Complex tritrophic interactions in response to crop ...

DOI: 10.1111/eea.12344

1 5 T H I N T E R N AT I O N A L S Y M P O S I U M O N I N S E C T- P L A N T R E L AT I O N S H I P S

Complex tritrophic interactions in response to crop domestication: predictions from the wild Yolanda H. Chen1*, Rieta Gols2, Chase A. Stratton1, Kristian A. Brevik1 & Betty Benrey3 1 Department of Plant and Soil Sciences, University of Vermont, Burlington, Vermont, USA, 2Laboratory of Entomology, Wageningen University, 6708 PB Wageningen, The Netherlands, and 3Institute of Biology, Laboratory of Evolutionary Entomology, Universit
e de Neuch^atel, Neuch^atel, Switzerland

Accepted: 25 March 2015

Key words: Insect–plant, tritrophic, trait variation, evolutionary ecology, agriculture, community ecology, natural ecosystem vs. agroecosystem, artificial selection

Abstract

Crop domestication is the process of artificially selecting plants to increase their suitability to human tastes and cultivated growing conditions. There is increasing evidence that crop domestication can profoundly alter interactions among plants, herbivores, and their natural enemies. However, there are few generalizable predictions on how insect herbivores and natural enemies should respond to artificial selection of specific plant traits. We reviewed the literature to determine how different insect herbivore feeding guilds and natural enemy groups (parasitoids and predators) respond to existing variation in wild and cultivated plant populations for plant traits typically targeted by domestication. Our goal was to look for broad patterns in tritrophic interactions to generate support for a range of potential outcomes from human-mediated selection. Overall, we found that herbivores benefit from directional selection on traits that have been targeted by domestication, but the effects on natural enemies were less studied and less consistent. In general, herbivores appear to mirror human preferences for higher nutritional content and larger plant structures. In contrast, the general effect of lowered plant secondary metabolites did not always influence herbivores consistently. Given that crop domestication appears to be a transformative process that fundamentally alters insect–plant interactions, we believe that a more detailed understanding of the community-wide effects of crop domestication is needed to simultaneously stimulate both biological control and plant breeding efforts to enhance sustainable pest control.

Introduction Human domestication of crop plants has been considered the key innovation that stabilized food availability and enabled the rise of large complex civilizations (Gepts, 2004; Meyer et al., 2012). Crop domestication is defined as deliberate artificial selection on plant traits to suit human tastes and cultivated conditions (Ladizinsky, 1998). Cultivation describes the agronomic activities that promote crop growth, including tillage, manipulation of cropping density, management of plant diversity, and

*Correspondence: Yolanda Chen, Department of Plant and Soil Sciences, University of Vermont, 63 Carrigan Drive, Burlington, VT 05405, USA. E-mail: [email protected]

pest control activities. Crop domestication is far from unidirectional; different human cultures have applied consistent and divergent selection pressures (Brush et al., 1995; Smartt & Simmonds, 1995; Brush & Perales, 2007). As a result, crop varieties can display extraordinary phenotypic differences compared to their wild progenitors in terms of their size, morphology, color, and secondary compounds (Darwin, 1868; Vavilov, 1951; Evans, 1993). However, plant traits that vary in morphology, chemistry, and nutritional content are also known to influence the outcome of interactions among plants, herbivores, and their natural enemies (Price et al., 1980; Turlings & Benrey, 1998; Cortesero et al., 2000; Kennedy, 2003; Ode, 2006). We previously reviewed how selection upon these traits during crop domestication can fundamentally alter interactions among naturally selected species, using only

© 2015 The Netherlands Entomological Society Entomologia Experimentalis et Applicata 1–20, 2015

