A Coevolutionary Arms Race: Understanding Plant-Herbivore Interactions

Abstract

Plants and insects share a long evolutionary history characterized by relationships that affect individual, population, and community dynamics (Gatehouse, 2002). Plant-herbivore interactions are a prominent feature of this evolutionary history; it is by plant-herbivore interactions that energy is transferred from primary producers to the rest of the food web (Agrawal, 2004). On average, more than 10% of plant production is consumed by herbivores annually (Coley et al., 1985). This initial interaction between plants and their herbivores establishes the amount of energy available to the rest of the community. Consequently, the nature and extent of plant- herbivore interactions can significantly impact community structure, diversity, and function (see Silliman et al., 2005). Not only are plant-herbivore food webs important to community dynamics, but these webs also constitute a significant portion of the world's biodiversity. A recent study estimated that plant-herbivore food webs represent more than 40% of the global terrestrial biodiversity (Novotny & Basset, 2005). Consequently, it is important to understand the concepts central to these interactions as well as the processes that might influence the evolution of plant and herbivore species. Back Off Bugs! Plant Defenses Plant-herbivore relationships pit the insect against the plant in a race to maximize fitness. Maximizing fitness is the general goal for both plants and insects; however, in the case of plant-herbivore interactions, the insect maximizes its fitness by consuming plant tissues. Reduced biomass and tissue damage can negatively impact plant growth and fecundity, which ultimately decrease plant population growth rate. Individual plants that can somehow prevent or tolerate herbivory have a higher fitness than their more vulnerable neighbors; thus, these individuals contribute more genes to future generations. Not all plant-herbivore interactions are equal; rather, the type and amount of herbivore damage varies greatly among plant species and populations (Coley et al., 1985). This variation in consumption is likely a reflection of variation in plant palatability. Plants employ a variety of mechanical and chemical defenses that affect palatability and deter herbivores (Lerdau et al., 1994; Mauricio, 1998; Gatehouse, 2002; Siemens et al., 2002; Kliebenstein, 2004). Leaf toughness and trichome production are two ways in which plants mechanically protect themselves from herbivores (Feeny, 1970; Mauricio, 1998). These defenses act as physical barriers, preventing or slowing herbivores from accessing and handling plant tissue. In contrast, chemical defenses make it difficult for herbivores to process plant material once it is ingested. Chemicals, including glucosinolates, monoterpenes, and tannins, are generally produced through secondary metabolism (Lerdau, 1994; Mauricio, 1998; Gatehouse, 2002; Siemens et al., 2002; Kliebenstein, 2004). These compounds may have several functions that make them important to the plant's survival. In terms of defense, these compounds are often toxic or lethal to herbivores, causing a suite of problems that deter herbivores from foraging on the defended plant (Gatehouse, 2002). Operation Adaptation: Herbivore Offenses Plant defenses are important to insect herbivore populations because of their effect on insect growth and reproduction (Agrawal, 2004). The direction and magnitude of these effects depend on the evolutionary relationship of the insect herbivore to the plant; in particular, the effects of plant defenses on herbivore populations depend on whether the insect is a specialist or generalist herbivore on a specific host plant (Traw & Dawson, 2002a,b). In general, specialist herbivores tend to be unaffected by chemical defenses, many of which are lethal to generalist herbivores (Agrawal et al., 1999; Agrawal, 2000; Traw & Dawson, 2002). In some cases, chemical defenses are actually positively correlated with feeding by specialist herbivores, indicating that specialist herbivores use the chemical defenses as a cue to locate their preferred prey or exploit the defense in their own interactions with predator species (Ehrlich & Raven, 1964; Agrawal et al. …