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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

View larger version (32K): [in a new window]   Fig. 1. Comparison of typical response profiles for R. pomonella parent and hybrid ORNs from (A) class A (1-octen-3-ol responders) (B) class B (hexyl butanoate or dihydro-ß-ionone responders) and (C) class C (4,8-dimethyl-1,3(E),7-nonatriene responders). Parent data was obtained previously (Olsson et al., 2006a). Bar charts indicate spike frequencies (spikes s-1) for the 500 (hybrid) and 600 ms (parent) following initial exposure to 10 µg of each volatile listed at the bottom of the figure. The first 2 s of the 10.5 s recordings from which these frequencies were obtained is shown below each chart with chart ticks demarcating corresponding traces. Lines under the first trace indicate location of stimulus delivery for subsequent traces. In A, the parent ORN is specific to 1-octen-3-ol, whereas the hybrid ORN (dogwood x apple) responds to 1-octen-3-ol along with hexyl butanoate and isoamyl acetate. The B parent cell is specific to hexyl butanoate whereas the hybrid cell (apple x hawthorn) also responds to butyl butanoate. Finally, in C, the parent ORN is specific to 4,8-dimethyl-1,3(E),7-nonatriene, whereas the hybrid ORN (dogwood x apple) also responds to dihydro-ß-ionone, isoamyl acetate and 1-octen-3-ol.

View larger version (41K): [in a new window]   Fig. 2. Bar graphs depicting olfactory receptor neuron (ORN) response profiles and sensitivities for Rhagoletis hybrid populations. Cells are grouped by receptor neuron class and host volatile. The x axes list contacted ORNs and bar pattern indicates the hybrid population. ORNs are arranged from left to right according to cluster analysis classes (Olsson et al., 2006a). Sensitivities (y axes) are depicted as log(sensitivity). Parent-like and Hybrid-like indicate hybrid ORNs from classes A-C that responded with parent- or hybrid-like response profiles, respectively (see Materials and methods). Asterisks below certain ORNs indicate that the response profile for that ORN corresponded to multiple classes and was listed for each class it resembled.

View larger version (32K): [in a new window]   Fig. 3. Most parsimonious TCS network depicting the relationships among ORN response patterns to the 11 tested fruit volatile compounds (see Fig. 2) for (A) parental apple, hawthorn and dogwood flies, and (B) F1 hybrids. Each oval node represents a different response pattern observed in the parent or hybrid neuron population, with numbers above or below nodes indicating the ORN response profile according to the numbered compounds listed in Fig. 2. The five black nodes at the top of each diagram designate the five general response categories identified in the parent population. These response categories are similar to the cluster analysis classes (Olsson et al., 2006a) (Table 2) listed above each node. The sizes of oval nodes reflect the relative proportions of the different neural response patterns observed in the test population (N=77 neurons recorded for parents, N=118 for F1 hybrids), with black nodes indicating shared response patterns seen in both parents and hybrids and white nodes unique response patterns. Furthermore, white labeled nodes represent neurons responding to only the respective compound shown (mono-response patterns). Shared neurons (black nodes) are anchored in the same positions in A and B to provide reference points for comparing the parent and hybrid networks, and are labeled by their response pattern. The number of straight-line segments connecting two nodes indicate the difference in the number of compounds that the neurons responded to. Compounds 7 and 8 (pentyl hexanoate and butyl hexanoate) were considered to represent a single volatile for network construction and branch length calculation owing to the high positive correlation in neuron response between the two compounds.

View larger version (14K): [in a new window]   Fig. 4. Histograms of nearest neighbor distances calculated between neuron response patterns observed in reference (first) vs comparison (second) populations for (A) parent vs parent, (B) parent vs F1 hybrid, and (C) F1 hybrid vs parent analyses. Also given are mean nearest neighbor distances for each comparison (mean NND), and the probability level (P value) for the mean NND as determined by Monte Carlo parametric bootstrapping. For the parent vs F1 hybrid and F1 hybrid vs parent analyses (B,C), P values indicate the proportions of randomly drawn parent and F1 hybrid data sets sampled with replacement from a combined neuron response sampling pool that had mean NND as great or greater than the observed value in 10 000 trials. For the parent to parent analysis, the P value represents the proportion of randomly drawn data sets of 77 neurons sampled with replacement from the F1 hybrid population that had a mean NND to the actual parent population the same or less than the observed parent to parent value in 10 000 trials.