Evolution and diversity of biomineralized columnar architecture in early Cambrian phosphatic-shelled brachiopods

Abstract

Biologically controlled mineral crystals producing organic-inorganic composites (hard skeletons) by metazoan biomineralizers has been an evolutionary innovation for more than half billion years on Earth. Among them, linguliform brachiopods are the only invertebrates that secrete phosphate to build their skeletons. One of the most distinct shell structures is the organic-phosphatic columns applied exclusively by phosphatic-shelled brachiopods. However, the complexity, diversity and biomineralization process of these microscopic columns are far from clear in brachiopod ancestors. Here, exquisitely well preserved columnar structures are discovered for the first time in the earliest eoobolids. The hierarchical shell architectures, epithelial cell moulds, and the shape and size of cylindrical columns are scrutinised in Latusobolus xiaoyangbaensis gen. et sp. nov. and Eoobolus acutulus sp. nov from the Cambrian Series 2 Shuijingtuo Formation of South China. The secretion and construction of the stacked sandwich model of columnar shell, which played a significant role in the evolution of linguliforms, is highly biologically controlled and organic-matrix mediated. Furthermore, a continuous transformation of anatomic features resulting from the growth of columns is revealed between Eoobolidae, Lingulellotretidae and Acrotretida, shedding new light on the evolutionary growth and adaptive innovation of stacked sandwich columns among early phosphatic-shelled brachiopods during the Cambrian explosion.