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systems that comprised domesticated crops and their wild ancestors (Chen et al., 2015). In that study, we wondered how generalizable the effects of selection on specific plant traits are along a domestication gradient on species interactions. Our approach involved examining insect interactions on both wild and cultivated plants to determine whether there were insect patterns associated with a directional change for a particular trait (e.g., larger leaves, lower secondary metabolites, and higher sugar content). Mean values of directly and indirectly selected morphological and chemical traits for a crop species would be considered an extreme or outlier phenotype compared to the mean trait values of the wild ancestor. By reviewing species interactions associated with a wide range of wild and agricultural plants, we expected to observe evidence demonstrating how insects would respond to the extremes of existing variation for plant traits targeted by domestication. Traditionally, crop plants have been considered to be so morphologically distinct from their wild progenitors that they were classified as separate species (Linnaeus, 1753; Spooner et al., 2003). The term ‘domestication syndrome’ has been frequently used to describe crop morphologies that are associated with the domestication of annual crops (Hammer, 1984; Evans, 1993). Some traits may be deliberately targeted by domestication, such as selection for larger plant structures (Schwanitz, 1966; Evans, 1993) or reductions in secondary metabolites (Jones, 1998). However, other plant traits of the ‘domestication syndrome’ may arise because of linkage disequilibrium, in that some traits are genetically linked with targeted traits in the genome (Tang et al., 2006; Blair et al., 2010; Mandel et al., 2013). In this study, we examined how insects respond to a subset of the traits that are often subject to domestication (Meyer et al., 2012) and considered to influence insect performance (Chen et al., 2015): enlargement of organs/ structures (Schwanitz, 1966; Evans, 1993; Smartt & Simmonds, 1995), reduction in branching and tillering (Evans, 1993; Rosenthal & Welter, 1995; Doust, 2007; Chen & Bernal, 2011), synchronization of plant maturation (Chen & Romena, 2006, 2008), decreased tissue toughness (Michaud & Grant, 2009), reduced plant chemical defenses (Lindig-Cisneros et al., 1997; Jones, 1998; Gols & Harvey, 2009; Sujana et al., 2012), and altered nutritional content (Sotelo et al., 1995; Grebenstein et al., 2011). In addition to these plant traits, we also examined two other traits that have been associated with domestication: a reduction in trichome density (Prasifka, 2014) and changes in the expression of induced defenses (RodriguezSaona et al., 2011; Szczepaniec et al., 2013). We searched the literature to determine how insect herbivores and natural enemies responded to existing

variation in wild and cultivated plant populations for the plant traits described above. We focused on the scale of the whole plant and individual plant structure, which is the unit that responds to artificial selection. Given that herbivore feeding guilds can differ in their response to variation in plant traits (Peeters et al., 2001), we constructed an orthogonal grid of plant traits and insect herbivore guilds. We largely avoided the studies that we previously reviewed, i.e., studies that explicitly compared species interactions on the wild ancestor and the crop (Chen et al., 2015). Therefore, this review focused on a wider pool of studies. Although we expected that herbivore and natural enemy responses would vary depending upon life history traits, we aimed to uncover broader patterns that would be characteristic of particular feeding guilds in nature.

How does selection on plant traits targeted by domestication influence insect–plant interactions? To locate host plants or prey, both herbivores and natural enemies must first locate the habitat and plant, recognize and accept the plant or host/prey, and assess plant or host/ prey suitability (Renwick & Chew, 1994; Vinson et al., 1998). Crop domestication could alter the cues used by herbivores or natural enemies for host location during the sequence of these events, which may positively or negatively affect insect host plant location and acceptance. Thus, different plant traits matter at different spatial scales. Insects are guided along these sequential behavioral steps by a number of cues. At long distances, visual cues (Prokopy, 1983), volatiles cues (Bruce et al., 2005), and landscape characteristics such as vegetation heterogeneity (Cronin & Reeve, 2005; Tscharntke et al., 2005) are important for locating potential food or host plants, whereas morphological and food plant quality traits (nutrients and phytochemicals) become more important once the insects are foraging on the plant (Schoonhoven et al., 2005). Given that morphological and plant quality traits become more important for herbivores and natural enemies at the level of host plant acceptance when insects are foraging on the plant, the effects of crop domestication on species interactions would be most apparent at the scale of the whole plant or the plant structure. Figure 1 illustrates the range of hypothetical effects on herbivores and their natural enemies for plant traits considered as part of the domestication syndrome. The effects can be direct or indirect and of varying strength. Crop domestication can dramatically alter morphological, secondary chemistry, and nutritional plant traits, which are, by design, phenotypes that are not found in nature. Although insect herbivores would never encounter such extreme phenotypes in the wild, herbivore responses

