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Biodiversity is an inherent outcome of evolution. Despite substantial progress toward discerning the nature of the evolutionary processes shaping and maintaining biodiversity , critical questions still remain. For example, what traits promote rapid speciation and how do they originate? Are certain groups of organisms more diverse than others and, if so, why? The Role of Nonhost Avoidance in Insect Specialization Phytophagous insects are the most prevalent form of animal life on Earth. Weis and Berenbaum (1989) estimate roughly 361,000 species of plant-feeding insects, compared to their roughly 308,000 species of green plant hosts. Most phytophagous insects are relative specialists, feeding, mating, and ovipositing on a limited subset of possible plants. Moreover , adoption of phytophagy has been associated with an increase in diversity for many insect species (Mitter et al. 1988; Farrell 1998). Discerning how host-specific phytophagous insects traverse host boundaries to switch and adapt to novel plants is therefore an important component for understanding the origins of biodiversity. Changes in chemosensory perception and interpretation related to host-plant recognition are key behavioral traits associated with host shifts for many phytophagous insects (Becerra 1997; Bernays 2001). This is generally assumed to involve changes in the relative preference of insects among potential host plants. The increased acceptance (higher ranking) of an insect for one plant over others would result, for example, from the insect possessing more preference alleles at host-recognition loci for the favored versus alternative plants. Less well appreciated is that nonhost compounds may also deter insects from many potential plants. As stated by Bernays (2001, p. 712): “As well as being sensitive to and attracted by host-specific chemicals, specialists tend to be deterred more than generalists by nonhost secondary metabolites, and I suggest that specialists benefit from the strong contrasts between positive cues from hosts and negative cues from nonhosts.” However, even in this context, avoidance is usually viewed in the same sense as preference; the relative number of preference and avoidance alleles an insect possess at host-discrimination loci determines a plant’s relative ranking. Little attention has been directed to the possibility that host preference and avoidance may have different physiological/behavioral consequences for insects, such that the same generic evolutionary model does not hold. Here, we examine the topic of host-fruit-odor discrimination in the apple maggot fly, Rhagoletis pomonella, and its role in sympatric speciation via host-plant shifting. We discuss results from recent laboratory and field studies showing that R. pomonella flies both positively orient to the odor of their respective natal host fruits and avoid nonnatal odor. Quite surprisingly, F1 hybrids between apple- and hawthorn-infesting host races of R. pomonella generally fail to orient to the fruit odor of either apples or hawthorns. This suggests that the evolution of new host-discrimination behaviors can generate significant postzygotic as well as premating reproductive isolation when insects must find appropriate host plants in a timely manner to mate and oviposit. The evolutionary consequences of host avoidance for sympatric race formation are not merely the flip side of preference; the two behaviors may have quite different evolutionary dynamics for the fly. A fair proportion of secondgeneration F2 and backcross R. pomonella hybrids displayed normal parental orientation to fruit volatiles, however, implying that differences at only a modest number of loci may underlie fruit-odor discrimination. We present a genetic model involving three genes (a preference locus and two avoidance loci) and cytonuclear gene interactions that can account for fruit-odor discrimination between 101 E I G HT Host Fruit-Odor Discrimination and Sympatric Host-Race Formation JEFFREY L. FEDER AND ANDREW A. FORBES apple and hawthorn flies. We conclude by discussing the generality of the Rhagoletis findings to other phytophagous insects. The Adaptive Zone Hypothesis Simpson (1953) argued that diversification is accelerated by ecological opportunity, such as dispersal into newly opened territory, extinction of natural enemies or competitors, or adoption of a new way of life. A lineage may enter an “adaptive zone” and proliferate either because it is preadapted for niches that become available, or because it evolves key innovations enabling it to use resources from which it has been previously barred (Futuyma 1986, p. 356). More recently, the adaptive zone hypothesis has been cast in terms of “ecological speciation,” which unites speciation modes occurring in allopatry or sympatry when divergent selection in contrasting environments leads to reproductive isolation (Schluter 2001). Tests of the adaptive zone hypothesis can be categorized as comparative or functional...


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