Gene frequency clines for host races of Rhagoletis pomonella in the Midwestern United States

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 dines 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. INTRODUCTIONSpeciation, the rendering of one closed genetic system into two, is a fundamental process responsible for the evolution of life on earth. Unfortunately, because speciation is a relatively rare, often time consuming event, much of our understanding of the process is based on population genetics models and indirect analyses of closely related species. We therefore have very few examples directly documenting how populations become reproductively isolated from one another.The apple maggot fly, Rhagoletis pomonella, is an exception, however, having a biology and natural history which makes it ideal for the empirical study of speciation. R. pomonella is part of an endemic, sibling species complex of true fruit flies whose members overlap broadly in their geographic distributions across North America (Bush, 1966). Rhagoletis larvae are internal parasites in the fruit of their hosts, with each species in the group being monophagous or oligophagous for a different set of host plants (Bush, 1966). Adult females lay their eggs directly into the host fruit which they identify by specific visual, tactile and olfactory cues (Prokopy, 1968a;Prokopy et a!., 1973Prokopy et a!., , 1987Prokopy et a!., , 1988Moericke et a!., 1975;Fein et a!., 1982;Owens and Prokopy, 1986;Papaj and Prokopy, 1986). Males are attracted by the same cues and courtship and mating occurs almost exclusively on or near the fruits of the host plant (Prokopy et a!., 1971(Pr...

Population structure of Rhagoletis mendax, the blueberry maggot

“…R. mendax is almost uniform across its range, with little differentiation (FsT=O.O15) and no clinal structure whereas R. pomonella is quite structured, with very significant differentiation (F1 0.220; McPheron, 1987) and strong clinal structure (Feder & Bush, 1989). The genetic uniformity of R. mendax is from a lack of variation; based on the 29 locus data set variable loci (partially different from the set used here), and observed FsT=O.O4O±O.Ol3, which is probably not significantly greater than the value reported here (Feder & Bush (1989) report a variance of F51 from bootstrapping instead of 95 per cent confidence limits). With respect to linkage disequilibrium, differences between R. pomonella and R. mendax are also apparent.…”

“…1 Because nomenclature, electrophoretic conditions, staining recipes and map positions for R. pornonella group electrophoretic loci have been previously described in detail (Berlocher & Smith, 1983;, only locus names are used here. Although as many as 29 loci have been scored from single Rhagoletis flies (Feder et at., 1989), the data set analysed here contains 16 polymorphic loci (polymorphic = more than one allele), all expressed in both larvae and adults (Berlocher & Smith, 1983;Feder et al, 1989). The loci that were excluded from analysis were either invariant in R. mendax or could not be reliably scored for technical reasons (the relatively small size of southern R. mendax was a contributing factor).…”

“…Electrophoretic and phenological studies have revealed several features of the biology and population genetics of the species that are potentially related, to varying degrees, to its ability to colonize novel plants. R. pomonella possesses abundant variation, at least for allozymes (average heterozygosity over 29 loci is 0.22 1 0.44; , populations are structured even at the level of individual host plants (McPheron et a!., 1988a;Feder et a!., 1990b), latitudinal allele frequency dines exist, with different slopes in the apple and hawthorn races (Feder & Bush, 1989), geographical differentiation over eastern North America is great (FST= 0.220;McPheron, 1987), linkage disequilibrium of allozyme loci involved in host race differentiation exists (Feder et a!., 1990a), and different allozyme genotypes are associated with different diapause and eclosion phenologies .…”

Fruit odor discrimination and sympatric host race formation in Rhagoletis

“…Apple and hawthorn flies were collected as larvae from infested fruit in Grant, MI, Fennville, MI, and Urbana, IL, during the 1999-2003 field seasons, and reared to adulthood in the laboratory by using standard protocols (19). Apple and hawthorn populations at these three sites have been the subject of previous ecological and genetic studies and have been shown to differ significantly from one another in allozyme frequencies (20)(21)(22)(23)(24). Eclosing adults were kept in cages in an environmental chamber at 23-24°C, 16 h light͞8 h dark photoperiod, 60-70% relative humidity, and fed an artificial diet containing water, sugar, vitamins, casein hydrolysate, and a salt mixture (25).…”

Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis

“…Host plant-related differentiation in R. pomonella is superimposed on a broader pattern of geographic variation (14)(15)(16)(17). (Note: the distribution of the apple race is limited to the northeastern and midwestern United States and Canada, whereas the range of haw flies extends into Mexico; Fig.…”