Connecting neuromodulation, brain development, and life history timing associated with ecological speciation in Rhagoletis pomonella

Abstract

AbstractHost shifts are considered a key generator of insect biodiversity. In insects, adaption to new host plants often requires synchronization of growth and development during larval and pupal stages with the new host as well as changes in adult preference for that host after metamorphosis. 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. These races are known to exhibit differences in both diapause timing as well as adult neurophysiological response with respect to their hosts. In turn, we found that the apple host race exhibited adult brain differentiation during metamorphosis three weeks earlier than the hawthorn host race, which correlated with significantly lower titers of several neurochemicals. These differences in neurotransmitter titres between the races are carried through further developmental stages. In some cases, particularly for biogenic amines, the differences persisted through the eclosion and sexual maturation in the adult fly, the stage at which host preference is exhibited. We thus propose that changes in neuromodulation during specific stages of adult brain development could link differences in life history timing and host preference in these races, providing a new hypothesis regarding the genesis of our planet’s most specious multicellular taxon.