The nervous system of the lophophore in the ctenostome Amathia gracilis provides insight into the morphology of ancestral ectoprocts and the monophyly of the lophophorates

Abstract

BackgroundThe Bryozoa (=Ectoprocta) is a large group of bilaterians that exhibit great variability in the innervation of tentacles and in the organization of the cerebral ganglion. Investigations of bryozoans from different groups may contribute to the reconstruction of the bryozoan nervous system bauplan. A detailed investigation of the polypide nervous system of the ctenostome bryozoan Amathia gracilis is reported here.ResultsThe cerebral ganglion displays prominent zonality and has at least three zones: proximal, central, and distal. The proximal zone is the most developed and contains two large perikarya giving rise to the tentacle sheath nerves. The neuroepithelial organization of the cerebral ganglion is revealed. The tiny lumen of the cerebral ganglion is represented by narrow spaces between the apical projections of the perikarya of the central zone. The cerebral ganglion gives rise to five groups of main neurite bundles of the lophophore and the tentacle sheath: the circum-oral nerve ring, the lophophoral dorso-lateral nerves, the pharyngeal and visceral neurite bundles, the outer nerve ring, and the tentacle sheath nerves. Serotonin-like immunoreactive nerve system of polypide includes eight large perikarya located between tentacles bases. There are two analmost and six oralmost perikarya with prominent serotonergic “gap” between them. Based on the characteristics of their innervations, the tentacles can be subdivided into two groups: four that are near the anus and six that are near the mouth. Two longitudinal neurite bundles - medio-frontal and abfrontal - extend along each tentacle.ConclusionThe zonality of the cerebral ganglion, the presence of three commissures, and location of the main nerves emanating from each zone might have caused by directive innervation of the various parts of the body: the tentacles sheath, the lophohpore, and the digestive tract. Two alternative scenarios of bryozoan lophophore evolution are discussed. The arrangement of large serotonin-like immunoreactive perikarya differs from the pattern previously described in ctenostome bryozoans. In accordance with its position relative to the same organs (tentacles, anus, and mouth), the lophophore outer nerve ring corresponds to the brachiopod lower brachial nerve and to the phoronid tentacular nerve ring. The presence of the outer nerve ring makes the lophophore innervation within the group (clade) of lophophorates similar and provides additional morphological evidence of the lophophore homology and monophyly of the lophophorates.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0744-7) contains supplementary material, which is available to authorized users.

Neuroanatomy of Hyalinella punctata: Common patterns and new characters in phylactolaemate bryozoans

“…In the ctenostome Amathia gracilis only, the tentacles are innervated by two neurite bundles, one frontally and one abfrontally. However, the single frontal neurite bundle results from fusions of the typical three bundles on the frontal side (Temereva & Kosevich, ). The cheilostome Electra pilosa shows a similar pattern to most ctenostomes with four neurite bundles for each tentacle, but with the abfrontal neurite bundle also originating in the median plane of each tentacle and not intertentacularly (Lutaud, ).…”

“…The bryozoan nervous system has been subject of several studies (see Gruhl & Schwaha, for review), but only few have employed modern techniques such as immunocytochemistry and confocal laser scanning microscopy on larval (e.g., Gruhl, ; Santagata, ; Schwaha, Handschuh, Redl, & Wanninger, Shimizu, Hunter, & Fusetani, ) or adults of this phylum (Schwaha, Wood, & Wanninger, ; Schwaha & Wanninger, ; Shunkina et al, ; Temereva & Kosevich, ; Weber, Wanninger, & Schwaha, ). A recent study investigated the nervous system in three phylactolaemates with modern techniques (Shunkina et al, ).…”

Ultrastructure of the coelom in the brachiopodLingula anatina

“…During the last two decades, however, the validity of the Lophophorata as a group has been discussed, and bryozoans were assigned to a separate clade (Halanych et al, ; Hausdorf, Helmkampf, Nesnidal, & Bruchhaus, ; Helmkampf, Bruchhaus, & Hausdorf, ); this clade was not considered to be related to the Brachiozoa, a group that recently included phoronids and brachiopods according to some authors (Cohen, ; Santagata & Cohen, ). Recent research supported the unity of the Lophophorata based on molecular characteristics (Jang & Hwang, ; Nesnidal et al, ) and morphology (Temereva & Kosevich, ; Temereva & Tsitrin, ).…”

Nemertean and phoronid genomes reveal lophotrochozoan evolution and the origin of bilaterian heads

“…Traditionally, the lophophore is a feeding apparatus defined as a mesosomal extension with ciliated tentacles that are present in both pterobranch hemichordates and lophophorates. To avoid confusion, here, we apply the term 'lophophore' to the horseshoeshaped homologous structure shared by brachiopods and phoronids 42 . Recent immunohistochemical and ultrastructural studies have shown that the lophophore is enriched with neural cells 42,43 , yet the molecular signature of the lophophore remains unclear.…”

“…To avoid confusion, here, we apply the term 'lophophore' to the horseshoeshaped homologous structure shared by brachiopods and phoronids 42 . Recent immunohistochemical and ultrastructural studies have shown that the lophophore is enriched with neural cells 42,43 , yet the molecular signature of the lophophore remains unclear. To explore the origin of the lophophore, we applied molecular profiling using an unbiased all-to-all pairwise comparison of different tissues among Notospermus, Phoronis and Lingula using RNAseq (Fig.…”