Amphibian water to land transition reveals physical limits of olfaction

Abstract

The evolutionary transition from water to land required animals to sense and respond to drastically different environments. Chemicals diffuse four orders of magnitude more slowly in water than in air, requiring significant remodeling of the olfactory system. Amphibians provide a powerful model to analyze these adaptations because they transition from an aquatic to terrestrial state during a single lifetime following metamorphosis. Here we exploit laboratory-induced metamorphosis of adult Ambystoma mexicanum to ask how fundamental chemical properties impact aquatic versus terrestrial olfaction. By combining asymptotic theory with numerical simulations using reconstructed olfactory chamber morphologies, we find that odor adsorption takes tens of seconds in water compared to milliseconds in air. Adsorption of an ephemeral odor whiff is maximized at an inhalation speed of $\sim$\SI{20}{\centi\meter\per\second} in air vs near zero in water, matching our measurements of negligible aquatic inhalation. Nevertheless, aquatic axolotls quickly respond to introduced odorant molecules. While morphological differences in the olfactory chamber of aquatic versus terrestrial axolotls are nearly irrelevant, aquatic olfactory cilia may pump water to significantly speed up the rate of odor adsorption. Together with adaptive behavioral responses that reduce proximity to the target, the wait time can reduce to less than one second. Thus, while aquatic olfaction is slower than terrestrial olfaction, aquatic animals exhibit anatomical and behavioral adaptations that support chemical detection as a proximal sense.