Models of sympatric speciation for phytophagous insects posit a central role for host plant-associated mating as a premating isolating mechanism in lieu of geographic barriers to gene flow. Here, by means of three markand-recapture studies, we confirm that host fidelity (i.e., the tendency of an insect to reproduce on the same host species that it used in earlier life-history stages) restricts gene flow between sympatric apple-and hawthorn-infesting races of Rhagoletis pomonela (Diptera: Tephritidae) to =6% per generation. Genetically based differences in host preference, adult eclosion under the "correct" host species, and allochronic isolation contribute to host fidelity in various degrees in the races. The results verify that host-associated adaptation can produce reproductive isolation as a correlated character (a key premise of sympatric speciation). The study also represents one of the few or perhaps only example in animals where the intra-specific isolating effects of specfic phenotypes have been quantified in nature. although we refer to host-specific taxa, our comments also apply to sympatric divergence based on habitat specialization.) (ii) The semiautonomous nature of host-specific subpopulations ("host races") permits the refinement of hostassociated adaptations (e.g., traits involved in survivorship or performance on a host) that produce reproductive isolation as a correlated character, by either pleiotropy or negative genetic tradeoffs (3, 4). (iii) These host-associated adaptations either isolate the host races to such an extent that they represent distinct species or favor the evolution of additional prezygotic barriers to gene flow that eventually lead to speciation; in the latter case, the additional premating isolation is most likely to involve traits increasing host fidelity, but it could also be caused by the evolution of assortative mating traits not directly tied to host selection (i.e., pheromones, cuticular hydrocarbons, or mating structures).Allozyme studies suggest that hawthorn (Crataegus spp.)-and recently derived apple (Malus pumila)-infesting populations of Rhagoletis pomonella, the apple maggot fly, represent host races in the initial stage of sympatric divergence (5-7). Because these flies mate exclusively on or near the fruit of their host plants (8, 9), a test for the existence and effectiveness of host fidelity (the tendency of an insect to reproduce on the same host species that it used in earlier life-history stages) as a premating isolating mechanism is possible (requirement i for sympatric speciation). Here, by means of three mark-and-recapture studies conducted at a
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 f low 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 metabolisms͞ development rates) in the apple f ly race. By experimentally lengthening the time period preceding winter, we exposed hawthorn race pupae to environmental conditions typically faced by apple f lies. This exposure induced a significant genetic response at six allozyme loci in surviving hawthorn f ly adults toward allele frequencies found in the apple race. The sensitivity of hawthorn f ly pupae to extended periods of warm weather therefore selects against hawthorn f lies that infest apples and helps to maintain the genetic integrity of the apple race by counteracting gene f low 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.Host plant-associated fitness trade-offs are critical for sympatric speciation in phytophagous insects (1). Fitness trade-offs refer to trait(s) or gene(s) that confer a selective advantage to an insect on one plant while incurring a cost on alternative plants. Such trade-offs are important because they can act as postzygotic barriers to gene flow between insect populations specialized on different host plants (1).There is currently little empirical evidence for host plantrelated fitness trade-offs in phytophagous insects (ref. 2, although see refs. 3-5 for some exceptions), which has raised questions concerning the likelihood of sympatric speciation (6). But many tests for fitness trade-offs have concentrated on larval feeding performance and the metabolic detoxification of plant secondary compounds while neglecting potential costs associated with coordinating an insect's life cycle with host plant phenology (7). Here, we test for fitness trade-offs in apple (Malus pumila)-and hawthorn (Crataegus spp.)-infesting populations of the apple maggot fly Rhagoletis pomonella (Diptera: Tephritidae) by examining whether and how differences in the fruiting phenologies (seasonalities) of apple and hawthorn trees affect the genetics of these flies.Previous studies have confirmed the status of apple and hawthorn populations of R. pomonella as g...
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