Crop domestication: predictions from the wild 3

Figure 1 Diagram that illustrates how crop domestication can affect herbivores and their natural enemies. The plant represents a simplified and hypothetical model of a cultivated plant, maize, and its wild ancestor, teosinte. Traits characteristic of a domesticated maize plant include simpler architecture, larger seeds and reproductive structures, lower concentrations and diversity of secondary compounds (volatile and non-volatile), and higher nutritional quality of plant organs for herbivores and their natural enemies. Traits characteristic of teosinte include complex architecture, smaller reproductive structures and seeds, higher concentrations and diversity of secondary compounds, and lower nutritional quality. Leaf toughness and greater phenological uniformity are not shown. Arrows indicate the direction of the effect from the plant or plant structure to the herbivore and/or natural enemy. Solid arrows indicate direct effects (i.e., herbivore performance, parasitoid host location), dashed arrows indicate indirect effects (i.e., herbivore-mediated parasitoid performance). Dark arrows indicate effects on performance, light arrows indicate effects on behavior. (A) Plant effects on a leaf herbivore and its parasitoid. (B) Plant effects on a seed feeder and its parasitoid.

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to the range of existing plant variation in nature could be predictive of responses to more extreme directional selection. Variation in morphological and chemical plant traits has been widely shown to influence insect herbivore host location success, ovipositional acceptance, and performance (Thompson & Pellmyr, 1991; Vet & Dicke, 1992; Chen & Welter, 2003; Kennedy, 2003). Factors that influence long-distance searching and orientation of insect herbivores are not well documented, although it has been demonstrated that visual cues such as color, shape, and size play an important role (Prokopy, 1983; Renwick & Chew, 1994). At close ranges (Braasch & Kaplan, 2012), volatile cues can be used by both herbivores and their natural enemies for food and host/prey location (Vet & Dicke, 1992; Bruce et al., 2005; Dicke & Baldwin, 2010). Domestication can alter the quantity and quality of volatile organic compound emissions (Gouinguen
e et al., 2001; Gols et al., 2011), and changes in the composition of herbivore-induced plant volatile (HIPV) emissions among plant varieties could affect parasitism rates (Degen et al., 2012). Crop domestication also frequently selects for the enlargement of economically important structures (Meyer et al., 2012), which may lead to higher herbivore attack rates because insect herbivores tend to lay more eggs on larger plants or on more rapidly growing structures (Craig et al., 1989; Awmack & Leather, 2002; Ishino et al., 2011). Therefore, artificial selection on plant morphology and chemistry can alter the abundance and within-plant distribution of insect herbivores (Chen & Welter, 2005; Michaud & Grant, 2009; Hoffman & Rao, 2011). Once nymphs or larvae are feeding on a plant, variation in the chemical resistance and nutritional quality may strongly affect the likelihood of insect herbivore survival and developmental rate (Chen & Welter, 2005; Harvey & Gols, 2011; Zaugg et al., 2013). Finally, changes in the quality or amount of plant resources can mediate competition among herbivores (Denno et al., 1995). Crop domestication may also have indirect (via the host herbivore) and direct effects on the performance and behavior of natural enemies (Figure 1). The degree to which a particular natural enemy’s foraging behavior is plastic may be important in influencing their ability to tolerate plant variation and still be able to capture prey effectively. The importance of HIPVs in herbivore and natural enemy foraging behavior is well documented (Turlings & Benrey, 1998; Dicke & Baldwin, 2010; Mumm & Dicke, 2010). However, both herbivores and their natural enemies are able to learn from previous experience with food plants or plant-host complexes (Papaj & Prokopy, 1989; Turlings et al., 1993; Tam o et al., 2006; Hoedjes et al., 2011), and may therefore rapidly adapt to changes in volatile cues if they are modified by domestication. Artificial

selection on morphological, chemical, or semiochemical plant traits may directly influence the ability of natural enemies to find host plants where prey may be located (Hoballah et al., 2002; Ode et al., 2004; Ode, 2006; K€ ollner et al., 2008; Chen & Bernal, 2011; Harvey et al., 2011; Reynolds & Cuddington, 2012). Therefore, selection on plant morphology and architectural complexity could disrupt natural biological control, especially if insect herbivores differ from their natural enemies in terms of their response to architectural complexity (Chen & Welter, 2003; Heisswolf et al., 2005; Obermaier et al., 2008). Natural enemies vary considerably in their patch foraging behavior and, consequently, their response to herbivore density. Once natural enemies locate the appropriate host plant where prey are present, shifts in the abundance and distribution of herbivores due to changes in plant architecture can influence natural enemy success in locating and capturing prey (Gingras et al., 2002; Chen & Welter, 2003; Reynolds & Cuddington, 2012). Some parasitoids respond in a positive density-dependent manner to increased local herbivore density (Costamagna et al., 2004; Pareja et al., 2008), whereas others are not sensitive to herbivore density (Anton et al., 2007). For instance, the ichneumonid parasitoid wasp Neotypus melanocephalus (Gmelid) disperses immediately after attacking a single caterpillar host (Strand & Vinson, 1982). If crop domestication selects for architecturally simpler plants that spatially aggregate herbivore species, parasitoids that attack a single herbivore at a time could be less effective in controlling herbivore populations. Therefore, due to the variability in life history characteristics, natural enemy species may vary in their response to bottom-up changes in herbivore densities that result from crop domestication.

