Abstract
BackgroundLarval features such as the apical organ, apical ciliary tuft, and ciliated bands often complicate the evaluation of hypotheses regarding the origin of the adult bilaterian nervous system. Understanding how neurogenic domains form within the bilaterian head and larval apical organ requires expression data from animals that exhibit aspects of both centralized and diffuse nervous systems at different life history stages. Here, we describe the expression of eight neural-related genes during the larval development of the brachiopod, Terebratalia transversa.ResultsRadially symmetric gastrulae broadly express Tt-Six3/6 and Tt-hbn in the animal cap ectoderm. Tt-NK2.1 and Tt-otp are restricted to a central subset of these cells, and Tt-fez and Tt-FoxQ2 expression domains are already asymmetric at this stage. As gastrulation proceeds, the spatial expression of these genes is split between two anterior ectodermal domains, a more dorsal region comprised of Tt-Six3/6, Tt-fez, Tt-FoxQ2, and Tt-otp expression domains, and an anterior ventral domain demarcated by Tt-hbn and Tt-NK2.1 expression. More posteriorly, the latter domains are bordered by Tt-FoxG expression in the region of the transverse ciliated band. Tt-synaptotagmin 1 is expressed throughout the anterior neural ectoderm. All genes are expressed late into larval development. The basiepithelial larval nervous system includes three neurogenic domains comprised of the more dorsal apical organ and a ventral cell cluster in the apical lobe as well as a mid-ventral band of neurons in the mantle lobe. Tt-otp is the only gene expressed in numerous flask-shaped cells of the apical organ and in a subset of neurons in the mantle lobe.ConclusionsOur expression data for Tt-Six3/6, Tt-FoxQ2, and Tt-otp confirm some aspects of bilaterian-wide conservation of spatial partitioning within anterior neurogenic domains and also suggest a common origin for central otp-positive cell types within the larval apical organs of spiralians. However, the field of sensory neurons within the larval apical organ of Terebratalia is broader and composed of more cells relative to those of other spiralian larvae. These cellular differences are mirrored in the broader spatial and temporal expression patterns of Tt-FoxQ2 and Tt-otp. Corresponding differences in the expression of Tt-hbn, Tt-NK2.1, and Tt-FoxG are also observed relative to their respective domains within the cerebral ganglia of spiralians. Based on these data we argue that the anterior region of the bilaterian stem species included Six3/6, NK2.1, otp, hbn, fez, and FoxQ2 expression domains that were subsequently modified within larval and adult neural tissues of protostome and deuterostome animals.
Highlights
Larval features such as the apical organ, apical ciliary tuft, and ciliated bands often complicate the evaluation of hypotheses regarding the origin of the adult bilaterian nervous system
During larval development the most anterior portion of the apical lobe differentiates into a rounded dome that sits on the wider cylindrically shaped portion that will include the anterior transverse ciliated band
Conclusions wide scale homology may be present in select, centralized, apical neuronal cell types among evolutionarily distant larval types [39], species-specific deployment of these cell types within the anterior regions of diverse larval forms may result in independently derived apical organs, evolutionarily old cell types may be used in new ways [46], or specific developmental patterns may result in the partial or complete absence of these cellular features
Summary
Larval features such as the apical organ, apical ciliary tuft, and ciliated bands often complicate the evaluation of hypotheses regarding the origin of the adult bilaterian nervous system. Based on similar expression patterns of evolutionarily conserved transcription factors, some authors have concluded that the structure of the adult nervous system of the last common ancestor of the Bilateria included an anterior brain with three divisions and a distinct longitudinal ventral nerve cord [1,2,3], with bilaterians that exhibit a more diffusely organized central nervous system (for example, hemichordates) having acquired this characteristic secondarily [4]. Other hypotheses suggest that the last common ancestor of all bilaterians was more similar to extant acoelomorph flatworms that have an anterior compact brain with a centralized neuropil and parallel dorsal, ventral, and lateral longitudinal nerve cords [5,6], and that adult bilaterian ‘brains’ have evolved independently several times [7]. The majority of information on bilaterian neural development focuses on animals that form a centralized subepithelial nervous system and much less information is known about animals with diverse forms of intraepithelial nervous systems (so called ‘skin brains’ see [11]), whose significance in protostome evolution is rarely addressed
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