Disentangling the multiple drivers of ecological adaptation in a microorganism

Abstract

To survive and reproduce, living organisms need to maintain an efficient balance between energy intake and energy expenditure. Changes in environmental conditions can disrupt previously efficient energy allocation strategies, and organisms are required to change their behaviour, physiology, or morphology to cope with the new environment. However, how multiple phenotypic traits interact with one another and with environmental conditions to shape energy allocation remains poorly understood. To better understand this type of phenotype-environment interactions, we develop a predictive framework, grounded in energetic and biophysical principles that allows us to make predictions on how metabolic rate and movement speed should change in response to environmental temperature and resource supply, differentiating between short-term, acute exposure to novel conditions and longer-term exposure that allows acclimation or adaptation. We tested these predictions by exposing axenic populations of the ciliate Tetrahymena pyriformis to different combinations of temperature and resource availability. We measured population growth, cell size, respiration, and movement. Acute increases in temperature led to higher movement speeds and respiration rates, consistent with expectations from physical scaling relationships such as the Boltzmann-Arrhenius equation and the viscous drag acting on movement. However, by around 3.5 days after the introduction of Tetrahymena into a novel environment, all measured traits shifted toward values closer to those of the original environment. These changes likely reflect phenotypic acclimation responses that restored a more efficient energy allocation under the new conditions. Changes in cell size played a key role in this process, by simultaneously affecting multiple phenotypic traits, including metabolic rate and the energetic costs of movement. In small microbial consumers like Tetrahymena, body size can change rapidly, relative to ecological and seasonal timescales. Changes in body size can therefore be effectively leveraged - alongside physiological and biochemical regulations - to cope with environmental changes. Open researchThe raw data and all the analysis code used for this work are publicly available on github (https://github.com/pernafrost/Tetrahymena), and they are also deposited in Dryad (https://doi.org/10.5061/dryad.2v6wwpzvv). By downloading and running the code, it is possible to reproduce all the figures presented in the manuscript and in the Appendix. Please refer to the linked repositories for additional information, and feel free to contact the authors in case you need additional guidance.