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

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Abstract
The gastropod molluskAplysiais 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 improvedAplysianervous 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 gastropodAplysia(20,000 neurons) andOctopus(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 betweenOctopusandAplysia.As expected, a number of synaptic scaffold proteins have more isoforms in humans than inAplysiaorOctopus. 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.
Funding Information
  • Howard Hughes Medical Institute (n/a)
  • National Science Foundation (IOS-1255695)
  • HHS | National Institutes of Health (R01 MH 55880)

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