The sleeping beauty: how reproductive diapause affects hormone signaling, metabolism, immune response and somatic maintenance in Drosophila melanogaster

PLoS One. 2014 Nov 13;9(11):e113051. doi: 10.1371/journal.pone.0113051. eCollection 2014.

Abstract

Some organisms can adapt to seasonal and other environmental challenges by entering a state of dormancy, diapause. Thus, insects exposed to decreased temperature and short photoperiod enter a state of arrested development, lowered metabolism, and increased stress resistance. Drosophila melanogaster females can enter a shallow reproductive diapause in the adult stage, which drastically reduces organismal senescence, but little is known about the physiology and endocrinology associated with this dormancy, and the genes involved in its regulation. We induced diapause in D. melanogaster and monitored effects over 12 weeks on dynamics of ovary development, carbohydrate and lipid metabolism, as well as expression of genes involved in endocrine signaling, metabolism and innate immunity. During diapause food intake diminishes drastically, but circulating and stored carbohydrates and lipids are elevated. Gene transcripts of glucagon- and insulin-like peptides increase, and expression of several target genes of these peptides also change. Four key genes in innate immunity can be induced by infection in diapausing flies, and two of these, drosomycin and cecropin A1, are upregulated by diapause independently of infection. Diapausing flies display very low mortality, extended lifespan and decreased aging of the intestinal epithelium. Many phenotypes induced by diapause are reversed after one week of recovery from diapause conditions. Furthermore, mutant flies lacking specific insulin-like peptides (dilp5 and dilp2-3) display increased diapause incidence. Our study provides a first comprehensive characterization of reproductive diapause in D. melanogaster, and evidence that glucagon- and insulin-like signaling are among the key regulators of the altered physiology during this dormancy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Diapause, Insect / physiology*
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster
  • Female
  • Insulins / metabolism*
  • Ovary / physiology*
  • Signal Transduction / physiology*
  • Time Factors

Substances

  • Drosophila Proteins
  • Ilp5 protein, Drosophila
  • Insulins

Grant support

The work was supported by the following: Swedish Research Council (projects VR-2012-3715, VR-2010-5988 and VR-2010-5742) to D.R.N., U.T. and Sören Nylin, http://www.vr.se/inenglish.4.12fff4451215cbd83e4800015152.html; The Knut and Alice Wallenberg Foundation (KAW2012.0058; Sören Nylin), https://www.wallenberg.com/kaw/en; Swedish Foundation for International Cooperation in Research and Higher Education (IG2011-2042) to U.T., http://www.stint.se/en/; and The Swedish Institute (Visby Program: 00197/2012) to O.I.K., https://eng.si.se/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.