restricted access 2. Evolution of Preference and Performance Relationships
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20 Natural selection should favor female phytophagous insects that have a preference for ovipositing on resources where their offspring will have the highest fitness (Dethier 1959a, 1959b; Singer 1972; Jaenike 1978). This assertion has been termed the naïve adaptationist hypothesis (Courtney and Kibota 1990). This hypothesis has been tested by measuring oviposition preference and offspring performance in a wide range of interactions, and contrary to initial expectations a wide range of preference-performance relationships have been found (Thompson 1988; Courtney and Kibota 1990; Mayhew 1998, 2001). General hypotheses explaining broad patterns in preference-performance relationships have been largely lacking, with the exception of the phylogenetic constraints hypothesis described below. We propose the “feeding niche constraints” hypothesis that adaptations to the characteristics of an herbivore’s feeding niche will determine the evolution of the relationship between preference and performance. In this chapter, to determine whether eggs are oviposited where offspring fitness is highest we looked at the correlation between preference and performance. Preference is nonrandom oviposition on resources offered simultaneously or sequentially (Singer 1986). Performance is any measure of offspring survival, growth, or reproduction that is presumed to be correlated with fitness (Thompson 1988). These indirect measures do not always correlate with ultimate fitness (Thompson 1988), but they are frequently used because of the difficulty of directly measuring fitness. Preference-performance relationships have important implications for ecological and evolutionary interactions. Insect population dynamics are strongly influenced by the nature of these relationships. Price (2003) showed that species that have highly selective oviposition behavior with a strong preference-performance correlation have stable or latent population dynamics, while species with low correlations between preference and performance have eruptive population dynamics. Preference-performance relationships also have evolutionary implications: species with strong relationships tend to be specialists, and those with weak relationships tend to be generalists. As a result an understanding of the forces responsible for the evolution of preference -performance relationships will allow us to understand the evolution of host range. To explain patterns in preference and performance, the feeding niche constraints hypothesis posits that the feeding niche of a species influences the evolution of the preference -performance relationship. The feeding niche of an herbivore determines the kinds of plant resource variation it will encounter. We hypothesize that insects share certain fundamental constraints that limit their ability to respond to this variation and that therefore impact the evolution of a positive preference-performance relationship. If all insects share these constraints, then the evolution of the preference -performance relationships depends on the resources insects encounter and not on their particular phylogenetic background. A testable prediction of this hypothesis is that insects with similar feeding niches will evolve similar preferenceperformance relationships. For example, stem-gallers on woody plants will have similar types of relationships, and free-feeding leaf-feeders on herbaceous plants will have relationships that differ from those of the stem-gallers. An alternative is the phylogenetic constraints hypothesis (Price 2003), which proposes that taxonomic groups differ from each other in preference-performance relationships because they have specific characters that constrain the evolution of these relationships. This hypothesis predicts that closely related species will evolve similar preference-performance relationships. The null hypothesis for both hypotheses is that there will be no relationship between either the taxonomic group or the feeding niche and the strength of the preference-performance relationship. TWO Evolution of Preference and Performance Relationships TIMOTHY P. CRAIG AND JOANNE K. ITAMI To develop predictions from the feeding niche hypothesis , we proceed through three steps. First, we identify the insect constraint: for example, an insect’s limited neural capacity to integrate information. Second, we identify resource variation that will cause this constraint to limit the evolution of the preference-performance relationship: for example, variation in a plant’s resource quality that differs in complexity. Third, we compare the preference-performance relationships in insects with different types of feeding niches: for example, monophagous species with less resource complexity versus polyphagous species. We argue that all insect herbivores are subject to at least three types of constraints that limit the kind of resources where strong preference-performance relationships can evolve. Limiting Constraints Complexity Constraints Bernays (1998, 2001) has advanced the neural limitation hypothesis, that there are inherent limitations of the insect nervous system such that specialists processing a limited set of information make more efficient and accurate choices than generalist insects faced with complex choices. This hypothesis also implies that as the complexity of resource variation in the feeding niche increases...


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