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Developmental Biology - Genes

Why Fruit Flies Can Eat Almost Anything

Some flies are 'generalists' while others are 'specialists, just like humans...

Say hello to the common fruit fly - a regular guest in all our homes, feasting on old banana peels tossed in the garbage a few days ago.

Despite their name, they don't just feast on fruit. These nimble insects will feed on all kinds of plant matter. In a paper published in Cell Reports scientists describe how this ability to diversify their diet stems from a flexible response to managing carbohydrates, giving us humans insight into how we evolved based on what we eat.

The fruit fly, Drosophila melanogaster, may be a nuisance in the kitchen, but they are the backbone of Genetic Research providing answers on how genes operate. Like the fruit fly, humans can also eat a wide range of food resources. Humans are known as 'nutritional generalists' much like fruit flies.

However, some genetic cousins of the fruit fly are known as 'nutritional specialists' and only survive on very specific plants. Many questions exist regarding organisms in the same gene family having such different feeding habits.
"Uncovering the differences in the molecular mechanisms between nutritional generalists and specialists can help us understand how organisms adapt to variable nutritional environments."

Kaori Watanabe PhD, Kyoto University Graduate School of Biostudies, who with Yukako Hattori PhD leads the study.

Changing nutrient balance in foods given to different species of Drosophila, researchers compared nutritional adaptability between species. They began by examining whether larvae of generalists and specialists could adapt to three experimental diets: • high protein • high carbohydrate - and • 'medium' protein-carbohydrate.
As expected, generalist flies - including the common fruit fly - grew under all diets. But, specialist eaters' larvae did not survive eating carbohydrate rich diets.

Specialists are known to eat and reproduce on specific fruits or flowers. Examining nutritional profiles of their native diets shows they survive on low-carbohydrate diets. The team hypothesizes differences between flies lies in their gene pathways which control their response to carbohydrate.

"A signaling pathway known as 'TGF-฿/Activin signaling' regulates the body's response to carbohydrates. In the generalists, this pathway is quite flexible and maintains metabolic homeostasis under different diets. In fact, there are about 250 metabolic genes that are downregulated when a diet is carbohydrate-rich," they explain.
In contrast, a specialist expresses these metabolic genes at higher levels, where they accumulate metabolites reducing their adaptability. The same lack of adaptation is also found when a gene in the TGF-฿/Activin pathway, named dawdle, is disabled in the common fruit fly.

These results suggest that generalists evolutionarily retain a robust carbohydrate-responsive system through genome-environmental interactions. Whereas specialists lose this robustness, consistent with low-carbohydrate environments.

Leading the research team to conclude: "considering humans and flies share a number of genes and regulatory factors, we can begin to develop an interspecies comparative approach - providing an informative model system addressing genetic variability amongst humans in response to dietary intake."

• The generalists adapt to various nutrient balances, whereas the specialists cannot
• The generalists regulate carbohydrate-responsive gene expression by Activin signaling
• The specialist species are defective in carbohydrate-responsive gene regulation
• The specialist D. sechellia accumulates various metabolites and reduces adaptation

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 ฿ (TGF-฿)/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.

Kaori Watanabe, Yasutetsu Kanaoka, Shoko Mizutani, Masayoshi Watada, Tadashi Uemura, Yukako Hattori.

The authors thank T. Kondo and Y. Sando for performing RNA sequencing; the metabolomics core facility at the University of Utah and J. Cox for GC-MS analysis of larvae; D. Shibata, A. Kurabayashi, T. Kawada, and T. Kambe for critical advice about GC-MS analysis of fermented foods; T. Usui, T. Kondo, and J.A. Hejna for polishing the manuscript; and K. Tamura, I. Ohshima, T. Matsuo, S. Koshikawa, T. Nishimura, M. Umeda, T. Suito, B. Lemaitre, M.B. O’Connor, B. Oliver, Z. Chen, T. Takano, V.I. Hietakangas, and members of the Uemura laboratory for technical advice and discussions. This work was supported by AMED-CREST (JP18gm1110001 to T.U.); the Mitsubishi Foundation (to T.U.); the SPIRITS program of Kyoto University (to T.U.); the Japan Society for the Promotion of Science (JSPS; 15H02400 and 15K14524 to T.U., 15K18455 and 17K15039 to Y.H., and 16J10660 to K.W.); MEXT (17H05766 to T.U.); the Naito Foundation (to Y.H.); the Sasakawa Scientific Research Grant (to Y.H.); a grant for RNA sequencing from MEXT KAKENHI (221S0002); and the Cooperative Research Grant of the Genome Research for BioResource, NODAI Genome Research Center, Tokyo University of Agriculture.

Author Contributions
Y.H. and T.U. conceived and designed the study. Y.H. and K.W. designed experiments. K.W. performed most of the experiments. Y.H. analyzed omics data and performed some initial experiments. K.W., Y.H., M.W., and T.U. collected wild D. elegans and morning glory. M.W. identified species of the generalists collected in the wild. Y.K. performed some experiments and quantifications of pupariation rate. S.M. performed the lipid droplet staining experiment and quantification. H.U. and S.Y. performed RNA sequencing (platform “N”). Y.H., K.W., and T.U. wrote and edited the manuscript, with contributions from all authors.

About Kyoto University
Kyoto University is one of Japan and Asia's premier research institutions, founded in 1897 and responsible for producing numerous Nobel laureates and winners of other prestigious international prizes. A broad curriculum across the arts and sciences at both undergraduate and graduate levels is complemented by numerous research centers, as well as facilities and offices around Japan and the world. For more information please see: http://www.kyoto-u.ac.jp/en

Declaration of Interests
The authors declare no competing interests.

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Sep 10 2019   Fetal Timeline   Maternal Timeline   News  

Drosophila elegans feed and breed on specific morning glory flowers found in Okinawa and Southeast Asia. They are 'nutritional specialists who cannot adapt to high carbohydrate diets.
CREDIT Kyoto University/Kaori Watanabe

Phospholid by Wikipedia