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Open Access Research article

Serotonin-immunoreactive neurons in the ventral nerve cord of Remipedia (Crustacea): support for a sister group relationship of Remipedia and Hexapoda?

Torben Stemme1, Thomas M Iliffe2, Björn M von Reumont3, Stefan Koenemann4, Steffen Harzsch5 and Gerd Bicker1*

Author Affiliations

1 Division of Cell Biology, University of Veterinary Medicine Hannover, Bischhofsholer Damm 15, 30173, Hannover, Germany

2 Department of Marine Biology, Texas A&M University at Galveston, 200 Seawolf Parkway, Galveston, TX 77553, USA

3 Department of Life Sciences, Natural History Museum London, Cromwell, Road SW7 5BD, United Kingdom

4 Montessori Bildungshaus Hannover, Bonner Straße 10, 30173, Hannover, Germany

5 Department of Cytology and Evolutionary Biology, Institute of Zoology, Ernst-Moritz-Arndt-University of Greifswald, Soldmannstraße 23, 17487, Greifswald, Germany

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BMC Evolutionary Biology 2013, 13:119  doi:10.1186/1471-2148-13-119

Published: 10 June 2013

Abstract

Background

Remipedia were initially seen as a primitive taxon within Pancrustacea based on characters considered ancestral, such as the homonomously segmented trunk. Meanwhile, several morphological and molecular studies proposed a more derived position of Remipedia within Pancrustacea, including a sister group relationship to Hexapoda. Because of these conflicting hypotheses, fresh data are crucial to contribute new insights into euarthropod phylogeny. The architecture of individually identifiable serotonin-immunoreactive neurons has successfully been used for phylogenetic considerations in Euarthropoda. Here, we identified neurons in three species of Remipedia with an antiserum against serotonin and compared our findings to reconstructed ground patterns in other euarthropod taxa. Additionally, we traced neurite connectivity and neuropil outlines using antisera against acetylated α-tubulin and synapsin.

Results

The ventral nerve cord of Remipedia displays a typical rope-ladder-like arrangement of separate metameric ganglia linked by paired longitudinally projecting connectives. The peripheral projections comprise an intersegmental nerve, consisting of two branches that fuse shortly after exiting the connectives, and the segmental anterior and posterior nerve. The distribution and morphology of serotonin-immunoreactive interneurons in the trunk segments is highly conserved within the remipede species we analyzed, which allows for the reconstruction of a ground pattern: two posterior and one anterior pair of serotonin-immunoreactive neurons that possess a single contralateral projection. Additionally, three pairs of immunoreactive neurons are found in the medial part of each hemiganglion. In one species (Cryptocorynetes haptodiscus), the anterior pair of immunoreactive neurons is missing.

Conclusions

The anatomy of the remipede ventral nerve cord with its separate metameric ganglia mirrors the external morphology of the animal’s trunk. The rope-ladder-like structure and principal architecture of the segmental ganglia in Remipedia corresponds closely to that of other Euarthropoda. A comparison of the serotonin-immunoreactive cell arrangement of Remipedia to reconstructed ground patterns of major euarthropod taxa supports a homology of the anterior and posterior neurons in Pancrustacea. These neurons in Remipedia possess unbranched projections across the midline, pointing towards similarities to the hexapod pattern. Our findings are in line with a growing number of phylogenetic investigations proposing Remipedia to be a rather derived crustacean lineage that perhaps has close affinities to Hexapoda.

Keywords:
Euarthropoda; Homology; Comparative neuroanatomy; Ground pattern; Phylogeny; Immunocytochemistry; Speleonectes; Godzilliognomus; Cryptocorynetes