Comparative neuroanatomy of Caudofoveata, Solenogastres, Polyplacophora, and Scaphopoda (Mollusca) and its phylogenetic implications

Abstract

The nervous system of invertebrates is considered to be a very conservative organ system and thus can be helpful to elucidate questions of phylogenetic relationships. Up to now, comparative neuroanatomical studies have been mainly focused on arthropods, where in-depth studies on major brain structures are abundant. In contrast, except for Gastropoda and Cephalopoda, the nervous system of representatives of the second largest phylum of invertebrates, the Mollusca, is as yet hardly investigated. We therefore initiated an immunohistochemical survey to contribute new neuroanatomical data for several molluscan taxa, especially the lesser known Caudofoveata, Solenogastres, Polyplacophora, and Scaphopoda, focusing on the cellular architecture and distribution of neurotransmitters in the brain. Antisera against the widespread neuroactive substances FMRFamide and serotonin were used to label subsets of neurons. Both antisera were additionally used in combination with acetylated -tubulin and the nuclear marker DAPI. This enables us to describe the morphology of the nervous system at a Wne resolution and to compare its cellular architecture between diVerent species of one taxon, as well as between diVerent taxa of mollusks. On the basis of these results, the nervous system of caudofoveates seems to be most highly derived within the so-called basal (non-conchiferan) mollusks, and a monophyly of a clade Aplacophora could not be conWrmed. In general, the brain as well as the remaining nervous system of the molluscan taxa investigated shows a great variability, suggesting a deep time origin of the diversiWcation of this prominent protostome clade.

The Testaria concept (Polyplacophora + Conchifera) updated

“…There is no synapomorphy of a 'ganglionated nervous system' in the aplacophoran groups; rather the four nerve cords in Caudofoveata are generally medullary and in Solenogastres they show serial swellings along with regular to scattered perikarya (Salvini-Plawen 1978;Todt et al 2008a;Redl and Salvini-Plawen 2009;Faller et al 2012). This gives evidence that the plesiomorphic amphineury for all Aculifera (and Mollusca) subsequently differentiated separately within the two aplacophoran clades.…”

“…The 'worm shape' in the Recent aplacophoran groups cannot be considered a synapomorphy of the two classes and their monophyly cannot be supported (Haszprunar 2000;Faller et al 2012). In Solenogastres there is a narrowing of the entire body with retention of the ciliary-gliding foot as a pedal groove.…”

“…This gives evidence that the plesiomorphic amphineury for all Aculifera (and Mollusca) subsequently differentiated separately within the two aplacophoran clades. The terminal section of the lateral nervous system in Aculifera shows (in most cases) a medullary suprarectal commissure (Faller et al 2012), which innervates the ctenidia and the paired terminal/osphradial sense organ(s) (Salvini-Plawen 1972Haszprunar 1987a). It appears that the subrectal position of the commissure in Conchifera is correlated to the differentiation of the uniform shell and that the aculiferan situation with suprarectal commissure most likely reflects a plesiomorphy.…”

A new sensory organ in “primitive” molluscs (Polyplacophora: Lepidopleurida), and its context in the nervous system of chitons

“…Tomographic visualisation of the anterior nervous system of lepidopleuran chitons reveals a strikingly large and well-developed neural mass (brain) that is at odds with previous reports for the neuroanatomy of the group [4,5,59]. A fundamental assumption that chitons are “primitive” among Mollusca may have biased the interpretation of anatomical results by early, and even some contemporary researchers.…”

“…Other authors recognised subradular ganglia and/or buccal ganglia [4,28], but stated that polyplacophorans lack a distinct ganglionic brain [4]. …”