Data collection We performed a systematic qualitative review to examine the relationship between plant traits targeted by plant domestication and plant-associated insect feeding guilds. We targeted the following categories: plant structure enlargement (leaves, fruit/flowers/seed heads, seed size, stem diameter), increased phenological uniformity, reduced architectural complexity, reduced trichome density, decreased tissue toughness, decrease in secondary metabolites, increased protein content (nitrogen, protein, or amino acids), and increased sugar content. We searched for insect responses in the following eight categories: chewing, boring, leaf mining, piercing/sucking, galling, seed predators (non-seed) natural enemy predators, and parasitoids. We attempted to identify as many studies as possible within each subcategory (plant trait*herbivore guild) in order to identify specific examples of how each insect

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to the range of existing plant variation in nature could be predictive of responses to more extreme directional selection. Variation in morphological and chemical plant traits has been widely shown to influence insect herbivore host location success, ovipositional acceptance, and performance (Thompson & Pellmyr, 1991; Vet & Dicke, 1992; Chen & Welter, 2003; Kennedy, 2003). Factors that influence long-distance searching and orientation of insect herbivores are not well documented, although it has been demonstrated that visual cues such as color, shape, and size play an important role (Prokopy, 1983; Renwick & Chew, 1994). At close ranges (Braasch & Kaplan, 2012), volatile cues can be used by both herbivores and their natural enemies for food and host/prey location (Vet & Dicke, 1992; Bruce et al., 2005; Dicke & Baldwin, 2010). Domestication can alter the quantity and quality of volatile organic compound emissions (Gouinguen
e et al., 2001; Gols et al., 2011), and changes in the composition of herbivore-induced plant volatile (HIPV) emissions among plant varieties could affect parasitism rates (Degen et al., 2012). Crop domestication also frequently selects for the enlargement of economically important structures (Meyer et al., 2012), which may lead to higher herbivore attack rates because insect herbivores tend to lay more eggs on larger plants or on more rapidly growing structures (Craig et al., 1989; Awmack & Leather, 2002; Ishino et al., 2011). Therefore, artificial selection on plant morphology and chemistry can alter the abundance and within-plant distribution of insect herbivores (Chen & Welter, 2005; Michaud & Grant, 2009; Hoffman & Rao, 2011). Once nymphs or larvae are feeding on a plant, variation in the chemical resistance and nutritional quality may strongly affect the likelihood of insect herbivore survival and developmental rate (Chen & Welter, 2005; Harvey & Gols, 2011; Zaugg et al., 2013). Finally, changes in the quality or amount of plant resources can mediate competition among herbivores (Denno et al., 1995). Crop domestication may also have indirect (via the host herbivore) and direct effects on the performance and behavior of natural enemies (Figure 1). The degree to which a particular natural enemy’s foraging behavior is plastic may be important in influencing their ability to tolerate plant variation and still be able to capture prey effectively. The importance of HIPVs in herbivore and natural enemy foraging behavior is well documented (Turlings & Benrey, 1998; Dicke & Baldwin, 2010; Mumm & Dicke, 2010). However, both herbivores and their natural enemies are able to learn from previous experience with food plants or plant-host complexes (Papaj & Prokopy, 1989; Turlings et al., 1993; Tam o et al., 2006; Hoedjes et al., 2011), and may therefore rapidly adapt to changes in volatile cues if they are modified by domestication. Artificial

