Fine-Scale Mapping of Natural Variation in Fly Fecundity Identifies Neuronal Domain of Expression and Function of an Aquaporin

Abstract

<div><p>To gain insight into the molecular genetic basis of standing variation in fitness related traits, we identify a novel factor that regulates the molecular and physiological basis of natural variation in female <em>Drosophila melanogaster</em> fecundity. Genetic variation in female fecundity in flies derived from a wild orchard population is heritable and largely independent of other measured life history traits. We map a portion of this variation to a single QTL and then use deficiency mapping to further refine this QTL to 5 candidate genes. Ubiquitous expression of RNAi against only one of these genes, an aquaporin encoded by <em>Drip</em>, reduces fecundity. Within our mapping population <em>Drip</em> mRNA level in the head, but not other tissues, is positively correlated with fecundity. We localize <em>Drip</em> expression to a small population of corazonin producing neurons located in the dorsolateral posterior compartments of the protocerebrum. Expression of <em>Drip</em>–RNAi using both the pan-neuronal <em>ELAV</em>-<em>Gal4</em> and the <em>Crz-Gal4</em> drivers reduces fecundity. Low-fecundity RILs have decreased <em>Crz</em> expression and increased expression of <em>pale</em>, the enzyme encoding the rate-limiting step in the production of dopamine, a modulator of insect life histories. Taken together these data suggest that natural variation in <em>Drip</em> expression in the corazonin producing neurons contributes to standing variation in fitness by altering the concentration of two neurohormones.</p> </div