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

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.

Complex brain and optic lobes in an early Cambrian arthropod

“…The brain of Fuxianhuia is thus tripartite, as are brains of Malacostraca 18 , Chilopoda 19 and Insecta 20 , but not those of Branchiopoda, in which the tritocerebral ganglion is separate from the deutocerebrum and situated post-orally 21 . Likewise, the indication of three nested optic neuropils in Fuxianhuia (Fig.…”

“…It is not possible to ascertain whether the entire tritocerebral ganglion lies in front of the stomodeum or whether, as in many extant pancrustaceans, the tritocerebrum is penetrated by the stomodeum, with one part of it pre-stomodeal and the other part poststomodeal. In other mandibulate arthropods, such as centipedes, the tritocerebrum flanks the gut, but its neuropil is contiguous with, not separate from, the deutocerebrum 19 . In no taxon is the tritocerebrum wholly pre-oral: in cases where the entire tritocerebrum appears to lie forward of the gut, there is still one bundle of post-stomodeal axons that connects both sides of the tritocerebrum 20 .…”

Arthropod eyes: The early Cambrian fossil record and divergent evolution of visual systems

“…Observations of both diplopod and chilopod brains also suggest a ground pattern organization that is simpler than observed in any pancrustacean other than Branchiopoda and pelagic Malacostraca that have undergone secondary loss of visual and mid-brain centers (Strausfeld and Andrew, 2011;Strausfeld, 2012). That myriapods possess homoplasies with insects is underlined by their possessing a single pair of antennae and glomerular antennal lobes (Sombke et al, 2012), but an entirely different suite of genes encodes the chilopod olfactory receptors (Chipman et al, 2014).…”

Immunolocalization of histamine in the optic neuropils of Scutigera coleoptrata (Myriapoda: Chilopoda) reveals the basal organization of visual systems in Mandibulata

“…Myriapods play a crucial role in considerations of evolutionary transformations of arthropod nervous systems [8,[28][29][30][31]. Therefore, we wanted to gain deeper insights into the identity of the two optic neuropils in Chilopoda in order to resolve the above mentioned discrepancies.…”