First Modern Data on the Lophophore Nervous System in Adult Novocrania anomala and a Current Assessment of Brachiopod Phylogeny

Abstract

Although the lophophore is regarded as the main synapomorphy of all lophophorates, the evolution of the lophophore in certain groups of lophophorates remains unclear. To date, the innervation of the lophophore has been studied with modern methods only for three brachiopod species belonging to two subphyla: Linguliformea and Rhynchonelliformea. In the third subphylum, the Craniiformea, there are data for juveniles but not for adults. In the current research, the innervation of the lophophore in Novocrania anomala adults was studied by immunocytochemistry and confocal laser scanning microscopy. In the spiral lophophore of adults of the craniiform N. anomala, each arm is innervated by six brachial nerves: main, additional main, accessory, second accessory, additional lower, and lower brachial nerves. Compared with other brachiopod species, this complex innervation of the lophophore correlates with the presence of many lophophoral muscles. The general anatomy of the lophophore nervous system and the peculiarities of the organization of the subenteric ganglion of the craniiform N. anomala have a lot in common with those of rhynchonelliforms but not with those of linguliforms. These findings are consistent with the “Calciata” hypothesis of the brachiopod phylogeny and are inconsistent with the inference that the Craniiformea and Linguliformea are closely related.

Homology of the lophophore and its evolution within lophophorates

“…These nervous centers are located in the thickened epithelium and cannot be called "true ganglia" . The two ganglia are connected by the circumenteric connectives (Bemmelen, 1883;Temereva, 2020bTemereva, , 2022.…”

“…Only rhynchonelliform brachiopods possess a supraenteric ganglion that is located above the mouth and gives rise to the main nerves of the lophophore (Bemmelen, 1883;Williams et al, 1997;. In adult craniiforms, dorsal thin neurites are located above the mouth and connect the left and right main brachial nerves; the circumenteric connectives emanate laterally from the subenteric ganglion and connect with the main brachial nerves, forming a ring around the esophagus (Temereva, 2022). The same structure of the main nervous system is known in adult lingulids (Linguliformea) (Blochmann, 1900).…”

“…However, juveniles of Novocrania anomala (Craniiformea) with a trocholophe have a prominent supraenteric ganglion that consists of two lobes and the commissure between them. In ontogenesis (in juveniles with schizolophe), the commissure between the two lobes of the ganglion extend and become the main brachial nerve in adults (Temereva, 2020b(Temereva, , 2022. Juvenile Glottidia pyramidata (Linguliformea) with trocholophous lophophore swim in the water and have the prominent apical ganglion located in the medial tentacle (Hay-Schmidt, 1992;Santagata, 2011).…”

“…In rhynchonelliforms , the subenteric ganglion also gives rise to the lower brachial nerves. In linguliforms (Blochmann, 1900) and craniiforms (Temereva, 2020b(Temereva, , 2022, the lower nerves connect with the circumenteric connectives. In juvenile G. pyramidata, the dorsal nerve connects the apical and subenteric ganglia, giving rise to the abfrontal nerves of the tentacles (Santagata, 2011), and is possibly homologous to the circumenteric connectives of other brachiopods.…”

“…In linguliforms, the development of the main nerve is unknown. In all investigated brachiopods, main nerves give rise to the series of cross nerves that extend in the connective tissue and join with the accessory nerve in linguliforms (Temereva, Tzitrin, 2015) and craniiforms (Temereva, 2022), and with the second accessory nerve in rhynchonelliforms (Temereva, Kuzmina, 2017.…”