Abstract
Phenotypic plasticity, the ability of an organism to alter its phenotype in response to an environmental cue, facilitates rapid adaptation to changing environments. Plastic changes in morphology and behavior are underpinned by widespread gene expression changes. However, it is unknown if, or how, genomes are structured to ensure these robust responses. Here, we use repression of honeybee worker ovaries as a model of plasticity. We show that the honeybee genome is structured with respect to plasticity; genes that respond to an environmental trigger are colocated in the honeybee genome in a series of gene clusters, many of which have been assembled in the last 80 My during the evolution of the Apidae. These clusters are marked by histone modifications that prefigure the gene expression changes that occur as the ovary activates, suggesting that these genomic regions are poised to respond plastically. That the linear sequence of the honeybee genome is organized to coordinate widespread gene expression changes in response to environmental influences and that the chromatin organization in these regions is prefigured to respond to these influences is perhaps unexpected and has implications for other examples of plasticity in physiology, evolution, and human disease.
Highlights
Phenotypic plasticity allows organisms to respond to their environment by dramatically changing their physiology and behavior without altering their underlying genotype (Pigliucci 2001; Nijhout 2003; West-Eberhard 2005)
Chromatin modification enzymes were identified as responding to ovary activation, in particular, genes that encode the polycomb repression complex (PRC) 1 and 2 and the trithorax acetylation complex (TAC)
We provide empirical evidence that the honeybee genome is ordered into genomic regulatory domains with respect to ovarian plasticity
Summary
Phenotypic plasticity allows organisms to respond to their environment by dramatically changing their physiology and behavior without altering their underlying genotype (Pigliucci 2001; Nijhout 2003; West-Eberhard 2005). Examples of phenotypic plasticity include changes in the morphology of the crustacean Daphnia due to predation (Laforsch and Tollrian 2004), or male horn length in species of horned beetles (Moczek 1998). Significant changes in shape, color, or form imply that global coordinated control of transcription and epigenetic regulation of the genome are required to change phenotype in response to environmental factors (Kucharski et al 2008; Brakefield and Frankino 2009). How globally coordinated changes in gene expression in response to environmental stimuli are regulated, remains largely unknown. To determine the genomic and epigenetic systems that establish and maintain phenotypic plasticity, we used a tractable and reliable model system: the honeybee Apis mellifera
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