Project Outcomes: RII Track-2 FEC: From Genome to Phenome in a Stressful World: Epigenetic Regulatory Mechanisms Mediating Thermal Plasticity in Drosophila

Unlike humans, who can exquisitely regulate their internal temperature over a broad range of conditions, body temperature in insects and other ectotherms reflects the temperature of the external environment.  As temperatures increase, so do the rates of cellular processes, accelerating growth, development, metabolism, reproduction, and aging, with extreme cold and extreme heat leading to immobilization, damage, and even death.  Although they cannot control their internal temperature, however, insects are not defenseless; they can both mount physiological responses as temperatures change to protect sensitive tissues and body functions, and proactively anticipate future stressors, a process called thermal acclimation.  Thermal acclimation was first described over forty years ago, yet we still do not know precisely how acclimation works at a genetic level, or the impact of acclimation for individual, population, and species persistence under increasingly unpredictable global temperatures.  Understanding this phenomenon is vital, as insects are the foundation of the terrestrial food web, play vital ecological roles as pollinators, scavengers, and biological control agents, and have an outsized impact on human food security and quality of life.

In this project, a multi-disciplinary team of geneticists, physiologists, and evolutionary biologists from academic institutions in Vermont, Rhode Island, Kentucky and Nevada investigated the mechanisms and evolution of thermal acclimation in the fruit fly Drosophila melanogaster and its wild relatives.  To identify what molecular processes are involved in the acclimation response, we profiled how flies alter and regulate their gene expression in response to temperature in both early embryos and adults, and looked in detail at two key organ systems, the brain and the muscle, which together are responsible for maintaining normal activity.   We found a widespread response to temperature, targeted toward the key problems posed at each extreme: cool temperatures, which slow down activity, were countered with heightened metabolism during development and fortification of structures in both brain and muscle to permit them to function more effectively.  Under heat, where overamped metabolism can lead to damage, only brain function was preserved, while muscle showed protective reduction in activity.  Two epigenetic mechanisms were identified that may allow the thermal acclimation response to be retained over time, conferring long-term protection to future temperature shocks.  To investigate the implications of these mechanisms for natural populations, we explored the genetic and evolutionary basis for thermal acclimation.  Using novel high-throughput methods to assay cold and heat tolerance in a set of fly lines whose genomes have been fully sequenced, we found that D. melanogaster harbors significant genetic variation in temperature tolerance and acclimation ability, suggesting that they may be able to adapt to changing conditions.  This was further supported by comparisons of D. melanogaster and three other fly species collected in the field along temperature gradients, all of which displayed increased temperature tolerance at sites with more extreme conditions.  Intriguingly, interactions with the microbes that colonize the digestive tract also appear to be important in determining individual tolerance, suggesting that predicting outcomes in nature will require a broader ecological approach that takes into account both genetic and environmental influences.

Broader Impacts

This project provided training to a total of 134 students in all aspects of biology, from ecology to physiology to molecular biology to computational bioinformatics.  Ninety-four undergraduates, many from primarily undergraduate institutions, participated as research assistants on every aspect of the work; eleven graduate students and 12 post-doctoral associates have been engaged in the project, leading directly to professional opportunities in teaching and research.  Eight laboratory technicians and other staff have also gained valuable career experience through employment with the grant.  Our trainees include several groups under-represented in STEM fields, including women, Black/African American, Hispanic, native Hawai’ian, first-generation college, and students with disabilities.  Team members were active in STEM outreach in local communities, with summer high school immersion workshops in entomology, field ecology and genetics that served students in Lexington, KY, Providence, RI and Burlington, VT. 

Last Modified: 01/30/2024
Modified by: Sara I Cahan