Email updates

Keep up to date with the latest news and content from BMC Evolutionary Biology and BioMed Central.

Open Access Highly Accessed Research article

Serotonin immunoreactive interneurons in the brain of the Remipedia: new insights into the phylogenetic affinities of an enigmatic crustacean taxon

Torben Stemme1, Thomas M Iliffe2, Gerd Bicker1*, Steffen Harzsch3 and Stefan Koenemann4

Author affiliations

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

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

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

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

For all author emails, please log on.

Citation and License

BMC Evolutionary Biology 2012, 12:168  doi:10.1186/1471-2148-12-168

Published: 5 September 2012

Abstract

Background

Remipedia, a group of homonomously segmented, cave-dwelling, eyeless arthropods have been regarded as basal crustaceans in most early morphological and taxonomic studies. However, molecular sequence information together with the discovery of a highly differentiated brain led to a reconsideration of their phylogenetic position. Various conflicting hypotheses have been proposed including the claim for a basal position of Remipedia up to a close relationship with Malacostraca or Hexapoda. To provide new morphological characters that may allow phylogenetic insights, we have analyzed the architecture of the remipede brain in more detail using immunocytochemistry (serotonin, acetylated α-tubulin, synapsin) combined with confocal laser-scanning microscopy and image reconstruction techniques. This approach allows for a comprehensive neuroanatomical comparison with other crustacean and hexapod taxa.

Results

The dominant structures of the brain are the deutocerebral olfactory neuropils, which are linked by the olfactory globular tracts to the protocerebral hemiellipsoid bodies. The olfactory globular tracts form a characteristic chiasm in the center of the brain. In Speleonectes tulumensis, each brain hemisphere contains about 120 serotonin immunoreactive neurons, which are distributed in distinct cell groups supplying fine, profusely branching neurites to 16 neuropilar domains. The olfactory neuropil comprises more than 300 spherical olfactory glomeruli arranged in sublobes. Eight serotonin immunoreactive neurons homogeneously innervate the olfactory glomeruli. In the protocerebrum, serotonin immunoreactivity revealed several structures, which, based on their position and connectivity resemble a central complex comprising a central body, a protocerebral bridge, W-, X-, Y-, Z-tracts, and lateral accessory lobes.

Conclusions

The brain of Remipedia shows several plesiomorphic features shared with other Mandibulata, such as deutocerebral olfactory neuropils with a glomerular organization, innervations by serotonin immunoreactive interneurons, and connections to protocerebral neuropils. Also, we provided tentative evidence for W-, X-, Y-, Z-tracts in the remipedian central complex like in the brain of Malacostraca, and Hexapoda. Furthermore, Remipedia display several synapomorphies with Malacostraca supporting a sister group relationship between both taxa. These homologies include a chiasm of the olfactory globular tract, which connects the olfactory neuropils with the lateral protocerebrum and the presence of hemiellipsoid bodies. Even though a growing number of molecular investigations unites Remipedia and Cephalocarida, our neuroanatomical comparison does not provide support for such a sister group relationship.

Keywords:
Arthropoda; Comparative neuroanatomy; Sister group relationship; Immunocytochemistry; Olfactory glomeruli; Central complex; Hemiellipsoid bodies; Olfactory globular tracts; Speleonectes; Godzilliognomus