Joseph B. Roethele

University of Notre Dame, Box Elder, SD, United States

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Publications (10)80.85 Total impact

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    Kenneth E. Filchak, Joseph B. Roethele, Jeffrey L. Feder
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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; 94(Nov 2001):902-908. DOI:10.1603/0013-8746(2001)094[0902:EOPALI]2.0.CO;2 · 1.17 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. DOI:10.1073/pnas.1730757100 · 9.81 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. · 4.87 Impact Factor
  • Annals of the Entomological Society of America 11/2001; 94(6):936-947. DOI:10.1603/0013-8746(2001)094[0936:EFBSCO]2.0.CO;2 · 1.17 Impact Factor
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    K E Filchak, J B Roethele, J L Feder
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    ABSTRACT: In On the Origin of Species, Darwin proposed that natural selection had a fundamental role in speciation. But this view receded during the Modern Synthesis when allopatric (geographic) models of speciation were integrated with genetic studies of hybrid sterility and inviability. The sympatric hypothesis posits that ecological specialization after a host shift can result in speciation in the absence of complete geographic isolation. The apple maggot, Rhagoletis pomonella, is a model for sympatric speciation in progress. Hawthorn (Crataegus spp.) is the native host for R. pomonella in N. Americas. But in the mid-1800s, a new population formed on introduced, domesticated apple (Malus pumila). Recent studies have conferred 'host race' status on apple flies as a potentially incipient species, partially isolated from haw flies owing to host-related adaptation. However, the source of selection that differentiates apple and haw flies is unresolved. Here we document a gene-environment interaction (fitness trade-off) that is related to host phenology and that genetically differentiates the races.
    Nature 11/2000; 407(6805):739-42. DOI:10.1038/35037578 · 42.35 Impact Factor
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    ABSTRACT: Host-plant dependent fitness trade-offs refer to traits that enhance the performance of an insect on one plant species to its detriment on others. Such trade-offs are central to models of sympatric speciation via host shifts, but have proven difficult to empirically demonstrate.Here, we test for host-plant dependent selection on larvae of apple (Malus pumila L.) and hawthorn (Crataegus mollis L. spp.)-infesting races of Rhagoletis pomonella (Walsh). Samples of larvae were reared in the field and under protective conditions in a garage. Our rationale was that the garage should slow rates of fruit rot relative to the field, relaxing selection pressures associated with declining fruit quality. Four findings emerged from the study. (1) Larvae suffered higher mortality in fruits in the field than the garage. (2) The increase in mortality was greater for larvae in haws. (3) Larvae possessing the alleles Me 100, Acon-2 95, and Mpi 37, three allozymes displaying host-related differentiation in R. pomonella that map to linkage group II in the fly, left fruits earlier than other genotypes. (4) Allele frequencies for Me 100, Acon-2 95, and Mpi 37 were significantly higher in both apple and haw larvae surviving the field versus the garage treatment.Our results suggested that field conditions favored larvae that rapidly developed and left rotting fruits. Since these individuals tended to possess the alleles Me 100, Acon-2 95, and Mpi 37, frequencies of these allozymes were higher in the field. Selection on larvae was directional for Me 100, Acon-2 95, and Mpi 37 (or linked genes) in both host races. We previously showed that these same alleles can be disfavored in the pupal stage, especially in the apple race, where they correlate with premature diapause termination. Fitness trade-offs in Rhagoletis may therefore be due as much to differences in the relative strengths of directional selection pressures acting on different life stages as to disruptive selection affecting any one particular stage. The necessity to consider details of the entire life-cycle highlights one of the many challenges posed to documenting fitness trade-offs for phytophagous insects.
    Evolution 02/1999; 53:187-200. DOI:10.2307/2640931 · 4.66 Impact Factor
