The Transcriptome in Transition: Global Gene Expression Profiles of Young Adult Fruit Flies Depend More Strongly on Developmental Than Adult Diet

Developmental diet is known to exert long-term effects on adult phenotypes in many animal species as well as disease risk in humans, purportedly mediated through long-term changes in gene expression. However, there are few studies linking developmental diet to adult gene expression. Here, we use a f...

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Main Authors: Christina M. May, Erik B. Van den Akker, Bas J. Zwaan
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-03-01
Series:Frontiers in Ecology and Evolution
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fevo.2021.624306/full
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spelling doaj-673e3141998441aa83d687d3cc265a7c2021-03-08T04:48:21ZengFrontiers Media S.A.Frontiers in Ecology and Evolution2296-701X2021-03-01910.3389/fevo.2021.624306624306The Transcriptome in Transition: Global Gene Expression Profiles of Young Adult Fruit Flies Depend More Strongly on Developmental Than Adult DietChristina M. May0Erik B. Van den Akker1Erik B. Van den Akker2Erik B. Van den Akker3Bas J. Zwaan4Laboratory of Genetics, Department of Plant Sciences, Wageningen University, Wageningen, NetherlandsLeiden Computational Biology Center, Department of Biomedical Data Sciences, Leiden University Medical Center, Leiden, NetherlandsMolecular Epidemiology, Department of Biomedical Data Sciences, Leiden University Medical Center, Leiden, NetherlandsPattern Recognition & Bioinformatics, Delft University of Technology, Delft, NetherlandsLaboratory of Genetics, Department of Plant Sciences, Wageningen University, Wageningen, NetherlandsDevelopmental diet is known to exert long-term effects on adult phenotypes in many animal species as well as disease risk in humans, purportedly mediated through long-term changes in gene expression. However, there are few studies linking developmental diet to adult gene expression. Here, we use a full-factorial design to address how three different larval and adult diets interact to affect gene expression in 1-day-old adult fruit flies (Drosophila melanogaster) of both sexes. We found that the largest contributor to transcriptional variation in young adult flies is larval, and not adult diet, particularly in females. We further characterized gene expression variation by applying weighted gene correlation network analysis (WGCNA) to identify modules of co-expressed genes. In adult female flies, the caloric content of the larval diet associated with two strongly negatively correlated modules, one of which was highly enriched for reproduction-related processes. This suggests that gene expression in young adult female flies is in large part related to investment into reproduction-related processes, and that the level of expression is affected by dietary conditions during development. In males, most modules had expression patterns independent of developmental or adult diet. However, the modules that did correlate with larval and/or adult dietary regimes related primarily to nutrient sensing and metabolic functions, and contained genes highly expressed in the gut and fat body. The gut and fat body are among the most important nutrient sensing tissues, and are also the only tissues known to avoid histolysis during pupation. This suggests that correlations between larval diet and gene expression in male flies may be mediated by the carry-over of these tissues into young adulthood. Our results show that developmental diet can have profound effects on gene expression in early life and warrant future research into how they correlate with actual fitness related traits in early adulthood.https://www.frontiersin.org/articles/10.3389/fevo.2021.624306/fullphenotypic plasticitytranscriptomicsdietdevelopmentnutritionDrosophila melanogaster
collection DOAJ
language English
format Article
sources DOAJ
author Christina M. May
Erik B. Van den Akker
Erik B. Van den Akker
Erik B. Van den Akker
Bas J. Zwaan
spellingShingle Christina M. May
Erik B. Van den Akker
Erik B. Van den Akker
Erik B. Van den Akker
Bas J. Zwaan
The Transcriptome in Transition: Global Gene Expression Profiles of Young Adult Fruit Flies Depend More Strongly on Developmental Than Adult Diet
Frontiers in Ecology and Evolution
phenotypic plasticity
transcriptomics
diet
development
nutrition
Drosophila melanogaster
author_facet Christina M. May
Erik B. Van den Akker
Erik B. Van den Akker
Erik B. Van den Akker
Bas J. Zwaan
author_sort Christina M. May
title The Transcriptome in Transition: Global Gene Expression Profiles of Young Adult Fruit Flies Depend More Strongly on Developmental Than Adult Diet
title_short The Transcriptome in Transition: Global Gene Expression Profiles of Young Adult Fruit Flies Depend More Strongly on Developmental Than Adult Diet
title_full The Transcriptome in Transition: Global Gene Expression Profiles of Young Adult Fruit Flies Depend More Strongly on Developmental Than Adult Diet
title_fullStr The Transcriptome in Transition: Global Gene Expression Profiles of Young Adult Fruit Flies Depend More Strongly on Developmental Than Adult Diet
title_full_unstemmed The Transcriptome in Transition: Global Gene Expression Profiles of Young Adult Fruit Flies Depend More Strongly on Developmental Than Adult Diet
title_sort transcriptome in transition: global gene expression profiles of young adult fruit flies depend more strongly on developmental than adult diet
publisher Frontiers Media S.A.
series Frontiers in Ecology and Evolution
issn 2296-701X
publishDate 2021-03-01
description Developmental diet is known to exert long-term effects on adult phenotypes in many animal species as well as disease risk in humans, purportedly mediated through long-term changes in gene expression. However, there are few studies linking developmental diet to adult gene expression. Here, we use a full-factorial design to address how three different larval and adult diets interact to affect gene expression in 1-day-old adult fruit flies (Drosophila melanogaster) of both sexes. We found that the largest contributor to transcriptional variation in young adult flies is larval, and not adult diet, particularly in females. We further characterized gene expression variation by applying weighted gene correlation network analysis (WGCNA) to identify modules of co-expressed genes. In adult female flies, the caloric content of the larval diet associated with two strongly negatively correlated modules, one of which was highly enriched for reproduction-related processes. This suggests that gene expression in young adult female flies is in large part related to investment into reproduction-related processes, and that the level of expression is affected by dietary conditions during development. In males, most modules had expression patterns independent of developmental or adult diet. However, the modules that did correlate with larval and/or adult dietary regimes related primarily to nutrient sensing and metabolic functions, and contained genes highly expressed in the gut and fat body. The gut and fat body are among the most important nutrient sensing tissues, and are also the only tissues known to avoid histolysis during pupation. This suggests that correlations between larval diet and gene expression in male flies may be mediated by the carry-over of these tissues into young adulthood. Our results show that developmental diet can have profound effects on gene expression in early life and warrant future research into how they correlate with actual fitness related traits in early adulthood.
topic phenotypic plasticity
transcriptomics
diet
development
nutrition
Drosophila melanogaster
url https://www.frontiersin.org/articles/10.3389/fevo.2021.624306/full
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