The evolution of cavefish odor perception shifts fish response from avoidance to approach when exposed to alarm and death odors

An animal’s survival is dependent on activating the correct behavioral circuit in response to a sensory stimulus. These stimuli include environmental odorants that evoke positive approach behavior and negative avoidance behavior. While stimulus perception has evolved similarly across ecological niches, we still do not know the mechanisms that drive evolution of stimulus perception across taxa. The blind Mexican cavefish provides a unique model for understanding how changes in environmental pressures impact the evolution of the vertebrate brain and behaviors. For instance, cavefish exhibit sleep loss due to life in an environment with no sunlight. Therefore, we wondered how odor perception has evolved in cave adapted populations that experience vastly different environmental conditions and odors than their surface ancestors. We found that surface fish display approach behaviors when exposed to food and social odors, while exhibiting avoidance behaviors when exposed to alarm and death odors. Conversely, we find that cave populations exhibit approach behaviors when exposed to alarm and death odors in the dark, while only females show approach behaviors when exposed to social odors. In addition, we find that surface to cave F ₂ hybrids display a range of behaviors, from full avoidance to approach when exposed to social, alarm and death odors, that suggests these differences are genetically inheritable. Finally, forebrain phospho-ERK mapping revealed overlap in the activity of thalamic and preoptic subregions of the brain when cavefish were exposed to food or death odors. Taken together, we find that changes to cavefish odor perception provide a unique model for investigating the genetic and neurological mechanisms underlying olfactory evolution in vertebrates.