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    ABSTRACT: Host plant-associated fitness trade-offs are central to models of sympatric speciation proposed for certain phytophagous insects. But empirical evidence for such trade-offs is scant, which has called into question the likelihood of nonallopatric speciation. Here, we report on the second in a series of studies testing for host-related selection on pupal life-history characteristics of apple- (Malus pumila L.) and hawthorn- (Crataegus mollis L. spp.) infesting races of the Tephritid fruit fly, Rhagoletis pomonella (Walsh). In particular, we examine the effects of winter length on the genetics of these flies. We have previously found that the earlier fruiting phenology of apple trees exposes apple-fly pupae to longer periods of warm weather preceding winter than hawthorn-fly pupae. Because R. pomonella has a facultative diapause, we hypothesized that this selects for pupae with more recalcitrant pupal diapauses (or slower metabolic/development rates) in the apple-fly race. A study in which we experimentally manipulated the length of the prewintering period for hawthorn-origin pupae supported this prediction. If the period preceding winter is important for apple- and hawthorn-fly pupae, then so too should be the length (duration) of winter; the rationale for this prediction is that 'fast developing' pupae that break diapause too early will deplete their energy reserves and disproportionately die during long winters. To test this possibility, we chilled apple- and hawthorn-origin pupae collected from a field site near Grant, Michigan, in a refrigerator at 4⚬C for time periods ranging from one week to two years. Our a priori expectation was that longer periods of cold storage would select against allozyme markers that were associated with faster rates of development in our earlier study. Since these electromorphs are typically found at higher frequencies in hawthorn flies, extending the overwintering period should favor 'apple-fly alleles' in both races. The results from this 'overwinter' experiment supported the diapause hypothesis. The anticipated genetic response was observed in both apple and hawthorn races, as allele frequencies became significantly more 'apple-fly-like' in eclosing adults surviving longer chilling periods. This indicates that it is the combination of environmental conditions before and during winter that selects on the host races. Many tests for trade-offs fail to adequately consider the interplay between insect development, host plant phenology, and local climatic conditions. Our findings suggest that such oversight may help to explain the paucity of reported fitness trade-offs.
    Evolution 12/1997; 51(6):1862. DOI:10.2307/2411008 · 4.66 Impact Factor
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    J L Feder, J B Roethele, B Wlazlo, S H Berlocher
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    ABSTRACT: Whether phytophagous insects can speciate in sympatry when they shift and adapt to new host plants is a controversial question. One essential requirement for sympatric speciation is that disruptive selection outweighs gene flow between insect populations using different host plants. Empirical support for host-related selection (i.e., fitness trade-offs) is scant, however. Here, we test for host-dependent selection acting on apple (Malus pumila)- and hawthorn (Crataegus spp.)-infesting races of Rhagoletis pomonella (Diptera: Tephritidae). In particular, we examine whether the earlier fruiting phenology of apple trees favors pupae in deeper states of diapause (or with slower metabolisms/development rates) in the apple fly race. By experimentally lengthening the time period preceding winter, we exposed hawthorn race pupae to environmental conditions typically faced by apple flies. This exposure induced a significant genetic response at six allozyme loci in surviving hawthorn fly adults toward allele frequencies found in the apple race. The sensitivity of hawthorn fly pupae to extended periods of warm weather therefore selects against hawthorn flies that infest apples and helps to maintain the genetic integrity of the apple race by counteracting gene flow from sympatric hawthorn populations. Our findings confirm that postzygotic reproductive isolation can evolve as a pleiotropic consequence of host-associated adaptation, a central tenet of nonallopatric speciation. They also suggest that one reason for the paucity of reported fitness trade-offs is a failure to consider adequately costs associated with coordinating an insect's life cycle with the phenology of its host plant.
    Proceedings of the National Academy of Sciences 11/1997; 94(21):11417-21. DOI:10.1073/pnas.94.21.11417 · 9.81 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. DOI:10.1093/aesa/90.4.470 · 1.17 Impact Factor
  • J. B. Roethele, J. Romero-Severson, J. L. Feder
    Annals of the Entomological Society of America 94(6):936-947. · 1.17 Impact Factor