Rapid brain development and reduced neuromodulator titres correlate with host shifts in Rhagoletis pomonella

Abstract

Host shifts are considered a key generator of insect biodiversity, yet how insects synchronize life history timing and preference for new hosts is not well understood. Neurochemicals such as biogenic amines play key roles in both development and behavior, and therefore provide a potential source for such synchronization. Here, we correlated life history timing, brain development, and corresponding levels of 14 neurochemicals in Rhagoletis pomonella (Diptera: Tephritidae), a species undergoing ecological speciation through an ongoing host shift from hawthorn to apple fruit. We found that adult brain differentiation in both host races was initiated only after pupal diapause ended, and at this stage the titers of precursors for several neurotransmitter pathways also increased significantly. Conversely, neurotransmitter product titres generally increased at later stages up to adult fly sexual maturation. Further analysis showed that the apple host race exhibited adult brain differentiation three weeks earlier than the hawthorn host race, which correlated with significantly lower titers of several neurochemicals, particularly biogenic amines, in the earlier developing apple race as compared to the hawthorn race. We thus propose that these neurotransmitter levels could influence the differences in life history timing and host preference observed in these two races, promoting their ongoing speciation.