Genetics of sexually motivated behavior in Caenorhabditis elegans
Lipton, Jonathan Oren
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Neural states called drives serve to stimulate essential species-specific motivated behaviors such as foraging, or mate searching. The expression of motivated behaviors occurs along a probabilistic continuum mediated by the monitoring of physiologically-determined drive states with environmental stimuli. Little is known about the genetic or neural architecture of drive states. Here, a C. elegans model is described that has enabled the characterization of both the environmental conditions and genetic factors that underlie the expression of a sexually motivated behavior.;C. elegans males cultured on a food source in the absence of hermaphrodite mating partners stochastically and spontaneously wander away from the food source, a behavior termed "leaving behavior." In contrast, self-fertile hermaphrodites rarely, if ever, wander away from food. Leaving behavior is completely abrogated by the presence of hermaphrodites but not by the presence of other males and thus may represent a mate-searching behavioral adaptation. The expression of leaving behavior is regulated by both the presence of food and the nutritional status of the animal. Anatomical and genetic analysis revealed that reproductive system signals play a pivotal role in the regulation of leaving behavior in both sexes. Somatic gonad signals are wholly accountable for the sexual dimorphism in the probability of expression of leaving behavior. Mutations affecting a serotonergic pathway also exhibit defects in male leaving behavior.;To gain insight into the genetic regulation of leaving behavior, a screen was performed for mutants that move and mate well but do not leave food with normal probability. Three recessive mutations falling into three complementation groups were isolated. One mutant, mod-5(bx121), harbors a mutation in a single conserved residue of the C. elegans serotonin reuptake transporter (CeSERT). SERT has been implicated in the control of sexual motivation in vertebrates, including humans. A second mutant, unc-77(bx122), results in the extension of hermaphrodite reproductive lifespan without affecting the overall lifespan of the population in addition to its leaving defective phenotype in males. Genetic analysis shows that unc-77 is epistatic to the daf-16 forkhead-like transcription factor in the control of reproductive schedule. A third mutant, las-1(bx117) has no discernible phenotype other than a defect in male leaving behavior. These data point to multiple pathways that govern the probability of expressing leaving behavior.;Finally, behavioral evidence is presented for a short-range sex attractant in C. elegans. Analysis of a leaving constitutive mutant, cod-16(bx72), demonstrates that distinct signals are used during different phases of sexual communication.;Mate-searching behavior in C. elegans shares both physiological and molecular similarity with sexually motivated behavior in vertebrates revealing that the control of appetitive behavior may be highly conserved across widely divergent phyla. Thus, the model for motivated sexual behavior presented here may have both biological and clinical relevance to an understanding of behavior in higher animals.