Abstract
Aggregation is a social behavior that varies between and within species, providing a model to study the genetic basis of behavioral diversity. In the nematode Caenorhabditis elegans, aggregation is regulated by environmental context and by two neuromodulatory pathways, one dependent on the neuropeptide receptor NPR-1 and one dependent on the TGF-β family protein DAF-7. To gain further insight into the genetic regulation of aggregation, we characterize natural variation underlying behavioral differences between two wild-type C. elegans strains, N2 and CB4856. Using quantitative genetic techniques, including a survey of chromosome substitution strains and QTL analysis of recombinant inbred lines, we identify three new QTLs affecting aggregation in addition to the two known N2 mutations in npr-1 and glb-5. Fine-mapping with near-isogenic lines localized one QTL, accounting for 5%–8% of the behavioral variance between N2 and CB4856, 3′ to the transcript of the GABA neurotransmitter receptor gene exp-1. Quantitative complementation tests demonstrated that this QTL affects exp-1, identifying exp-1 and GABA signaling as new regulators of aggregation. exp-1 interacts genetically with the daf-7 TGF-β pathway, which integrates food availability and population density, and exp-1 mutations affect the level of daf-7 expression. Our results add to growing evidence that genetic variation affecting neurotransmitter receptor genes is a source of natural behavioral variation.
Highlights
Most animal and human behaviors are variable, in part due to genetic variation between individuals
Mapping studies have demonstrated that the genetic component of natural behavioral variation is complex, with many genes that each contribute a small amount to the observed behavior
In the context of previous work, we suggest that a significant number of genes that generate behavioral variation encode neurotransmitter receptors
Summary
Most animal and human behaviors are variable, in part due to genetic variation between individuals. Multiple loci contribute to each behavior, the contribution of each locus is small, and the effect of many individual loci depends on the genotype at other loci and on environmental conditions [1] This genetic complexity poses challenges for the discovery of specific genetic variants that modulate behavior, and only a few genes contributing to natural behavioral diversity have been definitively identified. Animals within a species display different social behaviors based on their sex, developmental stage, reproductive status and environmental conditions [6]. These behaviors are shaped by individual genetic variation that interacts with environmental factors. Genetic variation among Drosophila males affects their territorial aggressive behavior, and this genetic variation interacts with an environmental regulator of aggression, population density [7,8,9]
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