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Distribution and evolution of serotonin-like immunoreactive cells in Thaliacea (Tunicata)

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Abstract

Thaliacea are marine planktonic animals within the taxon Tunicata. The species-poor taxon is characterized by diverse life cycles, with sexually (blastozooid) and asexually (oozooid) reproducing generations, that usually evolved polymorph phenotypes. While recent molecular phylogenetic studies indicate that tunicates might be closest living relatives to free-living craniates, additional insights into the evolution of the nervous systems of planktonic tunicates are overdue. To test the hypothesis that polymorphism in the different stages correlates with different distribution patterns of neurotransmitters, we comparatively conducted immunostaining experiments utilizing antibodies against serotonin and tyrosinated-α-tubulin, and confocal laser scanning microscopy in planktonic Thaliacea. We considerably increase the available data on serotonin-like immunoreactive (serotonin-lir) in Thaliacea and found that the pattern of distribution of serotonin-lir cells clearly differs between oozooid and blastozooid stages. Thereby, we reveal that the distribution of serotonin-lir cells in different tissues of thaliaceans can be considered as independent characters. Further, we test the potential phylogenetic signal present in serotonin-lir in thaliaceans, propose a phylogenetic mapping of conceptualized characters, and analyze the evolution of serotonin-lir cells. Comparing our results with data from previous studies indicated that it was necessary to reevaluate already described distribution patterns of serotonin-lir. Due to the complex life cycles of Salpida and Doliolida, erroneous descriptions of the localization of serotonin-lir occur in thaliacean literature. To facilitate the evaluation of data on serotonin-lir in thaliaceans for future readers, we suggest depicting whole-mount stainings of complete animals.

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Acknowledgements

The authors would like to thank Stefano Tiozzo for expert collection and fixation of specimens of Salpa fusiformis. We are thankful to the invaluable help of Woody Lee and Scott Jones from the Smithsonian Marine Station in Fort Pierce, Florida in securing specimens of Iasis cylindrica, Salpa fusiformis, Thalia democratica and Doliolum nationalis. We are also indebted to Prof. Valerie Paul and Prof. Mary Rice for generously providing access to the facilities of the Smithsonian Marine Station. We are much obliged to the scientific party and the crew of FS SONNE during the cruise SO258/1, especially to Dr. Nina Furchheim and Reinhard Werner for collecting and fixing specimens of Pyrostremma agassizi, Pyrosoma atlanticum, and Pyrosomella verticillata. We are grateful for the access to the Leica SPE CLSM granted by Dr. Carsten Lüter (Museum für Naturkunde Berlin). Funding by the Deutsche Forschungsgemeinschaft (DFG), the German Academic Exchange Service (DAAD), and the Elsa-Neumann-Stipendium des Landes Berlin is gratefully acknowledged.

Funding

This study was funded by the Deutsche Forschungsgemeinschaft (DFG) Grant STA655/4-1, the German Academic Exchange Service (DAAD), and the Elsa-Neumann-Stipendium des Landes Berlin.

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Correspondence to Katrin Braun.

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The authors declare that they have no conflict of interest. This article does not contain any studies with human participants performed by any of the authors. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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435_2018_416_MOESM1_ESM.pdf

Supplementary Fig.: Interactive 3d model of the internal anatomy of the blastozooid stage of D. nationalis and of P. atlanticum based on serial sections for light microscopy. A: Anatomy of D. nationalis, dorsal view anterior to the top. The ciliated funnel (cf) opens into the branchial basket (bb—not completely shown in the 3d reconstruction) in close spatial relation to the dorsal spiral of the peripharyngeal band (pb). B: Internal anatomy of P. atlanticum, view from the left side, anterior to the top. The pyloric gland (pg) is dendritically shaped. Originating from the stomach (st), the pyloric gland forms several branches that connect with the posterior intestinal wall. br: brain, en: endostyle, ep: epidermis, es: esophagus, ex: excurrent siphon, in: intestine, is: incurrent siphon, lo: light organ, ng: neural gland, ov: ovary, pe: pericardium, te: testis. (PDF 45876 KB)

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Braun, K., Stach, T. Distribution and evolution of serotonin-like immunoreactive cells in Thaliacea (Tunicata). Zoomorphology 137, 565–578 (2018). https://doi.org/10.1007/s00435-018-0416-9

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  • DOI: https://doi.org/10.1007/s00435-018-0416-9

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