Fine structure of mushroom bodies and the brain in Sthenelais boa (Phyllodocida, Annelida)

Abstract

Mushroom bodies are known from annelids and arthropods and were formerly assumed to argue for a close relationship of these two taxa. Since molecular phylogenies univocally show that both taxa belong to two different clades in the bilaterian tree, similarity must either result from convergent evolution or from transformation of an ancestral mushroom body. Any morphological differences in the ultrastructure and composition of mushroom bodies could thus indicate convergent evolution that results from similar functional constraints. We here study the ultrastructure of the mushroom bodies, the glomerular neuropil, glia-cells and the general anatomy of the nervous system in Sthenelais boa. The neuropil of the mushroom bodies is composed of densely packed, small diameter neurites that lack individual or clusterwise glia enwrapping. Neurites of other regions of the brain are much more prominent, are enwrapped by glia-cell processes and thus can be discriminated from the neuropil of the mushroom bodies. The same applies to the respective neuronal somata. The glomerular neuropil of insects and annelids is a region of higher synaptic activity that result in a spheroid appearance of these structures. However, while these structures are sharply delimited from the surrounding neuropil of the brain by glia enwrapping in insects, this is not the case in Sthenelais boa. Although superficially similar, there are anatomical differences in the arrangement of glia-cells in the mushroom bodies and the glomerular neuropil between insects and annelids. Hence, we suppose that the observed differences rather evolved convergently to solve similar functional constrains than by transforming an ancestral mushroom body design.

How Do Prostomial Sensory Organs Affect Brain Anatomy? Phylogenetic Implications in Eunicida (Annelida)

“…Fixation was performed in the refrigerator overnight using Bouin's fixative modified after Dubosque-Basil. The further steps applied follow the standardised methodology described by [33][34][35]. Serial sections (thickness 5 µm) of the animal's prostomium and the peristomium were created using a Reichert-Jung Autocut 2050 microtome (Leica, Wetzlar).…”

“…Already Hanström [12] compared the small and chromatinrich "Ganglienzellen" occurring in high amounts in the anterior region of the brains of Eunice norvegica (Linnaeus, 1767), Hyalinoecia tubicola and Diopatra cuprea (Bosc, 1802), with the cells of the corpora pedunculata. The presence of mushroom body-like structures in polychaete taxa was discussed already in the former literature [12,34,43] and it was pointed out, that mushroom body-like structures may be present in Eunicida [12]. However, the current literature (e.g., [1]) states that mushroom bodies are not present in Eunicida referring to the study of Bullock and Horridge [44].…”

“…Somata of type two and type three neurons generally contain densely arranged endoplasmatic reticula indicating a high metabolic rate [54]. Further, the high abundance of dense and lucent core vesicles in the brain neuropil indicates a high synaptic activity [34]. A high metabolic rate is a prerequisite for processing diverse sensory stimuli and for a predatory lifestyle.…”

Loss of nervous system complexity – Morphological analyses shed light on the neuronal evolution in Myzostomida (Annelida)

“…When compared to the anatomy and ultrastructure of the brain of putatively closely related groups, such as Amphinomida and errant polychaetes, a distinct glial layer surrounding the brain is entirely missing (Beckers et al, 2022; Beckers & Tilic, 2021; Golding, 1992; Purschke, 2016). Radial glia as well as other glial cell processes – components nicely observable in brain neuropils of errant annelid taxa (Beckers et al, 2022) – which often enwrap the neuronal somata, are also missing or could not be observed in our investigations. Furthermore, distinct tracts interconnecting various parts within the brain or a glomerular neuropil are not present in myzostomids.…”

Development and structure of the anterior nervous system and sense organs in the holopelagic annelid Tomopteris spp. (Phyllodocida, Errantia)

“…The situation is much better concerning a comparative perspective on the adult anterior nervous system. Numerous detailed investigations of putatively related errant taxa such as Syllidae (Orrhage, 1996;Schmidbaur et al, 2020), Phyllodocidae (Orrhage & Eibye-Jacobsen, 1998), Sigalionidae (Beckers et al, 2022), Dorvilleidae (Müller & Henning, 2004), and Eunicidae (Zanol, 2010) are available. The adult (anterior) nervous system shares numerous characteristics with other Errantia, including several commissures in the brain and the structure of the innervation of prominent sensory organs such as nuchal organs.…”