selection on morphological, chemical, or semiochemical plant traits may directly influence the ability of natural enemies to find host plants where prey may be located (Hoballah et al., 2002; Ode et al., 2004; Ode, 2006; K€ ollner et al., 2008; Chen & Bernal, 2011; Harvey et al., 2011; Reynolds & Cuddington, 2012). Therefore, selection on plant morphology and architectural complexity could disrupt natural biological control, especially if insect herbivores differ from their natural enemies in terms of their response to architectural complexity (Chen & Welter, 2003; Heisswolf et al., 2005; Obermaier et al., 2008). Natural enemies vary considerably in their patch foraging behavior and, consequently, their response to herbivore density. Once natural enemies locate the appropriate host plant where prey are present, shifts in the abundance and distribution of herbivores due to changes in plant architecture can influence natural enemy success in locating and capturing prey (Gingras et al., 2002; Chen & Welter, 2003; Reynolds & Cuddington, 2012). Some parasitoids respond in a positive density-dependent manner to increased local herbivore density (Costamagna et al., 2004; Pareja et al., 2008), whereas others are not sensitive to herbivore density (Anton et al., 2007). For instance, the ichneumonid parasitoid wasp Neotypus melanocephalus (Gmelid) disperses immediately after attacking a single caterpillar host (Strand & Vinson, 1982). If crop domestication selects for architecturally simpler plants that spatially aggregate herbivore species, parasitoids that attack a single herbivore at a time could be less effective in controlling herbivore populations. Therefore, due to the variability in life history characteristics, natural enemy species may vary in their response to bottom-up changes in herbivore densities that result from crop domestication.

Data collection We performed a systematic qualitative review to examine the relationship between plant traits targeted by plant domestication and plant-associated insect feeding guilds. We targeted the following categories: plant structure enlargement (leaves, fruit/flowers/seed heads, seed size, stem diameter), increased phenological uniformity, reduced architectural complexity, reduced trichome density, decreased tissue toughness, decrease in secondary metabolites, increased protein content (nitrogen, protein, or amino acids), and increased sugar content. We searched for insect responses in the following eight categories: chewing, boring, leaf mining, piercing/sucking, galling, seed predators (non-seed) natural enemy predators, and parasitoids. We attempted to identify as many studies as possible within each subcategory (plant trait*herbivore guild) in order to identify specific examples of how each insect

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density was not consistent (Table S1). The majority of the studies that focused on fruit/seed size examined whether the relationship between fruit/seed size variation influenced the incidence of herbivory (Table S1). An increase in fruit size clearly increased the likelihood of attack by seed predators/frugivores. Hare (1980) found that smaller fruits of cockleburr, Xanthium strumarium L. were more likely to be attacked by Euaresta aequalis (Loew) and Phaneta imbridana Fernald than larger fruits. We found only nine studies that examined parasitoid and predator responses to fruit enlargement, and they gave contrasting results. Although Gomez & Zamora (1994) found that larger fruit of Hormathophylla spinosa (L.) P. K€ upfer were more likely to be attacked by weevils, Ceutorhynchus spec., they did not find that parasitism rates responded to the number of weevils or fruit size. On the other hand, herbivores feeding on larger fruit can be more likely to escape parasitism, such as the apple maggot fly, Rhagoletis pomonella (Walsh), which are parasitized less on the larger apple fruit than on fruit of their native hawthorn trees (Feder, 1995). Grain and legume plants have been repeatedly selected for larger seeds (Evans, 1993; Fuller, 2007; Schmutz et al., 2014). It has been proposed that seed size evolved as a trade-off between the probability of survival after germination and the number of seeds. Larger seeds have a higher germination rate, whereas a larger number of smaller seeds increases the probability of dispersal and escape from predators (Crawley, 1983). Increases in seed size appear to be strongly associated with an increase in the likelihood of herbivore attack (Table S1A). For many seed crops, some of the most important traits altered during the domestication process are: dormancy, seed set and size, color, toughness, time to maturity, and dispersal (Evans, 1993). Plant stem diameter typically increases during domestication due to a reduction in overall branching and reallocation of plant photosynthates to the main stem or through a correlated increase in plant size (Evans, 1993). We did not find enough evidence to detect a pattern. For stemboring species, thicker stems are associated with an increase in pupal weight (Teder & Tammaru, 2002), higher growth rate (Ball & Dahlsten, 1973), and higher survival (Freese, 1995). Increased stem thickness is also associated with an increase in the size of galls (Stiling & Rossi, 1996). Enlargement of plant structures due to domestication can favor an increase in local abundance and spatial aggregation of the herbivores that attack those structures. Both the density and accessibility of hosts can influence the foraging behavior and efficacy of natural enemies. The enlargement of plant structures can impact natural enemies by being more directly attractive to natural enemies

