Use of axonal projection patterns for the homologisation of cerebral nerves in Opisthobranchia, Mollusca and Gastropoda

Abstract

IntroductionGastropoda are guided by several sensory organs in the head region, referred to as cephalic sensory organs (CSOs). These CSOs are innervated by distinct nerves. This study proposes a unified terminology for the cerebral nerves and the categories of CSOs and then investigates the neuroanatomy and cellular innervation patterns of these cerebral nerves, in order to homologise them. The homologisation of the cerebral nerves in conjunction with other data, e.g. ontogenetic development or functional morphology, may then provide insights into the homology of the CSOs themselves.ResultsNickel-lysine axonal tracing (“backfilling”) was used to stain the somata projecting into specific nerves in representatives of opisthobranch Gastropoda. Tracing patterns revealed the occurrence, size and relative position of somata and their axons and enabled these somata to be mapped to specific cell clusters. Assignment of cells to clusters followed a conservative approach based primarily on relative location of the cells. Each of the four investigated cerebral nerves could be uniquely identified due to a characteristic set of soma clusters projecting into the respective nerves via their axonal pathways.ConclusionsAs the described tracing patterns are highly conserved morphological characters, they can be used to homologise nerves within the investigated group of gastropods. The combination of adequate number of replicates and a comparative approach allows us to provide preliminary hypotheses on homologies for the cerebral nerves. Based on the hypotheses regarding cerebral nerve homology together with further data on ultrastructure and immunohistochemistry of CSOs published elsewhere, we can propose preliminary hypotheses regarding homology for the CSOs of the Opisthobranchia themselves.

At the limits of a successful body plan - 3D microanatomy, histology and evolution of Helminthope (Mollusca: Heterobranchia: Rhodopemorpha), the most worm-like gastropod

“…[81,83,84]). Their correct identification is regarded as relevant for understanding questions about evolutionary patterns within Heterobranchia and their currently assumed sistergroup, the Caenogastropoda: which nerves are homologous between larger groups, how complex was the ‘ancestral’ pattern, and how did the nerves evolve?…”

Flashback and foreshadowing—a review of the taxon Opisthobranchia

“…Euthyneura s.l. (3) have rhinophores innervated by N3 (nervus rhinophoralis) (Staubach 2008;Klussmann-Kolb et al 2013) and exhibit a euthyneurous nervous system (but with reversals in subgroups) (Brenzinger et al 2013a). Rather than representing a derived branch within the Euthyneuran tree, Nudipleura are in a basal position, suggesting a set of partly plesiomorphic rather than entirely derived character conditions.…”

“…sensu Dinapoli & KlussmannKolb (2010) (see Waren 2013. Numbers indicate putative apomorphies (partly adopted from Dayrat and Tillier 2002;Staubach 2008;Haszprunar et al 2011;Klussmann-Kolb et al 2013;Brenzinger et al 2013a): 1 Hyperstrophy, pallial kidney, hypobranchial gland in anterior position, odontophoral cartilages lacking (or muscular), hermaphroditism, loss of parasperm, sperm spiral-shaped, coarse fibres, intra-axonemal dense granules. 2 Giant neurons in macroscopic (larger) animals.…”

Neuromuscular development in Patellogastropoda (Mollusca: Gastropoda) and its importance for reconstructing ancestral gastropod bodyplan features

“…; Croll and Dickinson ; Klussmann‐Kolb et al. ). Numerous hypotheses and assumptions about ancestral gastropod bodyplan features have been mostly inspired by adult morphology and some developmental observations.…”

“…The colonization of the different habitats has led to the great morphological diversity seen in extant gastropods. The evolutionary origin of the gastropod bodyplan remains a fundamental question in various disciplines of, for instance, morphology, neurobiology, behavioural, and developmental biology (Haszprunar 1988; Van den Biggelaar and Haszprunar 1996;Katz et al 2001;Croll and Dickinson 2004;Klussmann-Kolb et al 2013). Numerous hypotheses and assumptions about ancestral gastropod bodyplan features have been mostly inspired by adult morphology and some developmental observations.…”