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First published online September 19, 2006
Journal of Experimental Biology 209, 3729-3741 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02444

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Receptor expression and sympatric speciation: unique olfactory receptor neuron responses in F₁ hybrid Rhagoletis populations

Shannon B. Olsson^1,*, Charles E. Linn, Jr¹, Andrew Michel², Hattie R. Dambroski², Stewart H. Berlocher³, Jeffrey L. Feder² and Wendell L. Roelofs¹

¹ Department of Entomology, Barton Lab, NYSAES, Cornell University, Geneva, NY 14456, USA
² Department of Biological Sciences, PO Box 369, Galvin Life Science Center, University of Notre Dame, Notre Dame, IN 46556-0369, USA
³ Department of Entomology, University of Illinois, 320 Morrill Hall, 505 South Goodwin Avenue, Urbana, IL 61801, USA

^* Author for correspondence at present address: Department of Ecology and Evolutionary Biology, University of California, Los Angeles, 618 Charles E. Young Drive South, PO Box 951786, Los Angeles, CA 90095-1786, USA (e-mail: shannonolsson{at}ucla.edu)

Accepted 13 July 2006

The Rhagoletis pomonella species complex is one of the foremost examples supporting the occurrence of sympatric speciation. A recent study found that reciprocal F₁ hybrid offspring from different host plant-infesting populations in the complex displayed significantly reduced olfactory host preference in flight-tunnel assays. Behavioral and electrophysiological studies indicate that olfactory cues from host fruit are important chemosensory signals for flies to locate fruit for mating and oviposition. The reduced olfactory abilities of hybrids could therefore constitute a significant post-mating barrier to gene flow among fly populations. The present study investigated the source of changes in the hybrid olfactory system by examining peripheral chemoreception in F₁ hybrid flies, using behaviorally relevant volatiles from the parent host fruit. Single-sensillum electrophysiological analyses revealed significant changes in olfactory receptor neuron (ORN) response specificities in hybrid flies when compared to parent ORN responses. We report that flies from F₁ crosses of apple-, hawthorn- and flowering dogwood-origin populations of R. pomonella exhibited distinct ORN response profiles absent from any parent population. These peripheral alterations in ORN response profiles could result from misexpression of multiple receptors in hybrid neurons as a function of genomic incompatibilities in receptor-gene pathways in parent populations. We conclude that these changes in peripheral chemoreception could impact olfactory host preference and contribute directly to reproductive isolation in the Rhagoletis complex, or could be genetically coupled to other host-associated traits.

Key words: host shift, hybridization, postzygotic isolation, single sensillum electrophysiology, discrimination, specificity