Demonstration of the preoral coelom in the brachiopod Lingula anatina with consideration of its phylogenetic significance

Abstract

The origin of the Bilateria and reconstruction of the last common bilaterian ancestor (LCA) are fundamental problems in zoology, including the question whether the LCA was a coelomic creature or not? Insight into the nature of the LCA might be obtained by investigating the coelomic system of poorly studied bilaterians. The Brachiopoda is a relict group of marine invertebrates whose anatomy has been seldom studied with modern methods. For most brachiopods, the coelomic system has been described as bipartite, i.e., as consisting of two parts: the lophophore coelom and trunk coelom. In the present report, a tripartite coelomic system is described for the first time in adult brachiopods, the linguliform Lingula anatina. In addition to a lophophoral and trunk coelom, L. anatina has a preoral coelom. The protocoel is located at the base of the epistome and has its own lining, which consists of non-muscular monociliated epithelial cells connected by desmosomes and tight junctions. Among brachiopods there are two types of the coelom: bipartite and tripartite. The same is known in phoronids and bryozoans (=ectoprocts). These three phyla – brachiopoda, phoronida, and bryozoa – are traditionally united into clade called lophophorata. An analysis of coelomic system organization revealed that the trimeric coelom is plesiomorphic for the lophophorates. The trimeric coelom is typical for the most of deuterostomes. The presence of the trimeric coelom in two main lineages of the bilateria allows to suggest that the LCA may have had a tripartite coelom and strongly specialized two the most anterior parts of the body – the prosome and the mesosome. This suggestion is consistent with published gene expression studies, in which Hox genes are never expressed in the two first segments of the body, whereas Otx genes are expressed in the most anterior segments of some bilaterians.