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. 1997 Oct 14;94(21):11417-21.
doi: 10.1073/pnas.94.21.11417.

Selective maintenance of allozyme differences among sympatric host races of the apple maggot fly

J L Feder  1 , J B Roethele, B Wlazlo, S H Berlocher
Affiliations

Selective maintenance of allozyme differences among sympatric host races of the apple maggot fly

J L Feder et al. Proc Natl Acad Sci U S A. .

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.

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Figures

Figure 1
Figure 1
Percentages of hawthorn-origin pupae that eclosed as diapausing adults (▴, flies eclosing after 30-week chilling period) and nondiapausing (•, flies eclosing before chilling) for the 2- to 32-day prewinter treatments. Total number of pupae in each prewinter treatment are given in parentheses.
Figure 2
Figure 2
(a–c) Allele frequencies for Me 100, Acon-2 95, and Mpi 37 in diapausing (▴) and nondiapausing (•) hawthorn -adults in the 2- to 32-day prewinter treatments. Allele frequencies for baseline apple and hawthorn fly control samples are designated by dashed lines. Sample sizes (number of flies scored) are given in a in parentheses. d, significant allele frequency difference between diapausing flies and hawthorn control sample as determined by one-tailed, randomized Fisher exact tests; n, significant difference between nondiapausing flies and hawthorn control sample; t, significant difference between diapause and nondiapause flies in the 32-day treatment. Number of letters designates significance level (one letter, P < 0.05; two, P < 0.01; three, P < 0.001; and four, P < 0.0001). Linear regressions (r2 and P values, 5 df) for arcsin-transformed allele frequencies vs. percentage survivorship (surv) and length of prewinter treatment (days) also are given.
Figure 3
Figure 3
(a–c) Allele frequencies for Dia-2 100, Aat-2 +75, and Had 100 in diapausing (▴) and nondiapausing (•) hawthorn adults in the 2- to 32-day prewinter treatments. See Fig. 2 legend for complete details. +75 for Aat-2 refers to the pooled frequency of all alleles of electrophoretic mobility ≥75 relative to the most common 100 allele. Previous studies have indicated that the + 75 and −75 classes of Aat-2 alleles are in very strong linkage disequilibrium with the 100 and 70 alleles, respectively, at the Dia-2 locus (7, 9, 26).
Figure 4
Figure 4
Allele frequencies for Acon-2 95 in apple (•) and hawthorn (▴) fly races at Grant, MI, from 1984–1994 (year N) plotted against growing degree days (GDD) base 50°F in the spring (March-June) of the preceding year (N − 1). Year numbers (N) and sample sizes (number of flies scored) for allozymes appear in parentheses. Linear regressions (r2 and P values, 10 df) for arcsin-transformed allele frequencies vs. growing degree days for all of the allozymes are given in the table.
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