Abstract
Animals have evolved a variety of behaviors to cope with adverse environmental conditions. Similar to other insects, the fly, Drosophila melanogaster, responds to sustained cold by reducing its metabolic rate and arresting its reproduction. Here, we show that a subset of dorsal neurons (DN3s) that express the neuropeptide allatostatin C (AstC) facilitates recovery from cold-induced reproductive dormancy. The activity of AstC-expressing DN3s, as well as AstC peptide levels, are suppressed by cold. Cold temperature also impacts AstC levels in other Drosophila species and mosquitoes, Aedes aegypti, and Anopheles stephensi. The stimulatory effect of AstC on egg production is mediated by cholinergic AstC-R2 neurons. Our results demonstrate that DN3s coordinate female reproductive capacity with environmental temperature via AstC signaling. AstC/AstC-R2 is conserved across many insect species and their role in regulating female reproductive capacity makes them an ideal target for controlling the population of agricultural pests and human disease vectors.
| Original language | English (US) |
|---|---|
| Pages (from-to) | 1362-1375.e8 |
| Journal | Current Biology |
| Volume | 32 |
| Issue number | 6 |
| DOIs | |
| State | Published - Mar 28 2022 |
Funding
We thank Dr. David Deitcher, Dr. Joe Fetcho, Dr. Mariana Wolfner, and the Yapici Lab for comments on the manuscript; Dr. Laura Harrington and Dr. Alexandra Amaro for their assistance in mosquito experiments; Dr. Qiaoran Li, Dr. Young-Joon Kim, Dr. Naoki Yamanaka, Dr. Michael Young, Dr. Benjamin White, Dr. Michael Reiser, and Dr. Andreu Casali for fly stocks; Dr. Laura Harrington for Ae. aegypti; and Dr. Courtney Murdock for An. stephensi mosquito strains. We acknowledge Bloomington Stock Center ( NIH P40OD018537 ) and the Developmental Studies Hybridoma Bank (NICHD of the NIH, University of Iowa) for reagents. Research in N.Y.’s laboratory is supported by NIH -R21 ( R21AI149772 ) and NIH R35-MIRA ( R35GM133698 ). We thank Dr. David Deitcher, Dr. Joe Fetcho, Dr. Mariana Wolfner, and the Yapici Lab for comments on the manuscript; Dr. Laura Harrington and Dr. Alexandra Amaro for their assistance in mosquito experiments; Dr. Qiaoran Li, Dr. Young-Joon Kim, Dr. Naoki Yamanaka, Dr. Michael Young, Dr. Benjamin White, Dr. Michael Reiser, and Dr. Andreu Casali for fly stocks; Dr. Laura Harrington for Ae. aegypti; and Dr. Courtney Murdock for An. stephensi mosquito strains. We acknowledge Bloomington Stock Center (NIH P40OD018537) and the Developmental Studies Hybridoma Bank (NICHD of the NIH, University of Iowa) for reagents. Research in N.Y.?s laboratory is supported by NIH-R21 (R21AI149772) and NIH R35-MIRA (R35GM133698). N.Y. and M.R.M. conceived the project and designed all the experiments. M.R.M. carried out and analyzed all the experiments except the electrophysiology recordings in Figure 4 and the two-photon imaging experiments in Figure 6. I.G. helped with experiments in Figure 1. J.S. built the chamber in Figure 1. M.G. and M.H.A. designed the experiments in Figure 4, which were then carried out and analyzed by M.H.A. X.C. carried out and analyzed the experiments in Figure 5. N.Y. and M.R.M. interpreted the results and wrote the paper with feedback from all authors. The authors declare no competing interests.
Keywords
- dormancy, cold-sensing, reproduction, flies, mosquitoes, neural circuits, neuropeptides
ASJC Scopus subject areas
- General Biochemistry, Genetics and Molecular Biology
- General Agricultural and Biological Sciences
