Abstract

During evolution, organisms have acquired variable feeding habits. Some species are nutritional generalists that adapt to various food resources, while others are specialists, feeding on specific resources. However, much remains to be discovered about how generalists adapt to diversified diets. We find that larvae of the generalists Drosophila melanogaster and D.simulans develop on three diets with different nutrient balances, whereas specialists D.sechellia and D.elegans cannot develop on carbohydrate-rich diets. The generalist D.melanogaster downregulates the expression of diverse metabolic genes systemically by transforming growth factor β (TGF-β)/Activin signaling, maintains metabolic homeostasis, and successfully adapts to the diets. In contrast, the specialist D.sechellia expresses those metabolic genes at higher levels and accumulates various metabolites on the carbohydrate-rich diet, culminating in reduced adaptation. Phenotypic similarities and differences strongly suggest that the robust carbohydrate-responsive regulatory systems are evolutionarily retained through genome-environment interactions in the generalists and contribute to their nutritional adaptabilities.

Highlights

  • Nutrition is a critical environmental determinant for animal growth, reproduction, and longevity

  • Larvae of all three specialists failed to develop on the C diet; most notably, two specialists, D. sechellia and D. elegans, reduced their pupariation rates proportionately with decreasing P:C ratios (Figures 1C and 1D; as for D. erecta, see Discussion)

  • Larvae of the specialists D. sechellia and D. elegans showed substantial developmental delays on the C and medium diet (M diet) compared to the P diet (Figures 1E, 1G, and S1A)

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Summary

Introduction

Nutrition is a critical environmental determinant for animal growth, reproduction, and longevity. Some species are generalists, which adapt to a wide range of food resources, while others are specialists, which feed on limited resources. It is still unclear how adaptabilities to nutritional conditions differ between generalist and specialist species, how different responses are in gene regulation and metabolism, and what molecular mechanisms underlie the difference. Previous studies on Drosophila specialist species have provided examples of the genetic underpinnings of traits that are adaptive to their host resources, such as chemoreception and egg production (Lang et al, 2012; Lavista-Llanos et al, 2014; Linz et al, 2013; Matsuo et al, 2007; McBride et al, 2007). It was reported that nutritional adaptability and gene expression are different between D. melanogaster and cactus-feeding species (Matzkin et al, 2011; Nazario-Yepiz et al, 2017); the underlying molecular mechanisms of these differences have not been resolved

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