Natural Enemy-Induced Plasticity in Plants and Animals
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7 Natural Enemy-induced Plasticity in Plants and Animals Douglas W. Whitman1 and Leon Blaustein2 1Department of Biological Sciences, Illinois State University, Normal, IL, USA 61790-4120, E-mail: [email protected] 2Community Ecology Laboratory, Institute of Evolution, Faculty of Sciences, University of Haifa, Haifa 31905, Israel, E-mail: [email protected] Abstract Natural enemy-induced plasticity in prey defense phenotype appears to be a generalized adaptation syndrome of considerable importance to ecology and evolution. Defense plasticity is evident across a wide range of animal, plant, and microbe taxa, and threatened prey can alter a wide range of mor- phological, physiological, behavioral, and life-history traits. By switching phenotypes in response to threats, prey can adaptively modify their relation- ships with natural enemies. Natural enemies can subsequently respond with phenotypic plasticity to prey plasticity. New prey phenotypes can alter biotic habitats, with sometimes profound consequences for communities. By changing phenotypes, prey come under new selective regimes, altering their evolutionary trajectories. The evolution and expression of defense plasticity are potentially influenced by nearly all aspects of the prey’s physiology and ecology. Defense plasticity is expected to evolve when benefits outweigh costs; but, taxonomic, physiological, and ecological constraints may hinder evolution of plastic response. Natural enemy-induced phenotypic plasticity has a genetic basis and can evolve. Researchers are beginning to understand the mechanisms underlying natural enemy-induced plasticity in prey. This includes identification of the specific chemical, visual, and mechanical elicitors from natural enemies that cue prey, and the elicitor receptors, signal trans- duction pathways, and effector systems in prey that ultimately produce the altered phenotype. Signal transduction and effector systems vary from simple to complex, and can involve translational, transcriptional, enzymatic, hormonal, and neural regulation. Natural enemy induction of prey is impor- tant for agriculture and medicine. New technologies offer possibilities to manipulate prey induction systems for economic gain. This is a rapidly evolving field of science and many questions and hypotheses need to be addressed. 234 Phenotypic Plasticity of Insects Introduction We now know that prey can respond adaptively to predators via phenotypic plasticity1. When confronted with actual or potential predation, individual prey can alter their morphology, physiology, behavior and life history characteristics (Karban and Baldwin 1997, Agrawal et al. 1999, Tollrian and Harvell 1999, Werner and Peacor 2003, Benard 2004, Kusch et al. 2005, Mondor et al. 2008). Predator-induced plasticity is expressed across a wide array of taxonomic groups, including bacteria, fungi, protozoa, algae, plants, and numerous invertebrate, and vertebrate taxa, and is found in diverse habitats, including marine, aquatic, and terrestrial ecosystems (Kush 1999, Tollrian and Harvell 1999, Pavia and Toth 2000, Radman et al. 2003, Benard 2004, Duquette et al. 2005, Thoms et al. 2006, Vaughn 2007, Rohde and Wahl 2008). Many induced defenses are beneficial for prey in that they result in reduced attack by predators or increased prey survival (Traw et al. 2007, McCoy and Bolker 2008), and many appear to have been shaped by natural selection. Given its wide taxonomic and ecological expression, predator-induced plasticity appears to be a generalized adaptation syndrome of considerable importance in ecology and evolution. Understanding predator-induced plasticity in prey is important for understanding the biology of individuals, populations, and species, and ecological relationships, such as predator-prey population dynamics, indirect effects, trophic webs, and community structure. Plasticity studies are also critical for understanding the production and maintenance of phenotypic, genetic, and interaction diversity, speciation, evolution, and co- evolution at the predator-prey interface (Agrawal 2001, Price 2002, Schlichting 2004, Strauss and Irwin 2004, Van Zandt and Agrawal 2004). Predator-induced changes in prey can have large ecosystem consequences (Agrawal 2005, Miner et al. 2005, Ohgushi 2005, Ohgushi et al. 2007). By inducing new prey phenotypes, predators alter biotic habitats, increasing habitat diversity, and alter interaction linkages, initiating new interactive cascades (Werner and Peacor 2003, Ohgushi 2005) that may favor instability (Abrams and Matsuda 1997) or stability (Vos et al. 2004, Miner et al. 2005). Predators induce changes in prey that can alter the availability of resources for, or otherwise influence, other