Abstract
Speciation in many host specific parasites may be initiated in sympatry when populations shift and adapt to new hosts. The recent shift of the apple maggot fly, Rhagoletis pomonella (Diptera: Tephritidae) from its native host plant hawthorn (Crataegus spp.) to introduced, domesticated apple (Malus pumila), provides a direct test of the “sympatric speciation” hypothesis by indicating whether partially reproductively isolated “host races” can evolve in the absence of geographic isolation. We report finding significant allele frequency differences for six allozymes between paired apple and hawthorn infesting populations of R. pomonella from across the midwestern United States. Latitudinal allele frequency clines exist among both apple and hawthorn populations, however, for a majority of the loci displaying racial differences. Inter-host genetic differentiation is therefore superimposed on clinal patterns of variation within the races such that the magnitude of host associated divergence is a function of latitude. The results indicate that host associated races can form in sympatry and implicate differences in host plant recognition and developmental timing (related to ambient temperature) as key factors restricting gene flow between apple and hawthorn populations. However, some of the same processes differentiating apple and hawthorn populations at sympatric sites also appear to be occurring within the two host races across their respective ranges. R. pomonella populations are therefore diverging with respect to both their host plant affiliations and local environmental conditions.
Similar content being viewed by others
Article PDF
References
Berlocher, S H. 1976. The genetics of speciation in Rhagoletis (Diptera: Tephritidae). Ph.D. Thesis, University of Texas at Austin.
Berlocher, S H. 1984. Genetic changes coinciding with the colonization of California by the walnut husk fly, Rhagoletis completa. Evolution, 38, 906–918.
Berlocher, S H, and Bush, G L. 1982. An electrophoretic analysis of Rhagoletis (Diptera: Tephritidae) phylogeny. Syst Zool, 31, 136–155.
Berlocher, S H, and Smith, D C. 1983. Segregation and mapping of allozymes of the apple maggot fly. J Hered, 74, 337–340.
Berger, E M. 1971. A temporal survey of allelic variation in natural and laboratory populations of Drosophila melanogaster. Genetics, 67, 121–136.
Boller, E F, and Prokopy, R J. 1976. Bionomics and management of Rhagoletis. Ann Rev Ent, 21, 223–246.
Bourne, A I, Thies, W H, and Shaw, F R. 1934. Some observations on long distance dispersal of apple maggot flies. J Econ Ent, 27, 352–355.
Buriff, C R. 1973. Recapture of released adult apple maggot flies on sticky-board traps. Environ. Entomol, 2, 757–758.
Bush, G L. 1966. The taxonomy, cytology and evolution of the genus Rhagoletis in North America (Diptera: Tephritidae). Museum of Comparative Zoology, Cambridge, Mass., U.S.A.
Bush, G L. 1969a. Sympatric host race formation and speciation in frugivorous flies of the genus Rhagoletis (Diptera: Tepthritidae). Evolution, 23, 237–251.
Bush, G L. 1969b. Mating behavior, host specificity, and the ecological significance of sibling species in frugivorous flies of the genus Rhagoletis (Diptera: Tephritidae). Am Nat, 103, 669–672.
Bush, G L. 1975. Modes of animal speciation. Ann Rev Ecol Syst, 6, 339–364.
Chapman, P J, and Lienk, S E. 1971. Toitricid Fauna of Apple in New York, Cornell Univ., Ithaca, New York.122pp.
Christiansen, F B, and Frydenberg, O. 1974. Geographic patterns of four polymorphisms in Zoarces viviporus as evidence of selection. Genetics, 77, 765–770.
Christiansen, F B, and Feldman, M W. 1975. Subdivided populations: A review of the one- and two-locus deterministic theory. Theor Pop Biol, 7, 13–38.
Clegg, M T, and Allard, R W. 1972. Patterns of genetic differentiation in the slender wild oat species, Avena barbata. PNAS, 69, 1820–1824.
Correll, D S, and Johnston, M C. 1970. Manual of the Vascular Plants of Texas. Texas Research Foundation, Renner, Texas, 1881pp.
Diehl, S R, and Bush, G L. 1984. An evolutionary and applied perspective of insect biotypes. Ann Rev Entomol, 29, 471–504.
