The neural basis for sympatric speciation in the apple maggot fly (Rhagoletis pomonella)

Rhagoletis pomonella (Diptera: Tephritidae) is a model for ecological speciation in action. Within the last 180 years, ancestral flies that infested hawthorn fruit (Crataegus spp.) shifted to attack recently introduced apple (Malus domesticus). One ecological adaptation differentiating the host races is their behavioral preference for their natal host volatile blends. Apple flies positively orient to the volatile compounds emitted from apple fruit and tend to be deterred by hawthorn volatiles, while the reverse is true for hawthorn flies. Because R. pomonella flies mate only on or near the fruit of their host plants, these behavioral differences in olfaction result directly in differences in mate choice and prezygotic reproductive isolation.

Here we characterize the structures of the nervous system of R. pomonella to determine their contribution to host fruit odor discrimination. In other systems, slight modifications in the organization and wiring of sensory inputs have had profound impacts on behavioral preference. The input from these sensory neurons is then integrated in the antennal lobe of the central nervous system. We conducted electrophysiological recordings from sensilla on the antennae that allowed us to survey flies for their olfactory sensory neuron (OSN) types. We report the existence of co-localized pairs of OSNs, with one neuron responding to the key component of the apple blend and one to the hawthorn blend. We discuss possible mechanisms involving these OSNs that could have affected the evolution of different fruit odor behavioral responses in the flies, leading to ecological specialization and population divergence. We also describe the first use of imaging methods to characterize antennal lobe processing in this species.