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Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella

Abstract

In On the Origin of Species, Darwin proposed that natural selection had a fundamental role in speciation1. But this view receded during the Modern Synthesis when allopatric (geographic) models of speciation were integrated with genetic studies of hybrid sterility and inviability2,3. The sympatric hypothesis posits that ecological specialization after a host shift can result in speciation in the absence of complete geographic isolation4,5. The apple maggot, Rhagoletis pomonella, is a model for sympatric speciation in progress4,5. Hawthorn (Crataegus spp.) is the native host for R. pomonella in N. America5. But in the mid-1800s, a new population formed on introduced, domesticated apple (Malus pumila)4,5. Recent studies6,7,8,9,10 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.

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Figure 1: Seasonal distributions of fly larvae.
Figure 2: Comparisons of allele frequencies in eclosing adults.
Figure 3: Absolute fitness estimates for Me 100 genotypes related to winter length.

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References

  1. Darwin, C. The Origin of Species by Means of Natural Selection (Murray, London, 1859).

    Google Scholar 

  2. Dobzhansky, T. Genetics and the Origins of Species (Columbia Univ. Press, New York, 1937).

    Google Scholar 

  3. Mayr, E. Systematics and the Origin of Species (Columbia Univ. Press, New York, 1942).

    Google Scholar 

  4. Bush, G. L. in Evolutionary Strategies of Parasitic Insects and Mites (ed. Price, P. W.) 187–206 (Plenum, New York, 1975).

    Book  Google Scholar 

  5. Bush, G. L. The Taxonomy, Cytology and Evolution of the Genus Rhagoletis in North America (Museum of Comparative Zoology, Cambridge, Massachusetts, 1966).

    Google Scholar 

  6. Prokopy, R. J., Diehl, S. R. & Cooley, S. S. Behavioral evidence for host races in Rhagoletis pomonella flies. Oecologia 76, 138– 147 (1988).

    Article  ADS  Google Scholar 

  7. Feder, J. L., Chilcote, C. A. & Bush, G. L. Genetic differentiation between sympatric host races of Rhagoletis pomonella. Nature 336, 61–64 (1988).

    Article  ADS  Google Scholar 

  8. McPheron, B. A., Smith, D. C. & Berlocher, S. H. Genetic differences between Rhagoletis pomonella host races. Nature 336, 64– 66 (1988).

    Article  ADS  Google Scholar 

  9. Feder, J. L. et al. Host fidelity is an effective pre-mating barrier between sympatric races of the apple maggot fly. Proc. Natl Acad. Sci. USA 91, 7990–7994 (1994).

    Article  ADS  CAS  Google Scholar 

  10. Feder, J. L. & Filchak, K. E. It's about time: The evidence for host plant-mediated selection in the apple maggot fly, Rhagoletis pomonella , and its implications for fitness trade-offs in phytophagous insects. Ent. Exp. Appl. 91, 211– 225 (1999).

    Article  Google Scholar 

  11. Prokopy, R. J., Bennett, E. W. & Bush, G. L. Mating behavior in Rhagoletis pomonella (Diptera: Tephritidae). I. Site of assembly. Canad. Ent. 103, 1405–1409 (1971).

    Article  Google Scholar 

  12. Feder, J. L. & Bush, G. L. A field test of differential host plant usage between two sibling species Rhagoletis pomonella fruit flies (Diptera: Tephritidae) and its consequences for sympatric models of speciation. Evolution 43, 1813– 1819 (1989).

    Article  Google Scholar 

  13. Reid, J. A. & Laing, J. E. Development threshold and degree-days to adult emergence for overwintering pupae of the apple maggot, Rhagoletis pomonella (Walsh) collected in Ontario. Proc. Ent. Soc. Ontario 197, 19–22 ( 1976).

    Google Scholar 

  14. Via, S. in Ecological Genetics (ed. Real, L. A.) 58–85 (Princeton Univ. Press, Princeton, New Jersey, 1994).

    Google Scholar 

  15. Craig, T. P., Horner, J. D. & Itami, J. K. Hybridization studies on the host races of Eurosta solidaginis: Implications for sympatric speciation. Evolution 51, 1552–1560 ( 1997).

    PubMed  Google Scholar 

  16. Thompson, J. N. The Coevolutionary Process (Univ. Chicago Press, Chicago, 1994).

    Book  Google Scholar 

  17. Abrahamson, W. G. et al. in Gall-Forming Insects (eds Price, P., Mattson, W. & Baranchilov, Y.) 208–222 (USDA Forest Service Tech. Report NC-174, St. Paul, Minnesota, 1994).

    Google Scholar 

  18. Wood, T. K. & Keese, M. C. Host-plant-induced assortative mating in Echenopa treehoppers. Evolution 44, 619–628 (1990).

    Article  Google Scholar 

  19. Tauber, C. A. & Tauber, M. J. in Speciation and Its Consequences (eds Otte, D. & Endler, J. A.) 307–344 (Sinauer, Sunderland, Massachusetts, 1989).

    Google Scholar 

  20. Fry, J. D. The evolution of host specialization: are trade-offs overrated? Am. Nat. 148, S84–S107 ( 1996).

    Article  Google Scholar 

  21. Feder, J. L. in Endless Forms: Species and Speciation (eds Howard, D. & Berlocher, S. H.) 130–144 (Oxford Univ. Press, New York, 1998).

    Google Scholar 

  22. Farrell, B. D. “Inordinate fondness” explained: Why are there so many beetles? Science 281, 555–558 (1998).

    Article  CAS  Google Scholar 

  23. Roethele, J. B. et al. Towards a molecular genetic linkage map for the apple maggot fly, Rhagoletis pomonella (Diptera:Tephritidae): a comparison of alternative strategies. Ann. Entomol. Soc. Am. 90, 470 –479 (1997).

    Article  CAS  Google Scholar 

  24. Lathrop, F. H. & Nickels, C. B. The biology and control of the blueberry maggot in Washington County Maine (Tech. Bull. 275 US Dept of Agriculture, Washington DC, 1932).

    Google Scholar 

  25. Feder, J. L. The effects of parasitoids on sympatric host races of the apple Maggot fly, Rhagoletis pomonella (Diptera: Tephritidae). Ecology 76, 801–813 (1995).

    Article  Google Scholar 

  26. Filchak, K. E. et al. A field test for host-plant dependent selection on larvae of the apple maggot fly, Rhagoletis pomonella. Evolution 53, 187–220 ( 1999).

    Article  Google Scholar 

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Acknowledgements

We thank S. Berlocher, J. Carbol, H. Dambroski, G. Dwyer, V. Gavrilovic, D. Gibbons, D. Lodge, B. Perry, D. Prokrym, U. Stolz, S. Via and the USDA lab at Niles, Michigan. This work was supported by grants from NSF (Young investigators, Integrative Research Challenges & GRT) and the USDA to J.L.F and the University of Notre Dame.

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Correspondence to Kenneth E. Filchak.

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Filchak, K., Roethele, J. & Feder, J. Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella. Nature 407, 739–742 (2000). https://doi.org/10.1038/35037578

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