Endler, J A. 1977. Geographic Variation, Speciation, and Clines. Princeton University Press, Princeton, New Jersey.
Feder, J L, and Bush, G L. Differential host utilization is an effective premating barrier between sibling species in the Rhagoletis pomonella group. Evolution (submitted).
Feder, J L, Chilcote, C A, and Bush, G L. 1988. Genetic differentiation between sympatric host races of the apple maggot fly, Rhagoletis pomonella. Nature, 336, 61–64.
Feder, J L, Chilcote, C A, and Bush, G L. 1989a. Geographic pattern of genetic differentiation between host associated populations of Rhagoletis pomonella (Diptera: Tephritidae) in the eastern United States and Canada. Evolution (In press).
Feder, J L, Chilcote, C A, and Bush, G L. 1989b. Inheritance and linkage relationships of allozymes in the apple maggot fly. J Hered, 80, 277–283.
Feder, J L, Chilcote, C A, and Bush, G L. 1989c. Regional, local and microgeographic allele frequency variation between host faces of Rhagoletis pomonella in western Michigan. Evolution (In press).
Feder, J L, Chilcote, C A, and Bush, G L. 1989d. Are the apple maggot, Rhagoletis pomonella and the blueberry maggot, R. mendax, distinct species? Implications for sympatric speciation. Entomol Exp Appl (In press).
Fein, B L, Reissig, W H, and Roelofs, W L. 1982. Identification of apple volatiles attractive to the apple maggot, Rhagoletis pomonella. J Chem Ecol, 8, 1473–1487.
Felsenstein, J. 1976. The theoretical population genetics of variable selection and migration. Ann Rev Genet, 10, 253–280.
Fernald, M L. 1950. Gray's Manual of Botany, 8th edn. American Book Company, New York, 1632PP.
Fisher, R A F. 1930. The Genetical Theory of Natural Selection. Clarendon Press. Oxford, England.
Hedrick, P W, Ginevan, M E, and Ewing, E P. 1976. Genetic polymorphism in heterogeneous environments. Ann Rev Ecol Syst, 7, 1–32.
Holm, S. 1979. A simple sequential rejective multiple test procedure. Scan J Stat, 6, 65–70.
Illingworth, J F. 1912. A study of the biology of the apple maggot (Rhagoletis pomonella), together with an investigation of methods of control. Cornell Univ Agr Expt Stat Bull, 324, 129–187.
Johnson, F M, and Schaffer, H E. 1973. Isozyme variability in species of the genus Drosophila. VII. Genotype-environmental relationships in populations of Drosophila melanogaster from the eastern United States. Biochem Genet, 10, 149–163.
Johnson, G B. 1976. Polymorphism and predictability of the alpha-glycerophosphate dehydrogenase locus in Colias butterflies. Biochem Genet, 14, 403–425.
Johnson, M S. 1971. Adaptive lactate dehydrogenase variation in the crested blenny, Anoplorchus. Heredity, 27, 205–226.
Koehn, R K. 1969. Esterase heterogeneity: Dynamics of a polymorphism. Science, 163, 943–944.
Koehn, R K, Milkman, R, and Mitton, J B. 1976. Population genetics of marine pelecypods. IV. Selection, migration and genetic differentiation in the blue mussel, Mytilus edulis. Evolution, 30, 2–32.
Levene, H. 1953. Genetic equilibrium when more than one ecological niche is available. Am Nat, 87, 331–333.
Levins, R. 1968. Evolution in Changing Environments. Princeton University Press, Princeton, New Jersey.
Maxwell, C W. 1968. Apple maggot adult dispersion in a New Brunswick apple orchard. J Econ Ent, 61, 103–106.
Maxwell, C W, and Parsons, E C. 1968. The recapture of marked apple maggot adults in several orchards from one release point. J Econ Ent, 61, 1157–1159.
Maynard Smith, J. 1966. Sympatric speciation. Am Nat, 100, 637–650.
Maynard Smith, J. 1970. Genetic polymorphism in a varied environment. Am Nat, 104, 487–490.
