Different amplitudes of temperature fluctuation induce distinct transcriptomic and metabolomic responses in the dung beetle Phanaeus vindex

Abstract

Most studies exploring molecular and physiological responses to temperature have focused on constant temperature treatments. To gain a better understanding of the impacts of fluctuating temperatures, we investigated impacts of increased temperature variation on Phanaeus vindex dung beetles across levels of biological organization. Specifically, we hypothesized that increased temperature variation is energetically demanding. We predicted that thermal sensitivity of metabolic rate and energetic reserves would be reduced with increasing fluctuation. To test this, we examined responses of dung beetles exposed to constant (20°C), low fluctuation (20±5°C), or high fluctuation (20±12°C) temperature treatments using respirometry, energetic reserves, and HPLC-MS-based metabolomics. We found no significant differences in metabolic rates or energetic reserves, suggesting increased fluctuations were not energetically demanding. To understand why there was no effect of increased amplitude on energetics, we assembled and annotated a de novo transcriptome, finding non-overlapping transcriptomic and metabolomic responses of beetles exposed to different fluctuations. We found that 58 metabolites increased in abundance in both fluctuation treatments, but 15 only did so in response to high amplitude fluctuations. We found 120 transcripts were significantly upregulated following acclimation to any fluctuation, but 174 were upregulated only in beetles from the high amplitude fluctuation. Several differentially expressed transcripts were associated with post-translational modifications to histones that support a more open chromatin structure. Our results demonstrate that acclimation to different temperature fluctuations is distinct and may be supported by increasing transcriptional plasticity. Our results indicate for the first time that histone modifications may underlie rapid acclimation to temperature variation.