or by influencing natural enemy foraging success. For instance, a generalist larval parasitoid of fruit flies, Diachasmimorpha longicaudata (Ashmead), responded to visual images by clearly preferring to search for hosts on larger artificial models (Segura et al., 2007). Enlargement of fruits may enable the fruit fly Bactrocera oleae (Rossi) to burrow deeper into the fruit and thereby making them less accessible to parasitoid wasps (Wang et al., 2009). Likewise, increased size of the sunflower head is associated with a decrease in the amount of time a parasitoid, Dolichogenidea homoeosomae (Muesebeck), spent foraging for its lepidopteran host, where many were protected within a refuge (Chen & Welter, 2003). Moreover, D. homoeosomae females left patches sooner if they were not rewarded by successful parasitism events, allowing herbivores that were not protected by a structural refuge to also escape parasitism (Chen & Welter, 2003, 2007). Simpler plant architecture

Domestication has strongly reduced the complexity of plant architecture within annual crops, by reducing plant branching (Doust, 2007). Plants that are more architecturally complex support a more diverse herbivore assemblages (Askew, 1980). For example, Araujo et al. (2006) found that an increase in plant architectural structure positively increased the species richness and survival of galling herbivores. Conversely, decreases in plant architectural complexity can influence the patterns of herbivory by altering the abundance and distribution of insect herbivores. The few studies that have studied this relationship have found that architectural simplification tends to increase oviposition and abundance of chewing herbivores and foraging activity of natural enemies (Tables S1B and C). Changes in the abundance and distribution of insect herbivores can influence the ability of natural enemies to successfully locate and attack their herbivorous hosts. Decreasing structural complexity tends to have a positive effect on the foraging of predators and parasitoids, resulting in higher predation and parasitism rates (Table S1). We did not find a clear pattern on how reduced branching affects the foraging of natural enemies. In some cases, there appeared to be no effects of plant architecture and the number of attacked prey (Grevstad & Klepetka, 1992; Obermaier et al., 2008). However, some natural enemies could be more successful in attacking herbivores when branching was reduced (Table S1). Change in trichome density

Trichomes, hairs or glandular outgrowths on the surfaces of plants, can be strongly reduced during the domestication process (Bellota et al., 2013), but the trend of reduced

Crop domestication: predictions from the wild 7

trichome density is not consistent across crops (Turcotte et al., 2014). Similarly, changes in trichome length and density are inconsistent during domestication and selective breeding, with some cultivars showing a decrease in trichomes (Kanno, 1996), and others an increase, especially when trichomes are selected for as a resistance trait (Talekar & Lin, 1994). With few exceptions, reduced trichomes are positively correlated with an increase in herbivore damage, growth, and higher oviposition for most herbivore guilds (Table S1C). However, smaller insect species, such as thrips, can utilize trichomes as protection from predation (Table S1C). Whereas piercing and sucking insects generally benefit from reduced trichomes (Obrycki et al., 1983; De Santana Souza et al., 2013), there can also be mixed effects, such as increased aphid populations simultaneous with lower plant injury (Kaplan et al., 2009) or different herbivory levels on plants which differ in trichome morphology (Hare & Elle, 2002). The reduction in trichome density appears to benefit generalists more than specialists (Smith & Grodowitz, 1983). Herbivores tend to select structures or plants with fewer trichomes when presented with plants or plant structures that vary in trichome density (Sato et al., 2013). In some plant genera (e.g., Solanum) trichomes also produce chemicals (glandular trichomes) that entrap or are toxic to insect herbivores and their natural enemies. In those cases, the effect of trichomes cannot always be clearly separated from the effects caused by chemical resistance (Kennedy, 2003). Many parasitoids oviposit and successfully parasitize more prey on plants with fewer trichomes (Table S1C), though the opposite can also be true (Demayo & Gould, 1994). In some cases, plant surfaces with high densities of trichomes can provide ‘enemy-free space’ by compromising the behavior of parasitoids and predators (Lovinger et al., 2000; Kaplan et al., 2009). Reductions in trichomes tend to have a negative effect on predatory mites, but a mixed effect on predation levels by coccinellid beetles and other larger predators (Table S2). Overall, the effects of trichomes on herbivore and natural enemies are quite similar, and governed by size and the degree of species specialization (Table S2). Decreased tissue toughness

