Abstract
Changes in behaviour often drive rapid adaptive evolution and speciation. However, the mechanistic basis for behavioural shifts is largely unknown. The tephritid fruit fly Rhagoletis pomonella is an example of ecological specialization and speciation in action via a recent host plant shift from hawthorn to apple. These flies primarily use specific odours to locate fruit, and because they mate only on or near host fruit, changes in odour preference for apples versus hawthorns translate directly to prezygotic reproductive isolation, initiating speciation. Using a variety of techniques, we found a reversal between apple and hawthorn flies in the sensory processing of key odours associated with host fruit preference at the first olfactory synapse, linking changes in the antennal lobe of the brain with ongoing ecological divergence. Indeed, changes to specific neural pathways of any sensory modality may be a broad mechanism for changes in animal behaviour, catalysing the genesis of new biodiversity.
Highlights
Changes in behaviour affecting an animal’s mate, food or habitat choice are often catalysts for rapid evolutionary change and speciation
Using a variety of techniques, we found a reversal between apple and hawthorn flies in the sensory processing of key odours associated with host fruit preference at the first olfactory synapse, linking changes in the antennal lobe of the brain with ongoing ecological divergence
We found that butyl hexanoate (BH) and 3-methyl butanol (3MB) responsive neurons innervated the same set of three glomeruli in apple (n = 9) and hawthorn (n = 10) flies, identified as the dorsal medial 1 (DM1), and ventral posterior 1 and 2 (VP1 and VP2) glomeruli
Summary
Changes in behaviour affecting an animal’s mate, food or habitat choice (i.e. moth sex pheromones [1], cichlid coloration [2], frog [3] and cricket [4] songs) are often catalysts for rapid evolutionary change and speciation. We provide evidence for a reversal in olfactory processing of fruit odour cues in Rhagoletis pomonella (Diptera: Tephritidae) affecting host plant and mate choice and contributing to rapid divergence into a derived race of apple-infesting flies. Host choice in R. pomonella is a behaviour that links finding mates for reproduction with finding fruit for oviposition and larval feeding Adults of both sexes of the ancestral hawthorn and derived apple races initially distinguish between apple versus hawthorn trees using specific olfactory cues [5,10]. Coupling of host and mate choice in R. pomonella, achieved through an evolved olfactory preference of apple race flies for apple odour, restricts gene flow with the ancestral hawthorn population to approximately 4% [12,14,15]. We use neurophysiological techniques to trace responses to BH and 3MB from OSNs through the antennal lobe to output via ALNs
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