Development of the nervous system in Phoronopsis harmeri (Lophotrochozoa, Phoronida) reveals both deuterostome- and trochozoan-like features

Elena Temereva,Andreas Wanninger

doi:10.1186/1471-2148-12-121

Abstract

BackgroundInferences concerning the evolution of invertebrate nervous systems are often hampered by the lack of a solid data base for little known but phylogenetically crucial taxa. In order to contribute to the discussion concerning the ancestral neural pattern of the Lophotrochozoa (a major clade that includes a number of phyla that exhibit a ciliated larva in their life cycle), we investigated neurogenesis in Phoronopsis harmeri, a member of the poorly studied Phoronida, by using antibody staining against serotonin and FMRFamide in combination with confocal microscopy and 3D reconstruction software.ResultsThe larva of Phoronopsis harmeri exhibits a highly complex nervous system, including an apical organ that consists of four different neural cell types, such as numerous serotonin-like immunoreactive flask-shaped cells. In addition, serotonin- and FMRFamide-like immunoreactive bi- or multipolar perikarya that give rise to a tentacular neurite bundle which innervates the postoral ciliated band are found. The preoral ciliated band is innervated by marginal serotonin-like as well as FMRFamide-like immunoreactive neurite bundles. The telotroch is innervated by two neurite bundles. The oral field is the most densely innervated area and contains ventral and ventro-lateral neurite bundles as well as several groups of perikarya. The digestive system is innervated by both serotonin- and FMRFamide-like immunoreactive neurites and perikarya. Importantly, older larvae of P. harmeri show a paired ventral neurite bundle with serial commissures and perikarya.ConclusionsSerotonin-like flask-shaped cells such as the ones described herein for Phoronopsis harmeri are found in the majority of lophotrochozoan larvae and therefore most likely belong to the ground pattern of the last common lophotrochozoan ancestor. The finding of a transitory paired ventral neurite bundle with serially repeated commissures that disappears during metamorphosis suggests that such a structure was part of the “ur-phoronid” nervous system, but was lost in the adult stage, probably due to its acquired sessile benthic lifestyle.

Highlights

Inferences concerning the evolution of invertebrate nervous systems are often hampered by the lack of a solid data base for little known but phylogenetically crucial taxa
While an impressive amount of data on the development of the nervous system has recently become available for numerous lophotrochozoan subtaxa, phoronid neurogenesis is still comparatively little known, with most studies dealing with the description of the neuroanatomy of more or less mature larvae rather than with the development of the nervous system as such [15,16,17,18,19,20,21]
In order to broaden the database on phoronid neurogenesis and larval neuroanatomy and to contribute to the discussion concerning the groundpattern of the phoronid and lophotrochozoan neural bauplan, we investigated the development of the serotoninlike and FMFRamide-like immunoreactive nervous system during larval development of Phoronopsis harmeri

Summary

Introduction

Inferences concerning the evolution of invertebrate nervous systems are often hampered by the lack of a solid data base for little known but phylogenetically crucial taxa. Based on a proposed homologous feeding organ, the lophophore, Phoronida has been traditionally aligned with Ectoprocta and Brachiopoda to form the monophyletic Lophophorata [6,7] This view is supported by a shared radial type of cleavage [8] ( some unpublished observations claim that spiral cleavage may be present in some phoronids), but otherwise there is little morphological support for such an assemblage, mainly due to the high disparity of the adult bodyplans of these phyla. The unexpected recent finding of a paired ventral neurite bundle in the actinotroch larva of Phoronopsis harmeri [22] similar to most spiralians may provide evidence for such a neural system in the phoronid as well as lophotrochozoan groundplan Such a scenario would imply, secondary loss of this paired ventral nervous system in adult phoronids (probably as a result of a sessile lifestyle), since they do not exhibit a comparable neural structure. In order to broaden the database on phoronid neurogenesis and larval neuroanatomy and to contribute to the discussion concerning the groundpattern of the phoronid and lophotrochozoan neural bauplan, we investigated the development of the serotoninlike and FMFRamide-like immunoreactive nervous system during larval development of Phoronopsis harmeri

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