Expanding Coelomic Cavity Reveals Key Evolutionary Innovations in Early Lingulellotretid Brachiopods

Lingulide brachiopods are traditional representatives for demonstrating extreme evolutionary conservatism with little change in outline from its Cambrian relatives. However, less attention has been paid to their anatomic and ontogenetic innovations and modifications since the early Cambrian when they firstly appeared. Here, new and exquisitely preserved specimens of Lingulellotretidae Lingulellotreta, a unique genus with typical elongate pedicle foramen and large pseudointerarea, representing one of the earliest lingulide groups, are described in detail, shedding light on studying lingulide evolution. The material comes both from the famous Cambrian Epoch 2 Chengjiang Lagerstätte and from associated co-eval limestones as Small Shelly Fossils. Although the evolution of lingulides is characterized by prolonged stasis, combined evidence from the soft-tissue preservation and three-dimensional phosphatic materials reveals the superficial persistence of tongue-shaped shells in lingulides from as early as the beginning of the Cambrian. Our results demonstrate that the posterior expansion of the pouch-like coelomic cavity, larval metamorphosis and columnar shell architecture represent plesiomorphic characters, which are dramatically modified in living lingulides. The evolutionary transition of these traits was probably helpful for their ecological adaptation to their benthic environments. Thus, the mixture of ancestral and derived traits in living lingulides may be resulted from the mosaic evolution commencing from the Cambrian explosion. However, the novel extension of the coelomic cavity posteriorly could be a failed evolutionary experiment by early Cambrian lingulellotretids, which limited their geographic distribution in Kazakhstan and South China, and extinguished quickly in the Early Ordovician. This research provides directly fossil evidence on the phenotypic evolution of a stereotypic brachiopod in terms of their anatomic construction, ontogeny and shell biomineralization. The development of the distinctive, persistent tongue-shaped body of linguloid brachiopods probably thrived during the Great Ordovician Biodiversification Event. Further studies of long-term evolutionary groups will help understanding the intrinsic transformations between living and fossil lineages over vast periods of time.