Abstract
SummaryThe extent to which behavior is shaped by experience varies between individuals. Genetic differences contribute to this variation, but the neural mechanisms are not understood. Here, we dissect natural variation in the behavioral flexibility of two Caenorhabditis elegans wild strains. In one strain, a memory of exposure to 21% O2 suppresses CO2-evoked locomotory arousal; in the other, CO2 evokes arousal regardless of previous O2 experience. We map that variation to a polymorphic dendritic scaffold protein, ARCP-1, expressed in sensory neurons. ARCP-1 binds the Ca2+-dependent phosphodiesterase PDE-1 and co-localizes PDE-1 with molecular sensors for CO2 at dendritic ends. Reducing ARCP-1 or PDE-1 activity promotes CO2 escape by altering neuropeptide expression in the BAG CO2 sensors. Variation in ARCP-1 alters behavioral plasticity in multiple paradigms. Our findings are reminiscent of genetic accommodation, an evolutionary process by which phenotypic flexibility in response to environmental variation is reset by genetic change.
Highlights
Animals reconfigure their behavior and physiology in response to experience, and many studies highlight mechanisms underlying such plasticity (Bargmann, 2012; Owen and Brenner, 2012)
Studies of genetic assimilation led to the broader concept of genetic accommodation, referring to evolutionary genetic variation leading to any change in the environmental regulation of a phenotype (Crispo, 2007; West-Eberhard, 2005)
By characterizing differences between C. elegans isolates, we identify a polymorphism in a dendritic ankyrin-repeat scaffold protein, ARCP-1, that alters plasticity in one strain
Summary
Animals reconfigure their behavior and physiology in response to experience, and many studies highlight mechanisms underlying such plasticity (Bargmann, 2012; Owen and Brenner, 2012). Waddington and Schmalhausen suggested genetic assimilation occurs when a phenotype initially responsive to the environment becomes fixed in a specific state (Renn and Schumer, 2013; Schmalhausen, 1949; Waddington, 1942, 1953). This loss of plasticity may reflect genetic drift or selection against the costs of expressing adaptive behaviors (Niemela€ et al, 2013). Fish, rodents, and primates highlight inter-individual variation in behavioral plasticity; in some cases this has been shown to be heritable (Dingemanse and Wolf, 2013; Izquierdo et al, 2007; Mery et al, 2007), but the mechanisms responsible for these differences remain enigmatic
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