Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly.

Abstract

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

Genetic differentiation in Zeiraphera diniana (Lepidoptera: Tortricidae, the larch budmoth): polymorphism, host races or sibling species?

“…One of the few cases that stands up to close examination is that of the apple versus hawthorn races of Rhagoletis pornonella (Feder et a!., 1988(Feder et a!., , 1994McPheron et a!., 1988;Smith, 1988;Bush et al, 1989). Overall, the scarcity of 'true' host races, as defined above, casts doubt on the idea that sympatric speciation is common.…”

On the scent of speciation: the chemosensory system and its role in premating isolation

“…The recently derived apple-infesting population of R. pomonella, which originated by a shift from hawthorn in the mid-1800s, is considered as an example of host race formation in action, the hypothesized initial stage of sympatric speciation. Reproductive isolation between host races is largely due to host choice because flies mate on their hosts with individuals that have made a similar choice and therefore differences in host preference translate directly into mate choice and premating reproductive isolation (Feder et al, 1994). Therefore, understanding the role of host acceptance and fidelity in host race maintenance and speciation in Rhagoletis requires elucidating the mechanistic basis for differential host choice.…”

“…However, the role of sensory systems in speciation is not restricted to behavioural isolation. Other modalities of premating isolation can involve the divergence of sensory traits (sensory systems and recognition signals): 'pollinator isolation' among angiosperm species due to the divergence of floral traits that promotes pollinator shifts (for example, floral colour divergence in the monkey flowers: Schemske and Bradshaw, 1999); 'habitat isolation' due to the divergence of host or habitat preferences (for example, apple maggot flies : Feder et al, 1994). Although habitat and pollinator isolation both involve behavioural change, we will use the term behavioural isolation to refer more narrowly to traits directly affecting species recognition or mate choice.…”

THE EFFECTS OF WINTER LENGTH ON THE GENETICS OF APPLE AND HAWTHORN RACES OF RHAGOLETIS POMONELLA (DIPTERA: TEPHRITIDAE)

“…Such trade-offs are necessary because mark-release-recapture studies indicate that host-specific mating is not absolute; genetic exchange has been estimated to occur at 6% per generation between the host races at a field site near Grant, Michigan (Feder et al 1994). Some form of host-associated selection is therefore needed to counteract this gene flow or the races would quickly fuse, and long-term allozyme studies indicate that this is not happening at the Grant site (Feder et al 1993.…”