Trade-off between toxicity and signal detection orchestrated by frequency- and density-dependent genes

• Published in: PloS one 2011-05, Vol.6 (5), p.e19805-e19805
• Main Authors: Arthaud, Laury, Rokia-Mille, Selim Ben, Raad, Hussein, Dombrovsky, Aviv, Prevost, Nicolas, Capovilla, Maria, Robichon, Alain
• Format: Article
• Language: English
• Subjects: Aldehyde Dehydrogenase - genetics; Aldehyde Dehydrogenase - metabolism; Aldehydes; Animal behavior; Animals; Animals, Genetically Modified; Bayesian analysis; Behavior, Animal; Biology; Cells, Cultured; Chemistry; Cognitive Sciences; Colonization; Cyclic GMP; Cyclic GMP-Dependent Protein Kinases - genetics; Cyclic GMP-Dependent Protein Kinases - metabolism; Dehydrogenases; Deprivation; Dietary restrictions; Dispersion; Drosophila; Drosophila melanogaster; Drosophila melanogaster - genetics; Ecological niches; Environment; Enzymes; Epigenetics; Exploration; Forage; Forages; Foraging behavior; Frequency dependence; Gene expression; Gene frequency; Genes; Genes, Insect; Genetic aspects; Genetic engineering; Genomes; Genotype; Insects; Isoforms; Kinases; Life Sciences; Metabolism; Neurogenesis; Neurons and Cognition; Niches; Odorants; Odors; Optimal foraging; Oxidation; Population density; Protein kinase; Protein kinase G; Protein kinases; Proteins; Signal detection; Toxicity; Transgenes - physiology; Volatile compounds
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0019805

Behaviors in insects are partly highly efficient Bayesian processes that fulfill exploratory tasks ending with the colonization of new ecological niches. The foraging (for) gene in Drosophila encodes a cGMP-dependent protein kinase (PKG). It has been extensively described as a frequency-dependent gene and its transcripts are differentially expressed between individuals, reflecting the population density context. Some for transcripts, when expressed in a population at high density for many generations, concomitantly trigger strong dispersive behavior associated with foraging activity. Moreover, genotype-by-environment interaction (GEI) analysis has highlighted a dormant role of for in energetic metabolism in a food deprivation context. In our current report, we show that alleles of for encoding different cGMP-dependent kinase isoforms influence the oxidation of aldehyde groups of aromatic molecules emitted by plants via Aldh-III and a phosphorylatable adaptor. The enhanced efficiency of oxidation of aldehyde odorants into carboxyl groups by the action of for lessens their action and toxicity, which should facilitate exploration and guidance in a complex odor environment. Our present data provide evidence that optimal foraging performance requires the fast metabolism of volatile compounds emitted by plants to avoid neurosensory saturation and that the frequency-dependent genes that trigger dispersion influence these processes.