species, and in this way, can function as indirect keystone species via trait-mediated indirect effects (Schmitz 2003, 1 For the purpose of this chapter, we define “prey” as an organism whose live tissues are consumed by another organism, and “predator” as an organism that consumes prey. Hence, a prey may be a microbe, a plant, or an animal, and a predator may be an herbivore, parasite, parasitoid, pathogen, or a traditional predator. Natural Enemy-induced Plasticity in Plants and Animals 235 Agrawal 2005, Ohgushi et al. 2007). For example, Melanoplus femurrubrum grasshoppers switch from feeding primarily on grasses to feeding primarily on forbs in the presence of predatory spiders (Schmitz 1998), a trait- mediated indirect effect. Such predator-induced defense could presumably impact both prey physiology (ingested nutrients and allelochemicals), and grasshopper, spider, and grass vs. forb species abundance, diversity, and ecosystem properties such as N-cycling (Schmitz 2006, 2008). If spiders switch from feeding on grasshoppers to other prey, this could initiate altered trophic cascades. Hence, a predator-induced response in a prey may alter community structure (Strauss and Irwin 2004, Ohgushi 2005). Predator-induced phenotypic plasticity is currently an active area for physiology and biochemistry (Vasconsuelo and Boland 2007, Wittkopp 2007), development and morphology (Kishida and Nishimura 2006, Ishikawa et al. 2008), behavior (Bruce and Herberstein 2006, Korb and Fuchs 2006, Chapman et al. 2008), ecology (Agawala et al. 2006, Heil 2008), chemical ecology (Heil et al. 2008, Opitz et al. 2008), signal transduction (Maffei et al. 2007a, b, Pieterse and Dicke 2007), life history (Relyea 2007, Benard and McCauley 2008, Mikolajewski et al. 2008), genetic (Bakker et al. 2008, Gomez-Mestre et al. 2008), evolution (Hammill et al. 2008, Urban 2008), and modeling and theoretical research (Morris et al. 2006, Rinke et al. 2008). Because predator-induced phenotypic plasticity influences the relationships among agricultural plants, plant pests, and their natural enemies, and also between pathogens, disease vectors, and animal hosts, understanding phenotypic plasticity has high practical significance for agriculture and medicine (see Dicke and Grostal 2001, Dean and De Moraes 2006). Finally, the broad taxonomic, ecological, and mechanistic expression of predator-induced plasticity allows unlimited and flexible approaches and experimental designs to test numerous evolutionary and mechanistic hypotheses and evolutionary models. Many inducible traits are easily studied in the lab or field. As such, predator-induction serves as an ideal focus area for understanding phenotypic plasticity and predator-prey and multi-trophic interactions. Evolution of Predator-induced Plasticity What are the species characteristics and ecological parameters that select for plastic vs. canalized anti-predator defenses, and what form will plasticity take? Overall, plasticity should evolve when plasticity has higher fitness than canalization. But what factors might favor such an outcome? 236 Phenotypic Plasticity of Insects (1) Strong selective pressure from predators (Riessen 1992). Without selective pressure from predators, no defense (one type of canalization) should evolve. (2) Fluctuating predatory pressure in either degree or type, over time or space (Riessen 1992, Blaustein 1999, Van Buskirk 2002, Berrigan and Scheiner 2004, Karban and Nagasaka 2004). When predator level and type are uniform over time and space, there would be no selection or advantage for plastic defense. (3) Induced defense is costly (Riessen 1992, Zangerl 2003). If the induced defense has little cost, then it should evolve to be constituently expressed. (4) Induced defense is effective. If there is no benefit for the induced defense (but it has a cost), then it should be selected against. Hence, there should be overall fitness benefits for expression of the plastic defense when the predator is present, and costs when the predator is absent, and vice versa (Harvell 1990, Järemo et al. 1999, Zangerl 2003). (5) Genetic variation for degree of plasticity. Without genetic variation, selection cannot occur (Agrawal et al. 2002, Berrigan and Scheiner 2004, Van Kleunen and Fischer 2005). (6) Predators provide detectible and reliable cues (Riessen 1992, Blaustein 1999, Gabriel et al. 2005). If prey cannot detect the predator or detect cues that predict increased risk of predation, then they cannot respond (Karban et al. 1999, Van de Meutter et al. 2005), which would favor constitutive defenses (Berrigan and Scheiner 2004). How often are these criteria met by species that have evolved predator- induced plasticity? Criteria 1 and 2 are nearly always met, because virtually all prey have multiple natural enemies, and because predatory