Evolution and biological control

Opinions about the value of biological control are often extreme. Colloquially, biological control most often refers to classical biological control, in which one species is introduced from another region to control pests such as arthropod herbivores in agricultural systems, or weeds in managed and natural systems. As such, biological control has the potential to be a low-cost, chemical free, means to control pests. Numerous biological control programs have been unqualified successes (Bellows 2001), such as the control of cacti in Australia with the moth Cactoblastis cactorum (Raghu and Walton 2007), of cottony-cushion scale (Icerya purchasi) in California with the vedalia lady beetle, Rodolia cardinalis (Caltagirone and Doutt 1989), and of glassy-winged sharpshooters in French Polynesia with the egg parasitoid Gonatocerus ashmeadi (Grandgirard et al. 2009). Yet, classical biological control, as with any introduction of a species into a new area, necessarily involves the unknown and therefore carries some inherent risk (Simberloff and Stiling 1996) – what will these organisms actually do in a novel ecosystem? The most unpredictable element in biological control is the extent to which the realized niche is modified in the new environment. This effect has been responsible for some disastrous outcomes of classical biological control, many of which occurred during an era when vertebrates were being introduced around the world by Europeans for a variety of reasons (e.g., introducing the birds of Shakespeare to America, Mirsky 2008), including for biological control (Howarth 1991). The introductions as biological control agents of cane toad to Australia (Crossland et al. 2008) and mongoose to Hawaii (Hays and Conant 2007) are notorious. Introductions of generalist invertebrate agents also have had dire consequences, such as the introduction of predatory snails to French Polynesia (Murray et al. 1988; Coote 2007). In retrospect, some of the unintended consequences of biological control could have been avoided with more ecological knowledge (McEvoy and Coombs 2000) or more societal appreciation for native species (which has developed with time, Henneman and Memmott 2001), but with other introductions, it would have been impossible to know ahead of time what the risks would be (e.g., gall fly agents of knapweeds providing supplementary food to mice that harbor hantavirus, Pearson and Callaway 2006). Many of the unknown outcomes of biological control are purely ecological – what is the risk that a wasp, introduced to parasitize an agricultural pest, will also be able to feed on a native insect? Other unknowns involve evolution – will a herbivore adapt over time to be able to feed on a new nontarget host or hybridize with a closely related species? This volume explores the evolutionary aspects of biological control. Although often overlooked, evolutionary considerations are critical to all stages of classical biological control, from agent selection, to quarantine, release, establishment, and ultimately success in pest control (Ehler et al. 2004). Many questions are unresolved. For example, should agents be chosen that have a long history with the host or are ‘new associations’ more likely to succeed (Hokkanen and Pimentel 1989)? Can one improve effectiveness through artificial selection (Hopper et al. 1993)? Will postcolonization adaptation of the agent increase the likelihood of success, and/or are hosts equally likely to evolve resistance over time (Roderick 1992; Holt and Hochberg 1997; Hufbauer 2001)? Are generalist consumers more likely to survive in novel environments or are specialists more effective (Murdoch et al. 1985; Waage 1990; Brodeur 2012)? More recently, concern for the environment, as well as theory examining the reasons for success of generalist predators, prompted a shift to the release of specialized consumers typically preceded by extensive testing aimed at delimiting the host range of candidate biological control agents. While this approach has clearly made biological control more predictive ecologically, research focused on host range currently lacks measures of genetic variation in host use and responses of those hosts, and thus evolutionary uncertainties remain.