Developmental history modulates adult olfactory behavioral preferences via regulation of chemoreceptor expression in Caenorhabditiselegans

Developmental experiences play critical roles in shaping adult physiology and behavior. We and others previously showed that adult Caenorhabditiselegans which transiently experienced dauer arrest during development (postdauer) exhibit distinct gene expression profiles as compared to control adults which bypassed the dauer stage. In particular, the expression patterns of subsets of chemoreceptor genes are markedly altered in postdauer adults. Whether altered chemoreceptor levels drive behavioral plasticity in postdauer adults is unknown. Here, we show that postdauer adults exhibit enhanced attraction to a panel of food-related attractive volatile odorants including the bacterially produced chemical diacetyl. Diacetyl-evoked responses in the AWA olfactory neuron pair are increased in both dauer larvae and postdauer adults, and we find that these increased responses are correlated with upregulation of the diacetyl receptor ODR-10 in AWA likely via both transcriptional and posttranscriptional mechanisms. We show that transcriptional upregulation of odr-10 expression in dauer larvae is in part mediated by the DAF-16 FOXO transcription factor. Via transcriptional profiling of sorted populations of AWA neurons from control and postdauer animals, we further show that the expression of a subset of additional chemoreceptor genes in AWA is regulated similarly to odr-10 in postdauer animals. Our results suggest that developmental experiences may be encoded at the level of olfactory receptor regulation, and provide a simple mechanism by which C. elegans is able to precisely modulate its behavioral preferences as a function of its current and past experiences.

Automated summary

Developmental experiences play a critical role in shaping adult physiology and behavior. In the nematode Caenorhabditis elegans, transient dauer arrest during development affects gene expression profiles and chemoreceptor levels, leading to altered behavioral preferences in adult worms. Specifically, postdauer adults exhibit enhanced attraction to food-related attractive odorants, which is correlated with the upregulation of the diacetyl receptor ODR-10. This study suggests that developmental experiences can be encoded at the level of olfactory receptor regulation, allowing C. elegans to modulate its behavioral preferences based on current and past experiences.