Introduction

Plants, and the organisms that eat them, constitute the majority of terrestrial multicellular diversity (Speight et al., 2008). Indeed, co-evolutionary interactions between herbivores and plants are thought by some to be ‘the major zone of interaction responsible for generating terrestrial organic diversity’ with plant secondary metabolites (PSMs) playing a central role in co-evolutionary processes (Ehrlich & Raven, 1964). As typically described, plants gain fitness advantages and the potential for evolutionary radiation from mutation or recombination events that generate novel PSMs that deter herbivores (or other attackers and competitors, e.g. pathogens). In turn, counter-adaptations, or offences (Karban & Agrawal, 2002; Sorensen & Dearing, 2006), by herbivore populations favour cladogenesis in the consumers and exert further selection pressure for novel PSMs (Janzen, 1980). Antagonistic interactions between plants and herbivores are, therefore, seen as a driving force behind the great diversity of PSMs that occur in plant populations (Rosenthal & Berenbaum, 1992; Gershenzon et al., Chapter 4).

The broad acceptance of a co-evolutionary arms race between plants and herbivores, with antagonism as the pivotal interaction, has led to the general view that PSMs are toxins that must be avoided, tolerated or overcome by consumers (Speight et al., 2008). Perhaps not surprisingly, many ecologists and evolutionary biologists have simply come to regard PSMs as barriers to consumption, with those barriers overcome to varying degrees by the generalist and specialist herbivore populations that consume plants (Shipley et al., 2009). However, the development of a tri-trophic perspective of plant–herbivore–enemy interactions (Price et al., 1980) paved the way for a deeper understanding of the role of PSMs in the ecology and evolutionary biology of herbivores. Variation within and among plant populations is now seen to provide the potential for ‘enemy free space’ for herbivores (Jeffries & Lawton, 1984; Bernays & Graham, 1988) and a template upon which interactions between herbivores, higher trophic levels and the abiotic environment can occur (Hunter & Price, 1992). Moreover, we recognise a variety of external stressors, including predation, disease and abiotic conditions, that may be ameliorated by some level of PSM consumption (Calvert et al., 1979; Hunter & Schultz, 1993; De Roode et al., 2008; Forbey et al., 2009), whereas the same PSMs can impose fitness costs if consumption rates are too high (Rossiter et al., 1988; van Zandt & Agrawal, 2004). These examples demonstrate that PSMs are neither inherently good nor inherently bad for herbivores.