Inducing extra copies of the Hsp70 gene in Drosophila melanogaster increases energetic demand

Mutations that increase gene expression are predicted to increase energy allocation to transcription, translation and protein function. Despite an appreciation that energetic tradeoffs may constrain adaptation, the energetic costs of increased gene expression are challenging to quantify and thus easily ignored when modeling the evolution of gene expression, particularly for multicellular organisms. Here we use the well-characterized, inducible heat-shock response to test whether expressing additional copies of the Hsp70 gene increases energetic demand in Drosophila melanogaster.

We measured metabolic rates of larvae with different copy numbers of the Hsp70 gene to quantify energy expenditure before, during, and after exposure to 36°C, a temperature known to induce robust expression of Hsp70. We observed a rise in metabolic rate within the first 30 minutes of 36°C exposure above and beyond the increase in routine metabolic rate at 36°C. The magnitude of this increase in metabolic rate was positively correlated with Hsp70 gene copy number and reflected an increase as great as 35% of the 22°C metabolic rate. Gene copy number also affected Hsp70 mRNA levels as early as 15 minutes after larvae were placed at 36°C, demonstrating that gene copy number affects transcript abundance on the same timescale as the metabolic effects that we observed. Inducing Hsp70 also had lasting physiological costs, as larvae had significantly depressed metabolic rate when returned to 22°C after induction.

Our results demonstrate both immediate and persistent energetic consequences of gene copy number in a multicellular organism. We discuss these consequences in the context of existing literature on the pleiotropic effects of variation in Hsp70 copy number, and argue that the increased energetic demand of expressing extra copies of Hsp70 may contribute to known tradeoffs in physiological performance of extra-copy larvae. Physiological costs of mutations that greatly increase gene expression, such as these, may constrain their utility for adaptive evolution.