Abstract
How dietary selection affects genome evolution to define the optimal range of nutrient intake is a poorly understood question with medical relevance. We have addressed this question by analyzing Drosophila simulans and sechellia, recently diverged species with differential diet choice. D. sechellia larvae, specialized to a nutrient scarce diet, did not survive on sugar-rich conditions, while the generalist species D. simulans was sugar tolerant. Sugar tolerance in D. simulans was a tradeoff for performance on low-energy diet and was associated with global reprogramming of metabolic gene expression. Hybridization and phenotype-based introgression revealed the genomic regions of D. simulans that were sufficient for sugar tolerance. These regions included genes that are involved in mitochondrial ribosome biogenesis and intracellular signaling, such as PPP1R15/Gadd34 and SERCA, which contributed to sugar tolerance. In conclusion, genomic variation affecting genes involved in global metabolic control defines the optimal range for dietary macronutrient composition.
Highlights
Animals require macronutrients to sustain growth, reproduction and repair over their lifetimes and the balance between nutrients has been shown to have significant effects on development, reproduction and longevity (Raubenheimer and Simpson, 1997; Lee et al, 2008; Arganda et al, 2017)
Related Drosophila species have differential macronutrient spaces Because the natural larval diet of the generalist species D. simulans may have a highly variable sugar content compared to that of the specialist species D. sechellia, we predicted that egg to pupa development time of these species would be dissociated along the sugar axis in a yeast  sugar macronutrient space
Larval development time was negatively correlated and survival was positively correlated with dietary yeast concentration; the correlation was weaker for D. sechellia than for D. simulans (Table 1)
Summary
Animals require macronutrients to sustain growth, reproduction and repair over their lifetimes and the balance between nutrients has been shown to have significant effects on development, reproduction and longevity (Raubenheimer and Simpson, 1997; Lee et al, 2008; Arganda et al, 2017). Some closely related species are distinguished by variation in morphological structures that are specialized for obtaining nutrients from unique resources (trophic morphology) (Malinsky et al, 2015; Parsons et al, 2016; Santana and Cheung, 2016). Darwin’s finches are considered ‘imperfect dietary generalists’ (De Leon et al, 2014) having similar preferred diets that overlap among species but specialize on a unique food when the preferred diet is limiting. Such difference in diet flexibility suggests that in addition to morphological differences, animals might display differential metabolic flexibility, that is the capacity to adapt nutrient use to nutrient availability.
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