Homologous Shell Microstructures in Cambrian Hyoliths And

HOMOLOGOUS SHELL MICROSTRUCTURES IN CAMBRIAN HYOLITHS AND MOLLUSCS by LUOYANG LI1,2, XINGLIANG ZHANG1*, CHRISTIAN B. SKOVSTED1,2*, HAO YUN1, BING PAN2,3 and GUOXIANG LI3 1State Key Laboratory of the Continental Dynamics, Shaanxi Key Laboratory of Early Life and Environments, Department of Geology, Northwest University, Xi’an 710069, PR China; e-mail: [email protected], [email protected] 2Department of Palaeobiology, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden; [email protected], [email protected] 3State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, PR China. [email protected], [email protected] *Corresponding authors Abstract: Hyoliths were one of the earliest biomineralizing metazoans in Paleozoic marine environments. They have been known for two centuries and widely assigned to lophotrochozoans. However, their origin and relationships with modern lophotrochozoan clades have been a longstanding paleontological controversy. Here, we provide broad microstructural data from hyolith conchs and opercula from the lower Cambrian Xinji Formation of North China, including two hyolithid genera and four orthothecid genera as well as unidentified opercula. Results show that most hyolith conchs contain a distinct aragonitic lamellar layer that is composed of foliated aragonite except in the orthothecid Protomicrocornus which has a crossed foliated lamellar microstructure. Opercula are mostly composed of foliated aragonite and occasionally foliated calcite. These blade or lath-like microstructural fabrics coincide well with biomineralization of Cambrian molluscs rather than lophophorates, as exemplified by the Cambrian members of the tommotiid-brachiopod linage. Accordingly, we propose that hyoliths and molluscs might have inherited their biomineralized skeletons from a non-mineralized or weakly mineralized common ancestor rather than as a result of parallel evolution or convergence. Consequently, from the view of biomineralization, the homologous shell microstructures in Cambrian hyoliths and molluscs strongly strengthen the phylogenetic links between the two groups. Key words: hyoliths, lophotrochozoan, biomineralization, Cambrian, North China. IN recent years, research on the origin and key transitions in the evolution of major lophotrochozoan clades (annelids, molluscs, “lophophorates”) have advanced remarkably in the light of numerous discoveries of crucial stem-group fossils in the Cambrian (Conway Morris & Caron 2007; Zhang et al. 2014b) and new molecular phylogenetic investigations (Kocot 2016). In many areas, consensus has been reached, for example regarding the placement of Myzostomida, Echiura and Sipuncula in the Annelida (Dunn et al. 2008); the divisions of the Mollusca into two subgroups: Conchifera and Aculifera (Kocot et al. 2011; Smith et al. 2011); the derivation of organophosphatic brachiopods (Linguliformea) from a direct ancestor within tommotiids (Balthasar et al. 2009), etc. However, our current understanding especially surrounding the roots of the lophotrochozoans is far from complete, and a well-accepted tree of basal lophotrochozoan clades has not yet been established. Intensive palaeontological studies have been focused on some controversial fossils in the Cambrian including halwaxiids (halkieriids and wiwaxiids) (Conway Morris & Caron 2007; Zhang et al. 2015), tommotiids (Skovsted et al. 2015) and hyoliths (Malinky & Yochelson 2007), which are conspicuous constituents of Cambrian marine communities and crucial breakthrough points for understanding the origin and radiation of lophotrochozoan animals during the Cambrian explosion. Hyoliths were one of the earliest biomineralizing metazoans in Paleozoic marine environments (existing from the beginning of the Cambrian to end Permian), with two orders recognized (the Orthothecida and the Hyolithida) (Malinky & Yochelson 2007). They produced a calcareous exoskeleton that consists of up to three parts: a conical conch, a lid-like operculum, and at least in the Hyolithida, an additional pair of elongate lateral spines or “helens” protruding from the commissure between the conch and operculum (Martí Mus et al. 2014). Although hyoliths have been known for two centuries, and their affiliation with lophotrochozoans seems to be a widely accepted assumption, the precise phylogenetic position within the lophotrochozoan clade is still a subject of debate. Traditionally, they have most often been regarded as an extinct class within the Mollusca, mainly based on the presence of crossed lamellar microstructure in some younger taxa, or a type of aragonitic microstructural fabric only known from the Mollusca (Malinky & Yochelson 2007; Carter 1990). Alternatively, they have been assigned