Serotonergic neurons in the ventral nerve cord of Chilopoda – a mandibulate pattern of individually identifiable neurons

Abstract

BackgroundGiven the numerous hypotheses concerning arthropod phylogeny, independent data are needed to supplement knowledge based on traditional external morphology and modern molecular sequence information. One promising approach involves comparisons of the structure and development of the nervous system. Along these lines, the morphology of serotonin-immunoreactive neurons in the ventral nerve cord has been investigated in numerous tetraconate taxa (Crustacea and Hexapoda). It has been shown that these neurons can be identified individually due to their comparably low number, characteristic soma position, and neurite morphology, thus making it possible to establish homologies at the single cell level. Within Chilopoda (centipedes), detailed analyses of major branching patterns of serotonin-immunoreactive neurons are missing, but are crucial for developing meaningful conclusions on the homology of single cells.ResultsIn the present study, we re-investigated the distribution and projection patterns of serotonin-immunoreactive neurons in the ventral nerve cord of three centipede species: Scutigera coleoptrata, Lithobius forficatus, and Scolopendra oraniensis. The centipede serotonergic system in the ventral nerve cord contains defined groups of individually identifiable neurons. An anterior and two posterior immunoreactive neurons per hemiganglion with contralateral projections, a pair of ipsilateral projecting lateral neurons (an autapomorphic character for Chilopoda), as well as a postero-lateral group of an unclear number of cells are present in the ground pattern of Chilopoda.ConclusionsComparisons to the patterns of serotonin-immunoreactive neurons of tetraconate taxa support the homology of anterior and posterior neurons. Our results thus support a sister group relationship of Myriapoda and Tetraconata and, further, a mandibulate ground pattern of individually identifiable serotonin-immunoreactive neurons in the ventral nerve cord. Medial neurons are not considered to be part of the tetraconate ground pattern, but could favor the ‘Miracrustacea hypothesis’, uniting Remipedia, Cephalocarida, and Hexapoda.

Histaminergic interneurons in the ventral nerve cord: assessment of their value for Euarthropod phylogeny

“…Examination of the pycnogonids, another rather basal clade within chelicerates, may reveal surprising results as already shown for serotonergic neurons [27]. These sea spiders are the only chelicerate taxon so far, where individually identifiable serotonergic neurons have been described, with some suggested homologies to mandibulate serotonergic neurons [27, 28].…”

“…In this context, no potentially homologous neurons between Remipedia and Hexapoda were identified in our study. Comparisons of serotonergic neurons in the ventral nerve cord of Tetraconata revealed a possible synapomorphy of Remipedia, Cephalocarida, and Hexapoda ([24, 25, 28]; but see [85] for a different interpretation).…”

“…Based on specific criteria for the homology of individually identifiable neurons established by Kutsch and Breidbach [20], these neurons might be homologized intra- and interspecifically. Along these lines, neuromorphologists have largely focused on the serotonin transmitter system [21–28]. Serotonergic neurons show clear advantages, which allow their individual identification and, consequentially, can be used for the analysis of evolutionary processes in Euarthropoda.…”

“…Second, due to the low number of serotonergic neurons, the characteristic neurite morphology can be traced rather easily, providing the basis for the reconstruction of evolutionary transformation in this transmitter system. Meanwhile, an impressive number of investigated taxa has accumulated in the literature, and ground patterns for major euarthropod taxa have been reconstructed (summarized in [24, 28]).…”

The visual pathway in sea spiders (Pycnogonida) displays a simple serial layout with similarities to the median eye pathway in horseshoe crabs

“…The biogenic amine 5-hydroxytryptamin (5HT, serotonin) is a widespread neurotransmitter in metazoans and was labeled with a polyclonal rabbit antiserum raised against serotonin coupled to BSA with PFA. The antiserum has been previously applied in various arthropod taxa, including pycnogonids [ 26 , 129 , 131 , 132 ].…”