McPheron, B A. 1987. The population genetics of the colonization of the western United States by the apple maggot, Rhagoletis pomonella (Walsh) (Diptera: Tephritidae). Ph.D. Dissertation, Univ. of Illinois, Urbana, Illinois.
McPheron, B A, Smith, D C, and Berlocher, S H. 1988a. Genetic differences between host races of the apple maggot fly. Nature, 336, 64–66.
McPheron, B A, Jorgensen, C D, and Berlocher, S H. 1988b. Low genetic variability in a Utah cherry-infesting population of the apple maggot, Rhagoletis pomonella. Entomol Exp Appl, 46, 155–160.
Merritt, R B. 1972. Geographic distribution and enzymatic properties of lactate dehydrogenase allozymes in the fat head minnow, Pimephales promelas. Am Nat, 196, 173–184.
Miller, S, Pearcy, R W, and Berger, E. 1975. Polymorphism at the alpha-glycerophosphate dehydrogenase locus in Drosophila melanogaster. I. Properties of adult allozymes. Biochem Genet, 13, 175–188.
Mitton, J B, and Koehn, R K. 1975. Genetic organization and adaptive response of allozymes to ecological variables in fundulus heteroclitus. Genetics, 79, 97–111.
Moericke, V, Prokopy, R J, Berlocher, S, and Bush, G L. 1975. Visual stimuli eliciting attraction of Rhagoletis pomonella flies to trees. Entomol Exp Appl, 18, 497–507.
Muniyamma, M, and Phipps, J B. 1984. Studies in Crataegus. XI. Further cytological evidence for the occurrence of apomixis in North American hawthorns. Can J Bot, 62, 2316–2324.
Muniyamma, M, and Phipps, J B. 1985. Studies in Crataegus. XII. Cytological evidence for sexuality in some diploid and tetraploid species of North American hawthorns. Can J Bot, 63, 1319–1324.
Murray, J. 1972. Genetic Diversity and Natural Selection. Oliver and Boyd. Edinburgh, Scotland.
Neilson, W T A. 1971. Dispersal studies of a natural population of apple maggot adults. J Econ Ent 64 (3) 648–653.
O'Kane, W C. 1914. The apple maggot. New Hampshire Expt Sta Bull, No. 171, 120 pp.
Owens, E D, and Prokopy, R J. 1986. Relationship between reflectance spectra of host plant surfaces and visual detection of host fruit by Rhagoletis pomonella flies. Physiol Entomol, 11, 297–307.
Papaj, D R, and Prokopy, R J. 1986. Phytochemical basis of learning in Rhagoletis pomonella and other herbivorous insects. J Chem Ecol, 12, 1125–1143.
Phipps, C R, and Dirks, C O. 1933. Dispersal of the apple maggot fly—1932 studies. J Econ Ent, 5, 576–582.
Phipps, J B. 1983. Biogeographic, Taxonomie, and Cladistic relationships between East Asiatic and North American Crataegus. Ann Missouri Bot Gard, 70, 667–700.
Phipps, J B. 1984. Problems of hybridity in the cladistics of Crataegus. In Grant, W. F., (ed.) Plant Biosystematics Academic Press, Toronto, Canada, pp. 417–438.
Porter, B A. 1928. The Apple Maggot. US Dept Agr Tech Bull 66, 48 pp.
Prokopy, R J. 1968a. Visual responses of apple maggot flies, Rhagoletis pomonella: Orchard studies. Entomol Exp Appl, 11, 403–422.
Prokopy, R J. 1968b. Influence of photoperiod, temperature and food on the initiation of diapause in the apple maggot. Canad Ent, 100, 318–329.
Prokopy, R J, Bennett, E W, and Bush, G L. 1971. Mating behavior in Rhagoletis pomonella (Diptera: Tephritidae). I. Site of assembly. Canad Ent, 103, 1405–1409.
Prokopy, R J, Bennett, E W, and Bush, G L. 1972. Mating behavior in Rhagoletis pomonella (Diptera: Tephritidae). II. Temporal organization. Canad Ent, 104, 97–104.
Prokopy, R J, Moericke, E, and Bush, G L. 1973. Attraction of apple maggot flies to odor of apples. Envir Entomol, 2, 112–119.