to sipunculan worms (Sun et al. 2016) or to constitute their own phylum (Runnegar et al. 1975; Runnegar 1980). The quintessence of the debate is whether the crossed lamellar microstructure is homologous or convergent between hyoliths and molluscs, which has been hard to assess (Malinky & Yochelson 2007). More recently, new discovery of soft-tissues from Cambrian Burgess Shale-type Lagerstätten (Moysiuk et al. 2017) and the Chengjiang Biota (Liu et al. unpublished data) revealed a tentaculate feeding structure and a distinct U-shaped gut, which suggest that they are closely related to the “lophophorates”, which include modern brachiopods, phoronids, and probably bryozoans (Dunn et al. 2014) as well as some fossil taxa such as tommotiids (Skovsted et al. 2008) and tentaculitoids (Vinn & Zatoń 2012). Early lophotrochozoan biomineralizers (including hyoliths, molluscs, brachiopods and tommotiids) acquired the capacity to produce mineralized external shells from their soft- bodied ancestors during the early Cambrian and exert exquisite controls over biomineralization (Murdock & Donoghue 2011; Kouchinsky et al. 2012). They generated a variety of biominerals, mainly calcium carbonate polymorphs and calcium phosphate mineral complex. The crystals, intercalated between macromolecules and secreted by the underlying tissues (the mantle), are used to construct an incredible diversity of shell patterns and macro- micro architectures (Carter 1990). Despite the fact that the phylogenetic significance of biomineralization in lophotrochozoans remains contentious, the most closely related groups generally share skeletal homologies and high morphological similarities, but each linage has evolved a distinctive array of characterization of their own in mineralogical composition, microstructural fabrics and crystallographic orientations, etc. For instance, nacre (“mother of pearl”), one of the most common types of shell microstructures known in molluscs, is generally composed of crystallites of aragonite arranged in a sheet or brick-wall appearance in bivalves (Cartwright et al. 2009), and a tower pattern in gastropods and cephalopods (Checa et al. 2009a). From this perspective, we expect that biomineralization can provide additional information towards a better resolution of deep lophotrochozoan phylogeny in general and that detailed shell microstructural investigations may shed new light on relationships between hyoliths and other lophotrochozoans, particularly with molluscs and “lophophorates”. Here, we provide new microstructural data of hyolith conchs and opercula based on abundant and exceptionally well-preserved specimens from the lower Cambrian Xinji Formation of North China, which can be assigned to two hyolithid genera (Microcornus Mambetov, 1972 and Parakorilithes He & Pei in He et al., 1984), four orthothecid genera (Allatheca Missarzhevsky in Rozanov et al., 1969, Conotheca Missarzhevsky in Rozanov et al., 1969, Cupitheca Duan in Xing et al., 1984, and Protomicrocornus Pan et al., unpublished data), as well as unidentified opercula. Our study shows that hyoliths are extremely similar to Cambrian molluscs in terms of their distinct lamellar shell microstructures that are composed of blade- or lath-like crystallites of either aragonite or calcite. GEOLOGICAL SETTING The North China Block is bounded to the north by the Central Asian Orogenic Belt, to the south by the Qinling-Dabie Belt and Su-Lu fault against the South China Block, to the west by the Qilian Orogenic Belt against the Tarim Block (Stern et al. 2018). During the early Cambrian, the North China Block was situated near the northern margin of the Gondwana supercontinent, particularly close to the Australia Block (Brock et al. 2000; Yun et al. 2016). The lithological sequences and sedimentary patterns from the Ediacaran to lower Cambrian are consistent and can be precisely correlated along the southern margin of North China, with sequences in ascending order: Luoquan Formation, Dongpo Formation, Xinji Formation and Zhushadong Formation. They are generally in conformable contact except a distinct disconformity at the base of the Cambrian, with strata of the Terreneuvian being absent anywhere. The Xinji Formation is the oldest record of Cambrian deposits, ranging stratigraphically in the upper part of Stage 3 or lower part of Stage 4 of the Cambrian System (Fig. 1A, B). The Xinji Formation consists of siliciclastic rocks intercalated with carbonates, which rests disconformably on the upper Ediacaran Dongpo Shale and is conformably overlain by the massive dolostones of the Zhushadong Formation in studied areas. The carbonate unit of the Xinji Formation yields an abundant, diverse assemblage of so-called

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