Evolutionary and Structural Diversification of the Larval Nervous System Among Marine Bryozoans

Abstract

Abstract. Regardless of the morphological divergence among larval forms of marine bryozoans, the larval nervous system and its major effector organs (musculature and ciliary fields) are largely molded on the basis of functional demands of feeding, ciliary propulsion, phototactic behaviors, and substrate exploration. Previously published ultrastructural information and immunohistochemical reconstructions presented here indicate that neuronal pathways are largely ipsilateral, with more complex synaptic connections localized within the nerve nodule. Multiciliated sensory-motor neurons diversify structurally and functionally on the basis of their position along the axis of swimming largely due to the functional demands of photoklinotaxis and substrate exploration. Vesiculariform, buguliform, and ascophoran coronate larvae all have patches of sensory neurons bordering the pyriform organ's ciliated groove (juxtapapillary cells and border cells) that are active during substrate selection. Despite their simplified form, cyclostome larvae maintain swimming and probing behaviors with sensory-motor systems functionally similar to those of some parenchymella and planula larval types. Considering the evolutionary relationships among the morphological grades of marine bryozoans, particular lineages within the gymnolaemates have independently evolved larval traits that convey a greater range of sensory abilities and increased propulsive capacity. The larval nervous system of bryozoans may be evolutionarily derived from the pretrochal region of a trochophore-like larval form.

Serotonergic and FMRFamidergic nervous systems in gymnolaemate bryozoan larvae

“…Pires and Woollacott (1997) and Shimizu et al (2000) reported brieXy on distribution of serotonin in larvae of Bugula neritina. Further data on coronate larvae have been obtained from Triphyllozoon mucronatum (Wanninger et al 2005b) and Celleporaria sherryae (Santagata 2008). The only immunocytochemical data from cyphonautes larvae come from Membranipora sp.…”

“…The only immunocytochemical data from cyphonautes larvae come from Membranipora sp. (Hay-Schmidt 2000) and Membranipora membranacea (Santagata 2008). However, bryozoans exhibit several more diVerent larval types.…”

Ectoprocta

“…The cell types and anatomy of the larval nervous system and musculature have been better studied in selected species of gymnolaemates, and, collectively, these data support some broad-scale homology with the larval neuromuscular systems of spiralian protostomes (Santagata 2008b ;Gruhl 2009 ;Wanninger 2009 ) All gymnolaemate embryos have a late gastrula stage with a comparatively large ring of coronal cells equatorially arranged between the more cell-rich oral and aboral larval fi elds. In species with a cyphonautes larva, the entirety of the oral cell fi eld will be internalized as the embryo fl attens laterally and takes on a more trapezoidal shape (Fig.…”

“…In all species investigated, these cells form the larval pyriform complex consisting of a superior and an inferior glandular fi eld of cells bordering four specialized multiciliated cells that constitute the vibratile plume. The pyriform complex has numerous other sensory and neuronal cells (Reed et al 1988 ;Santagata 2008b ) used during crawling behaviors to probe various substrates before metamorphosis. Another derivative of this cell tier is the oral epithelium that consists of ciliated cells whose primary function is to capture food particles (the ciliated ridges and cell lining of the vestibule) in feeding larvae.…”

“…The larval anatomy of cyclostome ectoprocts has been interpreted as simplifi ed or degenerate, since their larvae are the only type to lack an apical disc (and associated larval apical sense organ) and a pyriform organ and their nervous system consists of a basiepithelial network of sensory cells and neurons (Santagata 2008b ). It is not clear if the cuboidal multiciliated cells that make up the larval epidermis are homologous to the coronal cells and/or oral ciliated cells of gymnolaemate larvae.…”