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

• Published in: Proceedings of the National Academy of Sciences - PNAS 2022-07, Vol.119 (28), p.e2122301119-e2122301119
• Main Authors: Orvis, Joshua, Albertin, Caroline B, Shrestha, Pragya, Chen, Shuangshuang, Zheng, Melanie, Rodriguez, Cheyenne J, Tallon, Luke J, Mahurkar, Anup, Zimin, Aleksey V, Kim, Michelle, Liu, Kelvin, Kandel, Eric R, Fraser, Claire M, Sossin, Wayne, Abrams, Thomas W
• Format: Article
• Language: English
• Subjects: Animals; Aplysia; Aplysia - genetics; Aplysia - metabolism; Biological Evolution; Biological Sciences; Circuits; Cognition; Cognitive ability; Evolution; Genes; Genomes; Invertebrates; Isoforms; Molecular modelling; Mollusks; Nervous system; Neuronal Plasticity - genetics; Neurons; Neurons - metabolism; Octopuses; Plasticity; Protein families; Protein Isoforms - genetics; Proteins; Proteome; Proteomes; Scaffolds; Synapses - metabolism; Synaptic plasticity; Transcriptome; Transcriptomes; Vertebrates
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.2122301119

The gastropod mollusk 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 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 (20,000 neurons) and (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 and As expected, a number of synaptic scaffold proteins have more isoforms in humans than in or . 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.