The scent of habitat shift: Olfactory receptor evolution is associated with environmental transitions in turtles

Abstract

The transition between aquatic and terrestrial habitats leads to extreme structural changes in sensorial systems. Olfactory receptors (OR) are involved in the detection of odorant molecules both in water and on land. Therefore, ORs are affected by evolutionary habitat transitions experienced by organisms. In this study, we used turtles, a group of vertebrates which inhabit many distinct environments, to explore whether functional olfactory gene receptor repertoires are correlated to habitat. We found that the proportion of class I vs class II functional olfactory receptor genes (used for waterborne odorant detection and volatile odorant detection, respectively) was closely linked to habitat. Fully terrestrial turtles had the largest proportion of class II functional receptor genes while marine turtles had a larger proportion of class I receptor genes. Freshwater turtles had more balanced numbers of class I and class II functional receptor genes, but showed a gradient of OR type proportions likely reflecting species-specific amphibious preferences. Interestingly, freshwater turtles had by far the largest number of functional OR genes compared to those in other habitats, challenging the hypothesis that secondary adaptions to water may have reduced OR repertoires in amniotes. Our study provides novel results which shed new light on the relationship between chemical communication and habitat.