Nearly all animals alternate between mating behaviors that allow egg fertilization and reproductive behaviors that drive release of progeny into the environment. As the same organ mediates these two, mutually exclusive behaviors, understanding how females decide when and where to perform each behavior is critical for animal fertility and survival. Work in numerous systems has shown that mating and reproductive behaviors are controlled by diverse chemical signals that shape activity in neural circuits, but the function of physical contact and mechanosensory feedback is less explored. The goal of this research and education program is to identify how such mechanosensory signals regulate reproduction using the roundworm, Caenorhabditis elegans, as a model organism. The principal investigator and his student trainees have shown using cutting-edge imaging techniques that defined cells of the C. elegans female reproductive neural circuit are mechanically activated in sequence during specific steps of mating and egg-laying behaviors. The goal of this project is to determine how each of these cells is mechanically activated and how they signal to drive subsequent behavior steps. The rationale for this work is that understanding the regulation of key signaling events in simple neural circuits will reveal conserved mechanisms in other animals and people. This work will be paired with a new, innovative education program that teaches molecular genetic laboratory techniques through the development of new tools to regulate gene expression and through authentic research projects to study how animals respond to acute changes in pressure and stretch.
This work will identify how mechanosensory feedback modulates cellular signaling events to regulate animal reproductive behaviors. This project will use the roundworm, C. elegans, to test a model that mating and reproductive behaviors proceed via an ordered series of sequential motor steps regulated by three different types of mechanosensory feedback. This feedback activates unique cells which signal through distinct neurotransmitters and receptors to inhibit the prior motor step while activating the next. Objective 1 will determine how the female uv1 neuroendocrine cells are mechanically activated in response to male mating spicule insertion and during egg release. Objective 2 will determine whether the female VC motor neurons are mechanically activated in response to male sperm transfer through the vulva and by muscle contractile activity during vulval opening. Objective 3 will uncover how mechanical stretch of the uterus in response to sperm deposition or egg accumulation re-activates the vulval muscles to terminate mating or to initiate egg release. In each case, the experiments will identify the mechanosensory molecules that mediate cell activation and will determine how the activated cells signal to report the completion of each behavior step. The research is integrated with a new authentic research Molecular Genetics laboratory course where undergraduate students will develop and characterize new Gal4/UAS enhancer trap lines that will facilitate gene and behavior discovery. Together, this work will provide the most detailed model yet for how mechanosensory feedback shapes activity and neurotransmitter signaling in a neural circuit as it executes two mutually exclusive behavior states.
This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.
