Serotonin‐containing neurons in basal insects: In search of ground patterns among tetraconata

Abstract

The ventral nerve cord of Tetraconata contains a comparably low number of serotonin-immunoreactive neurons, facilitating individual identification of cells and their characteristic neurite morphology. This offers the rather unique possibility of establishing homologies at the single cell level. Because phylogenetic relationships within Tetraconata are still discussed controversially, comparisons of individually identifiable neurons can help to unravel these issues. Serotonin immunoreactivity has been investigated in numerous tetraconate taxa, leading to reconstructions of hypothetical ground patterns for major lineages. However, detailed descriptions of basal insects are still missing, but are crucial for meaningful evolutionary considerations. We investigated the morphology of individually identifiable serotonin-immunoreactive neurons in the ventral nerve cord of Zygentoma (Thermobia domestica, Lepisma saccharina, Atelura formicaria) and Archaeognatha (Machilis germanica, Dilta hibernica). To improve immunocytochemical resolution, we also performed preincubation experiments with 5-hydroxy-L-tryptophan and serotonin. Additionally, we checked for immunolabeling of tryptophan hydroxylase, an enzyme associated with the synthesis of serotonin. Besides the generally identified groups of anterolateral, medial, and posterolateral neurons within each ganglion of the ventral nerve cord, we identified several other immunoreactive cells, which seem to have no correspondence in other tetraconates. Furthermore, we show that not all immunoreactive neurons produce serotonin, but have the capability for serotonin uptake. Comparisons with the patterns of serotonin-containing neurons in major tetraconate taxa suggest a close phylogenetic relationship of Remipedia, Cephalocarida, and Hexapoda, supporting the Miracrustacea hypothesis. J. Comp. Neurol., 2016. © 2016 Wiley Periodicals, Inc. J. Comp. Neurol. 525:79-115, 2017. © 2016 Wiley Periodicals, Inc.

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

“…Open circles in the archaeognathan and zygentoman patterns show neurons that are part of the thoracic but not of the abdominal pattern (see [1] for details). In Zygentoma, identification of anterior serially homologous neurons proved to be impossible due to intra- and interspecific variations in number, projection pattern and cell body size (marked by ‘?’, compare [1]). Red box encloses taxa, constituting the Miracrustacea (after [48]).…”

“…The morphology of serotonin-immunoreactive (5HT-ir) neurons in the ganglia of the arthropod ventral nerve cord (VNC) caught the attention of scientists over the past 30 years (summarized in [1]). It has been proposed that these neurons are a suitable character set for phylogenetic comparisons due to the following characteristics: (1) Only a small number of neurons possessing serotonin (5HT) as neurotransmitter is distributed in the nervous system, (2) intra- and interspecific serial homology provide opportunities to reconstruct evolutionary scenarios, and (3) numerous studies have described these neurons in a great diversity of arthropod species.…”

“…Along these lines, Harzsch [21, 22] reconstructed ground patterns for major tetraconate lineages, demonstrating the potential of individually identifiable neurons as independent characters for evolutionary considerations. Recently, corresponding studies have been undertaken for the crustacean taxa Cephalocarida [23] and Remipedia [24], as well as the hexapod taxa Zygentoma and Archaeognatha [1], including an update on specific ground patterns (sensu [22]). Although a wealth of tetraconate taxa have been investigated in great detail, our knowledge on more basal arthropod lineages, i.e., Chelicerata and Myriapoda, is limited.…”

“…In recent studies on Cephalocarida [23], Remipedia [24], as well as basal insects [1], yet another group of neurons has been described in a medial position. In order to gain deeper insights into the phylogenetic significance of these data for Tetraconata, it is important explore the situation in Myriapoda, which is the proposed sister taxon to Tetraconata [28–30].…”

“…However, while to date the study by Harzsch [22] is the only to describe 5HT-ir neurons in the myriapod ventral nerve cord, the projection pattern of these neurons remained unresolved. Due to recent accounts and resulting controversies in interpreting these data, a detailed re-examination of myriapod taxa has been demanded [1, 23, 27], as information on basal mandibulate taxa is crucial for our understanding of the phylogenetic value of 5HT-ir neurons. In this context, two hypotheses concerning the tetraconate ground pattern have been proposed.…”