Abstract
How to respond to starvation determines fitness. One prominent behavioral response is increased locomotor activities upon starvation, also known as Starvation-Induced Hyperactivity (SIH). SIH is paradoxical as it promotes food seeking but also increases energy expenditure. Despite its importance in fitness, the genetic contributions to SIH as a behavioral trait remains unexplored. Here, we examined SIH in the Drosophila melanogaster Genetic Reference Panel (DGRP) and performed genome-wide association studies. We identified 23 significant loci, corresponding to 14 genes, significantly associated with SIH in adult Drosophila. Gene enrichment analyses indicated that genes encoding ion channels and mRNA binding proteins (RBPs) were most enriched in SIH. We are especially interested in RBPs because they provide a potential mechanism to quickly change protein expression in response to environmental challenges. Using RNA interference, we validated the role of syp in regulating SIH. syp encodes Syncrip (Syp), an RBP. While ubiquitous knockdown of syp led to semi-lethality in adult flies, adult flies with neuron-specific syp knockdown were viable and exhibited decreased SIH. Using the Temporal and Regional Gene Expression Targeting (TARGET) system, we further confirmed the role of Syp in adult neurons in regulating SIH. To determine how syp is regulated by starvation, we performed RNA-seq using the heads of flies maintained under either food or starvation conditions. RNA-seq analyses revealed that syp was alternatively spliced under starvation while its expression level was unchanged. We further generated an alternatively-spliced-exon-specific knockout (KO) line and found that KO flies showed reduced SIH. Together, this study demonstrates a significant genetic contribution to SIH as a behavioral trait, identifies syp as a SIH gene, and highlights the significance of RBPs and post-transcriptional processes in the brain in regulating behavioral responses to starvation.
Highlights
Animals living in the natural environment often experience periods of starvation, and they have developed different physiological and behavioral strategies to respond to starvation [1, 2]
Our results show that there is a significant genetic contribution to Starvation-Induced Hyperactivity (SIH) in this population, and that genes encoding RNA binding proteins (RBPs) are especially important
Using RNA interference and the TARGET system, we confirmed the role of an RBP Syp in adult neurons in SIH
Summary
Animals living in the natural environment often experience periods of starvation, and they have developed different physiological and behavioral strategies to respond to starvation [1, 2]. One well-documented behavioral response is Starvation-Induced Hyperactivity (SIH), that is, animals will increase their locomotor activity upon starvation [3]. From the viewpoint of energy gain and expenditure, SIH seems paradoxical. On one hand, it facilitates food acquisition and energy intake when food is available [7]; on the other hand, it increases energy expenditure and makes starved animals even more vulnerable when food is not available [4]. Genetic dispositions to either too much or too little SIH would impair fitness depending on the environment. The genetic contributions to SIH as a behavioral trait remains unexplored
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