Comparing peripheral olfactory coding with host preference in the rhagoletis species complex.

Recent studies have shown that flies from sympatric populations of Rhagoletis pomonella infesting hawthorn, apple, and flowering dogwood fruit can distinguish among unique volatile blends identified from each host. Analysis of peripheral chemoreception in Rhagoletis flies suggests that changes in receptor specificity and/or receptor neuron sensitivity could impact olfactory preference among the host populations and their hybrids. In an attempt to validate these claims, we have combined flight tunnel analyses and single sensillum electrophysiology in F(2) and backcross hybrids displaying a variety of behavioral phenotypes. Results show that differences in peripheral chemoreception among second-generation adults do not provide a direct correlation between peripheral coding and olfactory behavior. We conclude that either the plasticity of the central nervous system in Rhagoletis can compensate for significant alterations in peripheral coding or that peripheral changes present subtle effects on behavior not easily detectable with current techniques. The results of this study imply that the basis for olfactory behavior in Rhagoletis has a complicated genetic and neuronal basis, even for populations with a recent divergence in preference.

The genetic basis for fruit odor discrimination in Rhagoletis flies and its significance for sympatric host shifts.

Rhagoletis pomonella (Diptera: Tephritidae) use volatile compounds emitted from the surface of ripening fruit as important chemosensory cues for recognizing and distinguishing among alternative host plants. Host choice is of evolutionary significance in Rhagoletis because these flies mate on or near the fruit of their respective host plants. Differences in host choice based on fruit odor discrimination therefore result in differential mate choice and prezygotic reproductive isolation, facilitating sympatric speciation in the absence of geographic isolation. We test for a genetic basis for host fruit odor discrimination through an analysis of F2 and backcross hybrids constructed between apple-, hawthorn-, and flowering dogwood-infesting Rhagoletis flies. We recovered a significant proportion (30-65%) of parental apple, hawthorn, and dogwood fly response phenotypes in F2 hybrids, despite the general failure of F1 hybrids to reach odor source spheres. Segregation patterns in F2 and backcross hybrids suggest that only a modest number of allelic differences at a few loci may underlie host fruit odor discrimination. In addition, a strong bias was observed for F2 and backcross flies to orient to the natal fruit blend of their maternal grandmother, implying the existence of cytonuclear gene interactions. We explore the implications of our findings for the evolutionary dynamics of sympatric host race formation and speciation.

Development and characterization of novel, polymorphic microsatellite markers for oat crown rust, Puccinia coronata.

We report the development of 37 novel and polymorphic microsatellite markers for oat crown rust, Puccinia coronata f.sp. avenae. The allelic diversity ranged from two to 16 alleles per locus. Observed heterozygosity ranged from 0.000 to 0.971, and expected heterozygosity from 0.057 to 0.848. Thirteen of the loci were not in Hardy-Weinberg equilibrium, due to either the presence of null alleles, small sample size, or the effects of population subdivision (Wahlund's effect). All 37 primer pairs were tested with P. graminis and P. triticina showing that they are specific to P. coronata.

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

The Rhagoletis pomonella species complex is one of the foremost examples supporting the occurrence of sympatric speciation. A recent study found that reciprocal F(1) 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 F(1) 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 F(1) 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.

Fruit odor discrimination and sympatric host race formation in Rhagoletis.

Rhagoletis pomonella is a model for incipient sympatric speciation (divergence without geographic isolation) by host-plant shifts. Here, we show that historically derived apple- and ancestral hawthorn-infesting host races of the fly use fruit odor as a key olfactory cue to help distinguish between their respective plants. In flight-tunnel assays and field tests, apple and hawthorn flies preferentially oriented to, and were captured with, chemical blends of their natal fruit volatiles. Because R. pomonella rendezvous on or near the unabscised fruit of their hosts to mate, the behavioral preference for apple vs. hawthorn fruit odor translates directly into premating reproductive isolation between the fly races. We have therefore identified a key and recently evolved (<150 years) mechanism responsible for host choice in R. pomonella bearing directly on sympatric host race formation and speciation.

Postzygotic isolating factor in sympatric speciation in Rhagoletis flies: reduced response of hybrids to parental host-fruit odors.

Rhagoletis pomonella is a model for sympatric speciation (divergence without geographic isolation) by means of host-plant shifts. Many Rhagoletis species are known to use fruit odor as a key olfactory cue to distinguish among their respective host plants. Because Rhagoletis rendezvous on or near the unabscised fruit of their hosts to mate, behavioral preferences for fruit odor translate directly into premating reproductive isolation among flies. Here, we report that reciprocal F(1) hybrids between the apple and hawthorn host races of R. pomonella, as well as between the host races and an undescribed sibling species infesting Cornus florida (flowering dogwood) do not respond to host fruit volatiles in wind-tunnel assays at doses that elicit maximal directed flight in parental flies. The reduced ability of hybrids to orient to fruit volatiles could result from a conflict between neural pathways for preference and avoidance behaviors, and it suggests that hybrids might suffer a fitness disadvantage for finding fruit in nature. Therefore, host-specific mating may play a dual role as an important postzygotic as well as a premating reproductive barrier to isolate sympatric Rhagoletis flies.