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136 Host-specific herbivorous insects have inspired speculation about sympatric speciation at least since the 1860s, when Walsh (1864) described the now famous host races of the apple maggot (Berlocher and Feder 2002). Even Ernst Mayr, who lamented that “sympatric speciation is like the Lernaean Hydra which grew two new heads whenever one of its old heads was cut off,” admitted that “host races [of phytophagous insects] are a challenging biological phenomenon , and constitute the only known case indicating the possible occurrence of incipient sympatric speciation” (Mayr 1963, p. 460). He immediately added, though, that “even in this case a process of sympatric speciation is neither established nor even probable.” Mayr’s (1963) thorough analysis of the theoretical and empirical weaknesses of sympatric speciation in animals did not slay the Hydra. Review articles and books (e.g., Schilthuizen 2001; Via 2001; Dieckmann et al. 2004) continue to provide enthusiastic affirmation, and one could easily form an impression from reading the contemporary literature that it is as reasonable to assume a sympatric as an allopatric or parapatric origin of sister species. My aim in this chapter is to suggest that at least as it applies to herbivorous insects, the current enthusiasm for sympatric speciation exceeds both theoretical and empirical justification. My attention to this topic stems from an interest in speciation that predates even my formal education in biology, and from having adopted host-specific insects as research material in the 1970s. The problem of the evolution of host specificity leads quickly to the issue of speciation. In reviewing the still sparse literature on this subject, Gregory Mayer and I concluded (Futuyma and Mayer 1980) that the evidence did not support the growing acceptance of sympatric speciation. In particular, we argued that the evidence from the best and most widely cited case—Guy Bush’s study of the apple maggot Rhagoletis pomonella (Bush 1969)—was unconvincing, in part because there was no conclusive evidence of a genetic basis for the morphological and phenological differences that the supposed host races display. Soon afterward, Felsenstein (1981) provided a typically incisive theoretical analysis of a common verbal model, in which assortative mating evolves between two subpopulations adapted to different resources because it prevents production of poorly adapted hybrid offspring. The key issue, Felsenstein noted, is that recombination breaks down the association among loci that govern ecological adaptation and mate preference. The plausibility of sympatric speciation then depends on the recombination rate, the number of loci, and the strength of divergent selection. Felsenstein concluded that sympatric speciation “would be nearly impossible” if mating were based on a “two-allele” model of mate preference, and thus explained why sympatric speciation does not produce “a different species on every bush” (p. 124). Bush and his student Scott Diehl quite appropriately responded that Felsenstein’s objection did not apply to insects that mate only on their host plant, and in which reproductive isolation is a by-product of divergent host preference (Diehl and Bush 1989). Natural selection in this case favors linkage disequilibrium between loci that affect “performance ” on and “preference” for two different host species. In Diehl and Bush’s simulations, distinct host-specific species quickly formed, exhibiting complete linkage disequilibrium and complete genetic divergence. At about the same time, Bush’s student Jeffrey Feder, together with other colleagues, confirmed genetic differences between the host races of R. pomonella (Feder et al. 1988; Feder and Bush 1989), initiating a long-term program of study that has made this the most convincing instance of incipient sympatric speciation. Since then, host races have been claimed for several insects (reviewed by Drès and Mallet 2002). These cases, as well as pairs or groups of host-divergent sister species, are often interpreted as the result of sympatric TE N Sympatric Speciation: Norm or Exception? DOUGLAS J. FUTUYMA divergence and incipient speciation. Among these, of course, are the Enchenopa treehoppers to which Tom Wood dedicated his extraordinary energy and inspiring quest for understanding. I think Tom may have viewed my skepticism as a measure of the empirical difficulties that any attempt to demonstrate sympatric speciation must face. I immensely enjoyed our interactions, and I like to think he felt the same way. Theory Gavrilets (2004) has provided a detailed, clear exposition of the many mathematical and simulation models of speciation , and Coyne and Orr (2004) summarize and analyze empirical studies within a theoretical framework. Several of their general points bear repeating. First, any...

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