Dataset Information

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

ABSTRACT: 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.

SUBMITTER: Linn CE

PROVIDER: S-EPMC539775 | biostudies-literature | 2004 Dec

REPOSITORIES: biostudies-literature

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

Linn Charles E CE Dambroski Hattie R HR Feder Jeffrey L JL Berlocher Stewart H SH Nojima Satoshi S Roelofs Wendell L WL

Proceedings of the National Academy of Sciences of the United States of America 20041210 51

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 betwe ...[more]

PMID: 15591346

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Project description:BackgroundThe full power of modern genetics has been applied to the study of speciation in only a small handful of genetic model species--all of which speciated allopatrically. Here we report the first large expressed sequence tag (EST) study of a candidate for ecological sympatric speciation, the apple maggot Rhagoletis pomonella, using massively parallel pyrosequencing on the Roche 454-FLX platform. To maximize transcript diversity we created and sequenced separate libraries from larvae, pupae, adult heads, and headless adult bodies.ResultsWe obtained 239,531 sequences which assembled into 24,373 contigs. A total of 6810 unique protein coding genes were identified among the contigs and long singletons, corresponding to 48% of all known Drosophila melanogaster protein-coding genes. Their distribution across GO classes suggests that we have obtained a representative sample of the transcriptome. Among these sequences are many candidates for potential R. pomonella "speciation genes" (or "barrier genes") such as those controlling chemosensory and life-history timing processes. Furthermore, we identified important marker loci including more than 40,000 single nucleotide polymorphisms (SNPs) and over 100 microsatellites. An initial search for SNPs at which the apple and hawthorn host races differ suggested at least 75 loci warranting further work. We also determined that developmental expression differences remained even after normalization; transcripts expected to show different expression levels between larvae and pupae in D. melanogaster also did so in R. pomonella. Preliminary comparative analysis of transcript presences and absences revealed evidence of gene loss in Drosophila and gain in the higher dipteran clade Schizophora.ConclusionsThese data provide a much needed resource for exploring mechanisms of divergence in this important model for sympatric ecological speciation. Our description of ESTs from a substantial portion of the R. pomonella transcriptome will facilitate future functional studies of candidate genes for olfaction and diapause-related life history timing, and will enable large scale expression studies. Similarly, the identification of new SNP and microsatellite markers will facilitate future population and quantitative genetic studies of divergence between the apple and hawthorn-infesting host races.

Project description:Taxa harboring high levels of standing variation may be more likely to adapt to rapid environmental shifts and experience ecological speciation. Here, we characterize geographic and host-related differentiation for 10,241 single nucleotide polymorphisms in Rhagoletis pomonella fruit flies to infer whether standing genetic variation in adult eclosion time in the ancestral hawthorn (Crataegus spp.)-infesting host race, as opposed to new mutations, contributed substantially to its recent shift to earlier fruiting apple (Malus domestica). Allele frequency differences associated with early vs. late eclosion time within each host race were significantly related to geographic genetic variation and host race differentiation across four sites, arrayed from north to south along a 430-km transect, where the host races co-occur in sympatry in the Midwest United States. Host fruiting phenology is clinal, with both apple and hawthorn trees fruiting earlier in the North and later in the South. Thus, we expected alleles associated with earlier eclosion to be at higher frequencies in northern populations. This pattern was observed in the hawthorn race across all four populations; however, allele frequency patterns in the apple race were more complex. Despite the generally earlier eclosion timing of apple flies and corresponding apple fruiting phenology, alleles on chromosomes 2 and 3 associated with earlier emergence were paradoxically at lower frequency in the apple than hawthorn host race across all four sympatric sites. However, loci on chromosome 1 did show higher frequencies of early eclosion-associated alleles in the apple than hawthorn host race at the two southern sites, potentially accounting for their earlier eclosion phenotype. Thus, although extensive clinal genetic variation in the ancestral hawthorn race exists and contributed to the host shift to apple, further study is needed to resolve details of how this standing variation was selected to generate earlier eclosing apple fly populations in the North.

Dataset Information

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

Publications

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

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