Although changes in tissue toughness have not been directly described as a common trait of the domestication syndrome, several authors have observed that a decline in tissue toughness has been associated with crop domestication (Seiler et al., 1984; Michaud & Grant, 2009; Bellota et al., 2013). With a few exceptions, the effect of reduced tissue toughness facilitates insect access to plant tissue, promotes oviposition, and enhances feeding across

herbivore guilds (Table S1D). In the case of seed legumes for example, domestication has been associated with a decrease in the toughness of the seed coat (Lush & Evans, 1980). For predator and parasitoid species that oviposit on their prey by piercing through plant tissue, a decrease in toughness can make ‘encased’ prey more accessible to the ovipositors of parasitoids (Constant, 1996; Cattell & Stiling, 2004). Although it may not only change the outcome of species interactions, the available evidence suggests that decreased tissue toughness results in a decline in plant resistance against insect pests, but may also simultaneously benefit natural enemies (Table S1D). Plant-insect synchronization and greater phenological uniformity

To increase the efficiency of harvests and reduce multiple harvesting trips, humans have selected for greater synchronization of flowering and maturation within the plant and within the population (Evans, 1993). Greater phenological uniformity appears to have a variable effect within and among herbivore guilds. With greater phenological uniformity and the maturation of targeted structures synchronized with herbivore activity, the herbivore impact on plant fitness will likely increase (Table S1). For instance, English-Loeb & Karban (1992) found that a higher proportion of flowers was attacked on plant clones that were more highly synchronized in flowering compared to plant clones that flowered over a broader temporal period. On the other hand, increasing phenological uniformity did not affect seed predation for multiple Asteraceae plants (Fenner et al., 2002). If plant populations are synchronized to avoid peak herbivore activity, there can be an overall negative effect on chewing insects, no effect on oviposition by boring insects, and a variable effect on gall insects (Table S1E). We did not find any studies that explicitly observed the effects of increasing phenological uniformity of plant life stages on natural enemies.

Secondary metabolites and plant resistance Decreased secondary metabolites

Domestication has frequently reduced the concentrations of plant secondary metabolites (Meyer et al., 2012), but this pattern is not consistent across all crops (Turcotte et al., 2014). In examining the insect–plant interactions literature, we found that most of the studies on the effects of secondary metabolites on ovipositional preference and growth involved chewing lepidopteran species (but see Shlichta et al., 2014). We therefore summarize the general patterns for these herbivores. Decreases in secondary metabolites tended to negatively influence or have neutral effects on ovipositional preferences of specialist

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density was not consistent (Table S1). The majority of the studies that focused on fruit/seed size examined whether the relationship between fruit/seed size variation influenced the incidence of herbivory (Table S1). An increase in fruit size clearly increased the likelihood of attack by seed predators/frugivores. Hare (1980) found that smaller fruits of cockleburr, Xanthium strumarium L. were more likely to be attacked by Euaresta aequalis (Loew) and Phaneta imbridana Fernald than larger fruits. We found only nine studies that examined parasitoid and predator responses to fruit enlargement, and they gave contrasting results. Although Gomez & Zamora (1994) found that larger fruit of Hormathophylla spinosa (L.) P. K€ upfer were more likely to be attacked by weevils, Ceutorhynchus spec., they did not find that parasitism rates responded to the number of weevils or fruit size. On the other hand, herbivores feeding on larger fruit can be more likely to escape parasitism, such as the apple maggot fly, Rhagoletis pomonella (Walsh), which are parasitized less on the larger apple fruit than on fruit of their native hawthorn trees (Feder, 1995). Grain and legume plants have been repeatedly selected for larger seeds (Evans, 1993; Fuller, 2007; Schmutz et al., 2014). It has been proposed that seed size evolved as a trade-off between the probability of survival after germination and the number of seeds. Larger seeds have a higher germination rate, whereas a larger number of smaller seeds increases the probability of dispersal and escape from predators (Crawley, 1983). Increases in seed size appear to be strongly associated with an increase in the likelihood of herbivore attack (Table S1A). For many seed crops, some of the most important traits altered during the domestication process are: dormancy, seed set and size, color, toughness, time to maturity, and dispersal (Evans, 1993). Plant stem diameter typically increases during domestication due to a reduction in overall branching and reallocation of plant photosynthates to the main stem or through a correlated increase in plant size (Evans, 1993). We did not find enough evidence to detect a pattern. For stemboring species, thicker stems are associated with an increase in pupal weight (Teder & Tammaru, 2002), higher growth rate (Ball & Dahlsten, 1973), and higher survival (Freese, 1995). Increased stem thickness is also associated with an increase in the size of galls (Stiling & Rossi, 1996). Enlargement of plant structures due to domestication can favor an increase in local abundance and spatial aggregation of the herbivores that attack those structures. Both the density and accessibility of hosts can influence the foraging behavior and efficacy of natural enemies. The enlargement of plant structures can impact natural enemies by being more directly attractive to natural enemies

