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ABSTRACT: Rhagoletis pomonella (Walsh) is an important pest of apples and has been at the center of a long-standing debate concerning modes of speciation. The fly has been proposed to speciate without geographic isolation (i.e., in sympatry) in the process of shifting and adapting to new host plants. Previous studies have shown that diapause-related traits play a key role in adapting apple- and hawthorn-infesting races of R. pomonella to a difference in the fruiting times (phenologies) of their respective host plants. These experiments indicated that prewinter temperature and its duration affected the survivorship and genetics of over-wintering R. pomonella pupae. However, the earlier work did not test whether photoperiod and light intensity, two environmental factors that also differ between the host races, affect the genetics of diapause. Here, we report that variation in photoperiod, but not light intensity, during the larval stage affects adult eclosion. Haw-origin larvae exposed to longer photoperiods (18:6 [L:D] h) eclosed significantly earlier that those experiencing shorter photoperiods (14:10 and 10:14 [L:D] h). We also confirmed previously observed genetic relationships between eclosion time and six allozyme loci displaying allele frequency differences between the haw and apple host races. However, we did not find a significant genetic response to photoperiod for any allozyme. Our results suggest that, while photoperiod cues can regulate R. pomonella diapause, daylength is probably of secondary importance relative to temperature and season length in genetically differentiating the host races.
Annals of the Entomological Society of America 01/2009; · 1.32 Impact Factor
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ABSTRACT: Tephritid fruit flies belonging to the Rhagoletis pomonella sibling species complex are controversial because they have been proposed to diverge in sympatry (in the absence of geographic isolation) by shifting and adapting to new host plants. Here, we report evidence suggesting a surprising source of genetic variation contributing to sympatric host shifts for these flies. From DNA sequence data for three nuclear loci and mtDNA, we infer that an ancestral, hawthorn-infesting R. pomonella population became geographically subdivided into Mexican and North American isolates approximately 1.57 million years ago. Episodes of gene flow from Mexico subsequently infused the North American population with inversion polymorphism affecting key diapause traits, forming adaptive clines. Sometime later (perhaps +/-1 million years), diapause variation in the latitudinal clines appears to have aided North American flies in adapting to a variety of plants with differing fruiting times, helping to spawn several new taxa. Thus, important raw genetic material facilitating the adaptive radiation of R. pomonella originated in a different time and place than the proximate ecological host shifts triggering sympatric divergence.
Proceedings of the National Academy of Sciences 10/2003; 100(18):10314-9. · 9.68 Impact Factor
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ABSTRACT: Evidence suggests that the apple maggot, Rhagoletis pomonella (Diptera: Tephritidae) is undergoing sympatric speciation (i.e., divergence without geographic isolation) in the process of shifting and adapting to a new host plant. Prior to the introduction of cultivated apples (Malus pumila) in North America, R. pomonella infested the fruit of native hawthorns (Crataegus spp.). However, sometime in the mid-1800s the fly formed a sympatric race on apple. The recently derived apple-infesting race shows consistent allele frequency differences from the hawthorn host race for six allozyme loci mapping to three different chromosomes. Alleles at all six of these allozymes correlate with the timing of adult eclosion, an event dependent on the duration of the overwintering pupal diapause. This timing difference differentially adapts the univoltine fly races to an approximately 3- to 4-week difference in the peak fruiting times of apple and hawthorn trees, partially reproductively isolating the host races. Here, we report finding substantial gametic disequilibrium among allozyme and complementary DNA (cDNA) markers encompassing the three chromosomal regions differentiating apple and hawthorn flies. The regions of disequilibrium extend well beyond the previously characterized six allozyme loci, covering substantial portions of chromosomes 1, 2, and 3 (haploid n = 6 in R. pomonella). Moreover, significant recombination heterogeneity and variation in gene order were observed among single-pair crosses for each of the three genomic regions, implying the existence of inversion polymorphism. We therefore have evidence that genes affecting diapause traits involved in host race formation reside within large complexes of rearranged genes. We explore whether these genomic regions (inversions) constitute coadapted gene complexes and discuss the implications of our findings for sympatric speciation in Rhagoletis.
Genetics 04/2003; 163(3):939-53. · 4.01 Impact Factor
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ABSTRACT: Apple [Malus pumila (L.)] and hawthorn (Crataegus spp.) infesting populations of Rhagoletis pomonella Walsh are rapidly becoming a model system for the study of host plant specialization and sympatric race formation. Unfortunately, a major impediment to further progress in the Rhagoletis system is the lack of an adequate framework of genetic information. Here we report on the development of a molecular genetic linkage map for the fly and evaluate the relative merits of alternative strategies that we used to build the map. The most efficient method for detecting polymorphism in R. pomonella was based on screening a complementary DNA (cDNA) library for genetic variation. Twenty-four of the 98 cDNA clones that we attempted to analyze from plaques in the library displayed either restriction site (Alu I, Dde I, Sau 3A, or Taq I), fragment length, or single strand conformation polymorphism that could be mapped in R. pomonella and represented 25 different loci. Linkage group relationships were established for all 25 of these loci. Seven cDNA loci mapped to the 3 regions of the R. pomonella genome where the 6 allozyme loci with significant allele frequency differences between the host races are located. Furthermore, 5 of these 7 cDNA loci were in strong linkage disequilibrium with the allozyme loci residing within 2 of these 3 genomic regions, suggesting that the cDNA linkage map will be useful for dissecting the genetics of race formation in R. pomonella. Another successful strategy that we employed to map the locus glucose-6-phosphate dehijdrogenase (G-6-pdh) involved the use of a set of redundant primers that had been produced based on the conserved amino acid sequence of this gene. Surprisingly, a scheme based on screening plasmid libraries of randomly cloned restriction fragments was ineffective at detecting polymorphism, and it had an overall success rate of only 5.9% (3 mapped loci/51 low copy number clones screened for variation). In addition, application of random amplified polymorphic DNAs was unsuccessful in producing useful markers for the linkage map.
Annals of the Entomological Society of America 06/1997; 90(4):470-479. · 1.32 Impact Factor
