The evolution of synaptic and cognitive capacity: Insights from the nervous system transcriptome of Aplysia

Significance

An influential proposal for the evolution of intelligence in behaviorally sophisticated vertebrates is that increased diversity of synaptic proteins enabled enhanced neural plasticity. We recently completed an improved transcriptome for the nervous system of a simple neurobiological model, the marine mollusk Aplysia. A comparison of proteins that form synaptic scaffolds in Aplysia, in Octopus (a mollusk with an elaborate brain and complex behaviors), and in vertebrates revealed that several families of synaptic scaffold proteins in mollusks are absent in the vertebrate lineage. Despite dramatic differences in cognitive capacity, Octopus and Aplysia have very similar synaptic proteins. This suggests that another factor, such as increases in neural circuit complexity, may be the major contributor to the evolution of intelligence.

Abstract

The gastropod mollusk Aplysia is an important model for cellular and molecular neurobiological studies, particularly for investigations of molecular mechanisms of learning and memory. We developed an optimized assembly pipeline to generate an improved Aplysia nervous system transcriptome. This improved transcriptome enabled us to explore the evolution of cognitive capacity at the molecular level. Were there evolutionary expansions of neuronal genes between this relatively simple gastropod Aplysia (20,000 neurons) and Octopus (500 million neurons), the invertebrate with the most elaborate neuronal circuitry and greatest behavioral complexity? Are the tremendous advances in cognitive power in vertebrates explained by expansion of the synaptic proteome that resulted from multiple rounds of whole genome duplication in this clade? Overall, the complement of genes linked to neuronal function is similar between Octopus and Aplysia. As expected, a number of synaptic scaffold proteins have more isoforms in humans than in Aplysia or Octopus. However, several scaffold families present in mollusks and other protostomes are absent in vertebrates, including the Fifes, Lev10s, SOLs, and a NETO family. Thus, whereas vertebrates have more scaffold isoforms from select families, invertebrates have additional scaffold protein families not found in vertebrates. This analysis provides insights into the evolution of the synaptic proteome. Both synaptic proteins and synaptic plasticity evolved gradually, yet the last deuterostome-protostome common ancestor already possessed an elaborate suite of genes associated with synaptic function, and critical for synaptic plasticity.