topologies of Vicissicaudata and Aglaspidida same as those reported by Du et al. [30]

Fig. 10

Morphological evolution of Xandarellida derived from results of phylogenetic analyses and proposed model for cephalic evolution. Note that other character optimization options are plausible, but result in either an equal or greater number of character transformations. a Topology based on maximum parsimony with implied weights (see Fig. 9a, b). b Topology based on Bayesian inference (see Fig. 9c). Abbreviations: diff. ex., differentiated exopod; red. Reduced