The role of cell size in shaping responses to oxygen and temperature in fruit flies

Abstract

Abstract The body size of an animal is strongly coupled to key ecological traits such as fecundity, mortality and growth. Ectothermic animals mature at smaller body sizes in warmer conditions and under low oxygen availability (hypoxia). Whether these responses result from changes in cell size and cell number (which together determine body size) and how such cellular responses may help ectotherms cope with heat and hypoxia is poorly understood. The theory of optimal cell size postulates that cell size imposes constraints on oxygen delivery: Differences in cell size result in differences in membrane surface‐to‐volume ratio, which impact the capacity of cells to take up oxygen and has consequences for growth rate and hence body size. Here, using inbred lines of fruit flies Drosophila melanogaster, which exhibit differences in cell size, we demonstrate that thermal responses in body size are magnified under hypoxia and in lines of flies that exhibit larger cell size. Furthermore, reductions in body size were partly manifested via reductions in cell size, resulting in a coupling between the body mass and cell size of flies. The coupling between cell size and body size was tighter under conditions where oxygen is expected to become limited, that is, warm or hypoxia, supporting the idea that capacity for oxygen uptake is causally related to organismal growth and the resulting body size. Our data indicate that the benefits of diffusive oxygen uptake due to the higher surface‐to‐volume ratios in smaller cells can help explain the temperature‐size rule in this species. Read the free Plain Language Summary for this article on the Journal blog.