Sensory specificity and speciation: a potential neuronal pathway for host fruit odour discrimination in Rhagoletis pomonella.

Cheyenne Tait,Shannon B Olsson,Jeffrey L Feder,Sree Subha Ramaswamy,Srishti Batra

doi:10.1098/rspb.2016.2101

Abstract

Behavioural changes in habitat or mate choice can trigger population divergence, leading to speciation. However, little is known about the neurological bases for such changes. Rhagoletis pomonella (Diptera: Tephritidae) is a model for ecological speciation via host plant shifts. Within the past 180 years, Rhagoletis flies infesting hawthorn (Crataegus spp.) shifted to attack domesticated apple (Malus pumila). The two populations differ in their olfactory preferences for apple versus hawthorn fruit. Here, we looked for patterns of sensory organization that may have contributed to this shift by characterizing the morphology, specificity and distribution of olfactory sensory neurons (OSNs) on the antennae of Rhagoletis responding to host fruit and non-host volatiles. Of 28 OSN classes identified, two colocalized OSN pairs were found that specifically responded to the major behavioural attractant and antagonist volatiles for each fly population. A reversal in the response of these OSNs to fruit volatiles, either through a switch in receptor expression between these paired neurons or changes in neuronal projections in the brain, could therefore account for the behavioural difference between apple and hawthorn flies. The finding supports the hypothesis that relatively minor changes in olfactory sensory pathways may contribute to rapid host shifting and divergence in Rhagoletis.

Highlights

Ernst Mayr once said that behaviour is ‘the pacemaker of evolution’ [1]
One important way that insects accomplish this is through differences in their olfactory preferences for chemical cues associated with their host plants [5,6]
We removed butyl hexanoate from consideration in the downy hawthorn blend, as it is only present in trace amounts [13,15], and at concentrations found in the apple volatile blend butyl hexanoate is an antagonist to hawthorn flies [14]

Summary

Introduction

Ernst Mayr once said that behaviour is ‘the pacemaker of evolution’ [1]. By this he meant that changes in behaviour affecting an organism’s preference for different habitats or mates may act as catalysts for population divergence, potentially leading to speciation. Previous studies of olfactory divergence in R. pomonella have suggested that the apple and hawthorn host races do not differ in their number or classes of antennal sensilla [34] These studies did not resolve details of individual OSN specificity, sensitivity and organization within sensilla. A few neurons responding to key apple and downy hawthorn volatiles could serve as sensory pathways upon which a small change in neural response may have a large impact on behaviour To investigate such possibilities, we first morphologically and physiologically characterize the different classes of OSNs present in Rhagoletis using scanning electron microscopy and single sensillum recording (SSR) to a panel of 76 different odorants. We removed butyl hexanoate from consideration in the downy hawthorn blend, as it is only present in trace amounts [13,15], and at concentrations found in the apple volatile blend butyl hexanoate is an antagonist to hawthorn flies [14]

Results

Findings

Discussion

Conclusion