Evolution of highly diverse forms of behavior in molluscs

Abstract

Members of the phylum Mollusca demonstrate the animal kingdom's tremendous diversity of body morphology, size and complexity of the nervous system, as well as diversity of behavioral repertoires, ranging from very simple to highly flexible. Molluscs include Solenogastres, with their worm-like bodies and behavior (see phylogenetic tree; Figure 1); Bivalvia (mussels and clams), protected by shells and practically immobile; and the cephalopods, such as the octopus, cuttlefish and squid. The latter are strange-looking animals with nervous systems comprising up to half a billion neurons, which mediate the complex behaviors that characterize these freely moving, highly visual predators. Molluscs are undoubtedly special - their extraordinary evolutionary advance somehow managed to sidestep the acquisition of the rigid skeleton that appears essential to the evolution of other 'successful' phyla: the exoskeleton in ecdysozoan invertebrates and the internal skeleton in Deuterostomia, including vertebrates.

Figure 1. Diversity among molluscan nervous systems

The extreme diversity of molluscan nervous systems shown in relation to their position in the phylogenetic tree (taken from Stögere et al., 2013). The examples illustrate similarities among different groups, as well as the differences within the same group (see text). The derivatives of the pedal ganglia are shown in red, the components of the pleural-parietal ganglia are shown in green, and the cerebral ganglia are uncolored (Figures adapted from Bullock & Horridge 1965, except Octopus brain, which is taken from Brusca & Brusca 1990) with permission of Sinauer Associates..

Figure 2. The neural bases of Molluscan behavioral diversity

Network schemes showing the correlation between the level of complexity of molluscan behaviors and the number of sensory modalities involved in the behaviors (see text). The examples range from a simple defensive reflex (Network A) to the associative learning and memory network of the octopus (Network F). The neurons are schematized as a typical invertebrate monopolar neuron.

Figure 3. Wiring diagrams for a simple and a complex learning and memory network

The network organization of the defensive withdrawal reflex of Aplysia (A) and the associative learning and memory network of the Octopus vertical lobe (B). The vertical lobe comprises a ‘fan-out fan-in’ pattern of neural connectivity, which is also characteristic of the insect mushroom body and of an artificial machine learning classifier. VL, vertical lobe; SFL, superior frontal lobe; SFLn, superior frontal lobe neuron; AM, amacrine interneurons; LN, large efferent neuron; Ach, acetylcholine; Glut, glutamate.