Abstract
BackgroundReconstructing the evolutionary history of nervous systems requires an understanding of their architecture and development across diverse taxa. The spiralians encompass diverse body plans and organ systems, and within the spiralians, annelids exhibit a variety of morphologies, life histories, feeding modes and associated nervous systems, making them an ideal group for studying evolution of nervous systems.ResultsWe describe nervous system development in the annelid Capitella teleta (Blake JA, Grassle JP, Eckelbarger KJ. Capitella teleta, a new species designation for the opportunistic and experimental Capitella sp. I, with a review of the literature for confirmed records. Zoosymposia. 2009;2:25–53) using whole-mount in situ hybridization for a synaptotagmin 1 homolog, nuclear stains, and cross-reactive antibodies against acetylated α-tubulin, 5-HT and FMRFamide. Capitella teleta is member of the Sedentaria (Struck TH, Paul C, Hill N, Hartmann S, Hosel C, Kube M, et al. Phylogenomic analyses unravel annelid evolution. Nature. 2011;471:95–8) and has an indirectly-developing, lecithotrophic larva. The nervous system of C. teleta shares many features with other annelids, including a brain and a ladder-like ventral nerve cord with five connectives, reiterated commissures, and pairs of peripheral nerves. Development of the nervous system begins with the first neurons differentiating in the brain, and follows a temporal order from central to peripheral and from anterior to posterior. Similar to other annelids, neurons with serotonin-like-immunoreactivity (5HT-LIR) and FMRFamide-like-immunoreactivity (FMRF-LIR) are found throughout the brain and ventral nerve cord. A small number of larval-specific neurons and neurites are present, but are visible only after the central nervous system begins to form. These larval neurons are not visible after metamorphosis while the rest of the nervous system is largely unchanged in juveniles.ConclusionsMost of the nervous system that forms during larvogenesis in C. teleta persists into the juvenile stage. The first neurons differentiate in the brain, which contrasts with the early formation of peripheral, larval-specific neurons found in some spiralian taxa with planktotrophic larvae. Our study provides a clear indication that certain shared features among annelids - e.g., five connectives in the ventral nerve cord - are only visible during larval stages in particular species, emphasizing the need to include developmental data in ancestral character state reconstructions. The data provided in this paper will serve as an important comparative reference for understanding evolution of nervous systems, and as a framework for future molecular studies of development.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-015-0108-y) contains supplementary material, which is available to authorized users.
Highlights
MethodsAnimal care Capitella teleta adults [26] were maintained in the lab as described in [43] with the following exceptions
Reconstructing the evolutionary history of nervous systems requires an understanding of their architecture and development across diverse taxa
Animals with different larval and adult body plans can exhibit larval nervous systems that are restructured into the adult nervous system at metamorphosis or that degenerate and are replaced by the adult nervous system at metamorphosis [6,7,8]
Summary
Animal care Capitella teleta adults [26] were maintained in the lab as described in [43] with the following exceptions. ASW was made by mixing 2 cups (~559.8 g) of Instant Ocean Sea Salt into 15.14 L distilled water. This solution was vigorously mixed and allowed to sit overnight. Immunohistochemistry Depending on age, animals were treated for fixation as follows: 1) Stages 4 – 9 were incubated at room temperature (r.t.) in a 1:1 mixture of 0.37 M MgCl2 and FSW or ASW for 5 – 15 minutes, and fixed for 15 – 30 minutes at room temperature with 4 % paraformaldehyde (diluted from 32 % paraformaldehyde ampules from Electron Microscopy Sciences) in FSW or ASW. The animals were washed several times with phosphatase buffered saline (PBS) and PBS + 0.1 % Triton X-100 (PBT) and stored in PBS at 4 °C
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