Phenotypic Plasticity of the Drosophila Transcriptome

Phenotypic plasticity is the ability of a single genotype to produce different phenotypes in response to changing environments. We assessed variation in genome-wide gene expression and four fitness-related phenotypes of an outbred Drosophila melanogaster population under 20 different physiological, social, nutritional, chemical, and physical environments; and we compared the phenotypically plastic transcripts to genetically variable transcripts in a single environment. The environmentally sensitive transcriptome consists of two transcript categories, which comprise ∼15% of expressed transcripts. Class I transcripts are genetically variable and associated with detoxification, metabolism, proteolysis, heat shock proteins, and transcriptional regulation. Class II transcripts have low genetic variance and show sexually dimorphic expression enriched for reproductive functions. Clustering analysis of Class I transcripts reveals a fragmented modular organization and distinct environmentally responsive transcriptional signatures for the four fitness-related traits. Our analysis suggests that a restricted environmentally responsive segment of the transcriptome preserves the balance between phenotypic plasticity and environmental canalization.

[1]  D. Begun,et al.  Whole-genome expression plasticity across tropical and temperate Drosophila melanogaster populations from Eastern Australia. , 2011, Molecular biology and evolution.

[2]  E. Stone,et al.  The genetics of quantitative traits: challenges and prospects , 2009, Nature Reviews Genetics.

[3]  David B. Goldstein,et al.  Genome-Wide Transcript Profiles in Aging and Calorically Restricted Drosophila melanogaster , 2002, Current Biology.

[4]  C. Waddington Canalization of Development and the Inheritance of Acquired Characters , 1942, Nature.

[5]  E. Stone,et al.  Modulated Modularity Clustering as an Exploratory Tool for Functional Genomic Inference , 2009, PLoS genetics.

[6]  J. Mensch,et al.  Identifying candidate genes affecting developmental time in Drosophila melanogaster: pervasive pleiotropy and gene-by-environment interaction , 2008, BMC Developmental Biology.

[7]  R. Weindruch,et al.  Oxidative Stress, Caloric Restriction, and Aging , 1996, Science.

[8]  R Gomulkiewicz,et al.  Adaptive phenotypic plasticity: consensus and controversy. , 1995, Trends in ecology & evolution.

[9]  Gos Micklem,et al.  Supporting Online Material Materials and Methods Figs. S1 to S50 Tables S1 to S18 References Identification of Functional Elements and Regulatory Circuits by Drosophila Modencode , 2022 .

[10]  C. H. WADDINGTON,et al.  Canalization of Development and Genetic Assimilation of Acquired Characters , 1959, Nature.

[11]  Alex Wong,et al.  Evolution of protein-coding genes in Drosophila. , 2008, Trends in genetics : TIG.

[12]  E. Stone,et al.  Systems Genetics of Complex Traits in Drosophila melanogaster , 2009, Nature Genetics.

[13]  Linda Partridge,et al.  Extending Healthy Life Span—From Yeast to Humans , 2010, Science.

[14]  A. D. Bradshaw,et al.  Evolutionary Significance of Phenotypic Plasticity in Plants , 1965 .

[15]  COMPETITION CAN MAINTAIN GENETIC BUT NOT ENVIRONMENTAL VARIANCE IN THE PRESENCE OF STABILIZING SELECTION , 2007, Evolution; international journal of organic evolution.

[16]  J. Dow,et al.  Using FlyAtlas to identify better Drosophila melanogaster models of human disease , 2007, Nature Genetics.

[17]  J. Dhahbi,et al.  Genomic profiling of short- and long-term caloric restriction effects in the liver of aging mice , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Brad T. Sherman,et al.  Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists , 2008, Nucleic acids research.

[19]  J. Hemingway,et al.  Genomic analysis of detoxification genes in the mosquito Aedes aegypti. , 2008, Insect biochemistry and molecular biology.

[20]  E. Stone,et al.  Plasticity of the Chemoreceptor Repertoire in Drosophila melanogaster , 2009, PLoS genetics.

[21]  R. Feyereisen,et al.  Evolution of insect P450. , 2006, Biochemical Society transactions.

[22]  Richard Weindruch,et al.  Gene-expression profile of the ageing brain in mice , 2000, Nature Genetics.

[23]  Brad T. Sherman,et al.  Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources , 2008, Nature Protocols.

[24]  Peer Bork,et al.  The Genome of the Model Beetle and Pest Tribolium Castaneum Vertebrate-specific Orthologues Insect-specific Orthologues Homology Undetectable Similarity , 2022 .

[25]  Y. Jan,et al.  Genome-wide study of aging and oxidative stress response in Drosophila melanogaster. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[26]  S. Cohen,et al.  microRNA functions. , 2007, Annual review of cell and developmental biology.

[27]  Kevin R. Thornton,et al.  The Drosophila melanogaster Genetic Reference Panel , 2012, Nature.

[28]  Melanie A. Huntley,et al.  Evolution of genes and genomes on the Drosophila phylogeny , 2007, Nature.

[29]  M. Berenbaum,et al.  A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee , 2006, Insect molecular biology.

[30]  Antoine M. van Oijen,et al.  Real-time single-molecule observation of rolling-circle DNA replication , 2009, Nucleic acids research.

[31]  L. B. Snoek,et al.  Genome-wide gene expression regulation as a function of genotype and age in C. elegans. , 2010, Genome research.

[32]  Stephen Guest,et al.  DroID 2011: a comprehensive, integrated resource for protein, transcription factor, RNA and gene interactions for Drosophila , 2010, Nucleic Acids Res..

[33]  Trudy F C Mackay,et al.  Phenotypic Plasticity and Genotype by Environment Interaction for Olfactory Behavior in Drosophila melanogaster , 2008, Genetics.

[34]  Guozhen Liu,et al.  DroID: the Drosophila Interactions Database, a comprehensive resource for annotated gene and protein interactions , 2008, BMC Genomics.

[35]  Janet Hemingway,et al.  Evolution of Supergene Families Associated with Insecticide Resistance , 2002, Science.

[36]  V. Loeschcke,et al.  Developmental time and size-related traits in Drosophila buzzatii along an altitudinal gradient from Argentina. , 2006, Hereditas.

[37]  Greg Gibson,et al.  Decanalization and the origin of complex disease , 2009, Nature Reviews Genetics.

[38]  L. Partridge,et al.  Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products , 1995, Nature.