The oldest known priapulid‐like scalidophoran animal and its implications for the early evolution of cycloneuralians and ecdysozoans

Abstract

Morphological phylogenetic analyses suggest that scalidophorans (priapulids, loriciferans, and kinorhynchs) and nematoids (nematodes and nematomorphs) form the ecdysozoan clade Cycloneuralia, which is a sister group to panarthropods. It has been proposed that extant priapulids and Cambrian priapulid-like scalidophorans, because of their conserved evolution, have the potential to illuminate the ancestral morphology, ecology, and developmental biology of highly derived ecdysozoans such as nematods and arthropods. As such, Cambrian fossils, particularly Markuelia and possibly olivooids, can inform the early evolution of scalidophorans, cycloneuralians, and ecdysozoans. However, the scalidophoran Markuelia is known exclusively as embryo fossils, and the olivooids have been alternatively interpreted as cnidarians or cycloneuralians. Here, we describe a post-embryonic scalidophoran fossil Eopriapulites sphinx new genus and species, which represents the oldest known scalidophoran, from the early Cambrian Period (∼535 Ma) in South China. E. sphinx is similar to modern scalidophorans in having an introvert armed with hollow scalids, a collar with coronal scalids, and a pharynx with pharyngeal teeth, but its scalids and pharyngeal teeth are arranged in a hexaradial pattern. Phylogenetically resolved as a stem-group scalidophoran, E. sphinx shares a hexaradial pattern with the hexaradial arrangement of certain anatomical structures in kinorhynchs, loriciferans, nematoids, and Cambrian fossils such as Eolympia pediculata, which could also be a scalidophoran. Thus, the bodyplan of ancestral cycloneuralians may have had a component of hexaradial symmetry (i.e., some but not necessarily all anatomical parts are hexaradially arranged). If panarthropods are nested within paraphyletic cycloneuralians, as several molecular phylogenetic analyses suggest, the ancestral ecdysozoans may have been a legless worm possibly with a component of hexaradial symmetry.

New material of the oldest known scalidophoran animal Eopriapulites sphinx

“…1). For detailed geological background of Zhangjiagou section, please refer to Li (1984), Liu et al (2014b) and Steiner et al (2014). Zhangjiagou section was first measured and described by Li (1984), and later studied as Hexi section by Steiner et al (2007Steiner et al ( , 2014, and as Xixiang section by Liu et al (2014a, b).…”

“…As cuticle-bearing animals, cycloneuralians have a strong fossilization potential and left abundant fossils in the Cambrian rocks (Maas, 2013). The markers of the Precambrian-Cambrian boundary are some subhorizontal segmented burrow systems possibly caused by some early cycloneuralians (Vannier et al, 2010), but cycloneuralian body fossils first occurred in the Cambrian Fortunian small shelly faunas (~535 Ma) of South China (Liu et al, 2014b). Generally, the Cambrian cycloneuralians were preserved mainly either as centimeter-sized flattened forms in the Burgess Shale-type preservation (Conway Morris, 1977;Briggs et al, 1994;Chen, 2004;Hou et al, 2004;Conway Morris and Peel, 2010;Peel, 2010;Erwin and Valentine, 2013), or as millimeter-sized three dimensional forms in the Orsten-type preservation (Bentson and Yue, 1997;Dong et al, 2004Dong et al, , 2005aDong et al, , 2010Maas et al, 2007bMaas et al, , 2009Zhang, X.G.…”

“…Generally, the Cambrian cycloneuralians were preserved mainly either as centimeter-sized flattened forms in the Burgess Shale-type preservation (Conway Morris, 1977;Briggs et al, 1994;Chen, 2004;Hou et al, 2004;Conway Morris and Peel, 2010;Peel, 2010;Erwin and Valentine, 2013), or as millimeter-sized three dimensional forms in the Orsten-type preservation (Bentson and Yue, 1997;Dong et al, 2004Dong et al, , 2005aDong et al, , 2010Maas et al, 2007bMaas et al, , 2009Zhang, X.G. et al, 2011;Liu et al, 2014b), with some minor reports as small carbonaceous fossils (Smith et al, 2015). They have comparatively great individual abundance (Conway Morris, 1979;Zhao et al, 2014) and played an important role in the Cambrian ecosystems (Maas, 2013).…”

“…But due to the size limit of Orsten-type preservation (Maas et al, 2006), only specimens no larger than 2 mm can be preserved, whereas larger animals exemplified by palaeoscolecids (Müller and Hinz-Schallreuter, 1993;Duan et al, 2012) are only known by fragments. Liu and Xiao in Liu, Xiao, Shao, Broce, and Zhang, 2014b is the oldest known scalidophoran worm and so far the only cycloneuralian animal reported from the Cambrian Fortunian Stage (Liu et al, 2014b). The holotype and only specimen is a fragment with the proboscis and only the anterior trunk part preserved (Liu et al, 2014b).…”

“…Liu and Xiao in Liu, Xiao, Shao, Broce, and Zhang, 2014b is the oldest known scalidophoran worm and so far the only cycloneuralian animal reported from the Cambrian Fortunian Stage (Liu et al, 2014b). The holotype and only specimen is a fragment with the proboscis and only the anterior trunk part preserved (Liu et al, 2014b). The posterior trunk part was missing, preventing a complete reconstruction of this microscopic worm.…”