Comparative analysis of deutocerebral neuropils in Chilopoda (Myriapoda): implications for the evolution of the arthropod olfactory system and support for the Mandibulata concept

Andy Sombke,Elisabeth Lipke,Matthes Kenning,Steffen Harzsch,Bill S Hansson,Carsten Hg Müller

doi:10.1186/1471-2202-13-1

Abstract

BackgroundOriginating from a marine ancestor, the myriapods most likely invaded land independently of the hexapods. As these two evolutionary lineages conquered land in parallel but separately, we are interested in comparing the myriapod chemosensory system to that of hexapods to gain insights into possible adaptations for olfaction in air. Our study connects to a previous analysis of the brain and behavior of the chilopod (centipede) Scutigera coleoptrata in which we demonstrated that these animals do respond to volatile substances and analyzed the structure of their central olfactory pathway.ResultsHere, we examined the architecture of the deutocerebral brain areas (which process input from the antennae) in seven additional representatives of the Chilopoda, covering all major subtaxa, by histology, confocal laser-scan microscopy, and 3D reconstruction. We found that in all species that we studied the majority of antennal afferents target two separate neuropils, the olfactory lobe (chemosensory, composed of glomerular neuropil compartments) and the corpus lamellosum (mechanosensory). The numbers of olfactory glomeruli in the different chilopod taxa ranged from ca. 35 up to ca. 90 and the shape of the glomeruli ranged from spheroid across ovoid or drop-shape to elongate.ConclusionA split of the afferents from the (first) pair of antennae into separate chemosensory and mechanosensory components is also typical for Crustacea and Hexapoda, but this set of characters is absent in Chelicerata. We suggest that this character set strongly supports the Mandibulata hypothesis (Myriapoda + (Crustacea + Hexapoda)) as opposed to the Myriochelata concept (Myriapoda + Chelicerata). The evolutionary implications of our findings, particularly the plasticity of glomerular shape, are discussed.

Highlights

Originating from a marine ancestor, the myriapods most likely invaded land independently of the hexapods
In S. coleoptrata and C. tasmanianus this unpaired neuropil is associated with small lateral lobes
As this study focuses on the organization of deutocerebral neuropils, we will not further consider here, if these neuropils represent an equivalent of the crustacean and hexapod central bodies or the chelicerate arcuate bodies

Summary

Introduction

Originating from a marine ancestor, the myriapods most likely invaded land independently of the hexapods. In arthropod phylogeny the emerging consensus is that Myriapoda are not to be considered the closest relatives of Hexapoda anymore (Tracheata concept), but rather that hexapods constitute a sister group or even an ingroup of Crustacea The position of monophyletic Myriapoda within the Euarthropoda is still under debate and most of the recent phylogenetic studies either place them as sister group to the Tetraconata (Crustacea + Hexapoda) together forming the taxon Mandibulata The Notostigmophora (Scutigeromorpha) (Figure 1A) are the sister group to the Pleurostigmophora which are composed of Lithobiomorpha (Figure 2A) and Phylactometria In the latter taxon, the Craterostigmomorpha (Figure 3A) are the sistergroup to the Epimorpha which are composed of Scolopendromorpha (Figure 4A, G) and Geophilomorpha (Figure 5A) [14]

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