Prokopy, R J, Averill, A L, Cooley, S S, and Roitberg, C A. 1982. Associative learning in egglaying site selection by apple maggot flies. Science, 218, 76–77.
Prokopy, R J, Papaj, D R, Cooley, S S, and Kallet, C. 1986. On the nature of learning in oviposition site acceptance by apple maggot flies. Anim Behav, 34, 98–107.
Prokopy, R J, Aluja, M, and Green, T A. 1987. Dynamics of host odor and visual stimulus interaction in host finding behavior of apple maggot flies. In Labeyrie, V., Fabres, G. and Lachaise, D. (eds) Insects-Plants, Junk, Netherlands, pp. 161–166.
Prokopy, R J, Diehl, S R, and Cooley, S S. 1988. Behavioral evidence for host races in Rhagoletis pomonella flies. Oecologia, 76, 138–147.
Resissig, W H. 1977. Capture of released apple maggot flies, Rhagoletis pomonella (Diptera: Tephritidae), on sticky panels. Can Ent, 109, 631–634.
Reissig, W H, and Smith, D C. 1978. Bionomics of Rhagoletis pomonella in Crataegus. Ann Ent Soc Amer, 71, 155–159.
Reissig, W H, Barnard, J, Weires, R W, Glass, E H, and Dean, R W. 1979. Prediction of apple maggot fly emergence from thermal unit accumulation. Environ Entomol, 8, 51–54.
Rice, W R. 1989. Analyzing tables of statistical tests. Evolution, 43, 223–225.
Roitberg, B D, van Lenteren, J C, van Alphen, J J M, Galis, F, and Prokopy, R J. 1982. Foraging behavior of Rhagoletis pomonella, a parasite of hawthorn (Crataegus), in nature. J Anim Ecol, 51, 307–325.
Scriber, J M, and Hainze, J H. 1987. Geographic invasion and abundance as facilitated by differential host plant utilization abilities. In Barbosa, P. and Shultz, J. C. (eds) Insect Outbreaks: Ecology and Evolutionary Processes, Academic Press, New York, pp. 433–468.
Showers, W B. 1981. Geographic variation of the diapause response in the European corn borer. In Denno, R. F. and Dingle, H. (eds) Insect Life History Patterns, SpringerVerlag, Berlin and New York, pp. 97–111.
Smith, D C. 1988. Heritable divergence of Rhagoletis pomonella host races by seasonal asynchrony. Nature, 336, 66–67.
Spiess, E B. 1977. Genes in Populations. Wiley and Sons, New York.780 pp.
Standley, P C. 1922. Trees and Shrubs of Mexico. Smithsonian Press, Washington, D.C., 1721 pp.
Vigue, C L, and Johnson, F M. 1973. Isozyme variability in speces of the genus Drosophila. VI. Frequency-property-environment relationships of allelic alcohol dehydrogenase in D. melanogaster. Biochem Genet, 9, 213–227.
Walsh, B J. 1867. The apple-worm and the apple maggot. J Hort, 2, 338–343.
Wasbauer, M S. 1972. An annotated host catalog of the fruit flies of America north of Mexico (Diptera: Tephritidae). Bureau of Entomol, Dept of Agric, Sacramento, Calif. Occasional papers no. 19.
Weir, B S, and Cockerham, C C. 1984. Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358–1370.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Feder, J., Bush, G. Gene frequency clines for host races of Rhagoletis pomonella in the Midwestern United States. Heredity 63, 245–266 (1989). https://doi.org/10.1038/hdy.1989.98
Received:
Issue Date:
DOI: https://doi.org/10.1038/hdy.1989.98
This article is cited by
-
Variation in host usage among geographic populations of Leptinotarsa decemlineata, the Colorado potato beetle
Journal of Pest Science (2014)
-
10.1007/BF00189367
CrossRef Listing of Deleted DOIs (2011)
-
Population structure of Rhagoletis pomonella, the apple maggot fly
Heredity (1996)
-
Population structure of Rhagoletis mendax, the blueberry maggot
Heredity (1995)
-
Intra- and interspecific competition and host race formation in the apple maggot fly, Rhagoletis pomonella (Diptera: Tephritidae)
Oecologia (1995)