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Boston Children's Hospital and Harvard Medical School

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Sci. Adv., Jun 14 2024, 10 (24) | https://doi.org/10.1126/sciadv.adk9481 Genetic variants that modify neuroendocrine gene expression and foraging behavior of C. elegans

Harksun Lee¹, Sonia A. Boor^1,2†, Zoë A. Hilbert^2‡, Joshua D. Meisel^2§, Jaeseok Park¹, Ye Wang^3¶, Ryan McKeown³, Sylvia E. J. Fischer^1,4, Erik C. Andersen⁵, Dennis H. Kim^1*

¹Division of infectious diseases, department of Pediatrics, Boston children’s hospital and harvard Medical School, Boston, MA 02115, USA.

²Department of Biology, Massachusetts institute of technology, cambridge, MA 02139, USA.

³Department of Molecular Biosciences, northwestern University, evanston, IL 60208, USA.

⁴Harvard Medical School initiative for RnA Medicine, Boston, MA 02115, USA.

⁵Department of Biology, Johns hopkins University, Baltimore, Md 21212, USA.

^*corresponding author: Dennis H. Kim

^†Present address: Whitehead institute for Biomedical Research and department of Biology, Massachusetts institute of technology, cambridge, MA 02139 USA.

^‡Present address: department of Biology, Boston college, chestnut hill, MA 02467 USA.

^§Present address: department of Molecular Biology, Massachusetts General hospital, Boston, MA 02114, USA.

^¶Present address: chengdu Research Base of Giant Panda Breeding, chengdu 610016, china.

Abstract

The molecular mechanisms underlying diversity in animal behavior are not well understood. A major experimental challenge is determining the contribution of genetic variants that affect neuronal gene expression to differences in behavioral traits. In Caenorhabditis elegans, the neuroendocrine transforming growth factor-β ligand, DAF-7, regulates diverse behavioral responses to bacterial food and pathogens. The dynamic neuron-specific expression of daf-7 is modulated by environmental and endogenous bacteria-derived cues. Here, we investigated natural variation in the expression of daf-7 from the ASJ pair of chemosensory neurons. We identified common genetic variants in gap-2, encoding a Ras guanosine triphosphatase (GTPase)-activating protein homologous to mammalian synaptic Ras GTPase-activating protein, which modify daf-7 expression cell nonautonomously and promote exploratory foraging behavior in a partially DAF-7-dependent manner. Our data connect natural variation in neuron-specific gene expression to differences in behavior and suggest that genetic variation in neuroendocrine signaling pathways mediating host-microbe interactions may give rise to diversity in animal behavior.

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