Voltage-gated ion channel diversity underlies neuronal excitability and nervous system evolution

Nervous systems function via electrical excitability mediated by ion channels, an ancient preneuronal feature that many cells use to rapidly adjust behavior. Here, we systematically study the evolutionary paths to neuronal excitability by characterizing the voltage-gated ion channel complements (VGL-chanomes) of 623 organisms, dissecting their expression in 11 whole-body cell atlases and 3 entire nervous systems, and recording electrical properties of cnidarian neurons in Nematostella. We find a disconnect between ion channel availability and nervous system complexity and instead find an association with lifestyle and behavior. Cell-type restricted VGL-chanome expression predated the emergence of nervous systems, and multiple gene-family expansions and contractions have led to a surprising pattern: it is not the number of ion channels, but rather their diversity and restrictive recruitment that is a hallmark of neuronal complexity. These findings suggest that the evolution of complex nervous systems was not a stepwise progression of expanding complexity but a convergent path to diversity.