Abstract
We leverage two complementary Drosophila melanogaster mapping panels to genetically dissect starvation resistance-an important fitness trait. Using >1600 genotypes from the multiparental Drosophila Synthetic Population Resource (DSPR), we map numerous starvation stress QTL that collectively explain a substantial fraction of trait heritability. Mapped QTL effects allowed us to estimate DSPR founder phenotypes, predictions that were correlated with the actual phenotypes of these lines. We observe a modest phenotypic correlation between starvation resistance and triglyceride level, traits that have been linked in previous studies. However, overlap among QTL identified for each trait is low. Since we also show that DSPR strains with extreme starvation phenotypes differ in desiccation resistance and activity level, our data imply multiple physiological mechanisms contribute to starvation variability. We additionally exploited the Drosophila Genetic Reference Panel (DGRP) to identify sequence variants associated with starvation resistance. Consistent with prior work these sites rarely fall within QTL intervals mapped in the DSPR. We were offered a unique opportunity to directly compare association mapping results across laboratories since two other groups previously measured starvation resistance in the DGRP. We found strong phenotypic correlations among studies, but extremely low overlap in the sets of genomewide significant sites. Despite this, our analyses revealed that the most highly associated variants from each study typically showed the same additive effect sign in independent studies, in contrast to otherwise equivalent sets of random variants. This consistency provides evidence for reproducible trait-associated sites in a widely used mapping panel, and highlights the polygenic nature of starvation resistance.
Highlights
Since starvation resistance is sensitive to the thermal environment, and may vary under different photoperiods (Sheeba et al 2000; Xu et al 2008; Seay and Thummel 2011), we sought to remeasure starvation resistance for a subset of Drosophila Synthetic Population Resource (DSPR) recombinant inbred lines (RILs) at 25° and with a 12 hr/12 hr light/dark cycle—conditions that have been used in other starvation studies (e.g., Mackay et al 2012; Everman and Morgan 2018)
The DSPR and Drosophila Genetic Reference Panel (DGRP) panels have the advantage of increased, stable genetic diversity, and provide a unique comparison to many previous quantitative genetic studies of starvation resistance that may be limited by genetic diversity or mapping power
Correlations between starvation resistance and the additional traits described in this study offer insight into the genetic control of related stress response traits, and provide support for the hypothesis that the genetic architecture of stress traits varies by population and is dependent upon sex, environment, and the evolutionary history of the populations studied
Summary
PERIODS of food scarcity and suboptimal nutrient resources present an important challenge for most species (McCue 2010), and this form of environmental stress can limit the survival of individuals with poor nutritional status and reduced stress resistance (Harshman et al 1999; Lee and Jang 2014). Several studies have examined the genetic basis of starvation resistance in D. melanogaster using a combination of selection experiments (Rose et al 1992; Chippindale et al 1996; Harshman et al 1999; Bochdanovits and de Jong 2003; Bubliy and Loeschcke 2005; Schwasinger-Schmidt et al 2012; Hardy et al 2018; Michalak et al 2018), gene expression studies following exposure to starvation stress (Harbison et al 2005; Sørensen et al 2007), and genetic mapping (Harbison et al 2004; Mackay et al 2012; Huang et al 2014; Everman and Morgan 2018) These studies have provided extensive lists of candidate genes and variants, some of which have been functionally validated (Lin et al 1998; Clancy et al 2001; Harbison et al 2004, 2005; Sørensen et al 2007). Doing so would allow a detailed comparison of quantitative trait loci (QTL) that contribute to variation in each trait, provide insight into the similarity of the genetic architectures of starvation resistance and correlated traits, and facilitate a better understanding of their evolution, and the mechanisms underlying their variation
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