or by influencing natural enemy foraging success. For instance, a generalist larval parasitoid of fruit flies, Diachasmimorpha longicaudata (Ashmead), responded to visual images by clearly preferring to search for hosts on larger artificial models (Segura et al., 2007). Enlargement of fruits may enable the fruit fly Bactrocera oleae (Rossi) to burrow deeper into the fruit and thereby making them less accessible to parasitoid wasps (Wang et al., 2009). Likewise, increased size of the sunflower head is associated with a decrease in the amount of time a parasitoid, Dolichogenidea homoeosomae (Muesebeck), spent foraging for its lepidopteran host, where many were protected within a refuge (Chen & Welter, 2003). Moreover, D. homoeosomae females left patches sooner if they were not rewarded by successful parasitism events, allowing herbivores that were not protected by a structural refuge to also escape parasitism (Chen & Welter, 2003, 2007). Simpler plant architecture

Domestication has strongly reduced the complexity of plant architecture within annual crops, by reducing plant branching (Doust, 2007). Plants that are more architecturally complex support a more diverse herbivore assemblages (Askew, 1980). For example, Araujo et al. (2006) found that an increase in plant architectural structure positively increased the species richness and survival of galling herbivores. Conversely, decreases in plant architectural complexity can influence the patterns of herbivory by altering the abundance and distribution of insect herbivores. The few studies that have studied this relationship have found that architectural simplification tends to increase oviposition and abundance of chewing herbivores and foraging activity of natural enemies (Tables S1B and C). Changes in the abundance and distribution of insect herbivores can influence the ability of natural enemies to successfully locate and attack their herbivorous hosts. Decreasing structural complexity tends to have a positive effect on the foraging of predators and parasitoids, resulting in higher predation and parasitism rates (Table S1). We did not find a clear pattern on how reduced branching affects the foraging of natural enemies. In some cases, there appeared to be no effects of plant architecture and the number of attacked prey (Grevstad & Klepetka, 1992; Obermaier et al., 2008). However, some natural enemies could be more successful in attacking herbivores when branching was reduced (Table S1). Change in trichome density

Trichomes, hairs or glandular outgrowths on the surfaces of plants, can be strongly reduced during the domestication process (Bellota et al., 2013), but the trend of reduced

Crop domestication: predictions from the wild 9

A reduction in concentrations of secondary metabolites had an overall positive effect on the performance of parasitoids (Table S2A). Secondary metabolites show corresponding effects on different trophic levels: they tend to affect natural enemies and herbivores in the same direction (Table S2A). Few studies have reported effects of reduced phytochemical concentrations on predator performance. Herbivores that are well adapted to their host plant and sequester phytochemicals from them can experience increased predation if a reduction in secondary metabolites causes them to become less deterrent to generalist predators (Francis et al., 2001; Karban & Agrawal, 2002; M€ uller et al., 2002). Concentrations of secondary metabolites are not evenly distributed among or within plant organs and tissues (Schoonhoven et al., 2005). Toxins are often stored in special organs (glandular trichomes) or cells to prevent phytotoxicity. Most insect herbivores feed on specific plant tissues, and they can be quite selective, even when feeding on a specific organ. Herbivores such as aphids, gallers, and trenching caterpillars are also known to manipulate or circumvent plant resistance traits (Dussourd et al., 1993; Inbar et al., 1995; Walling, 2008). Food plant specialization in general and specialization at the tissue level tends to correlate positively with the size of the insect herbivore (Schoonhoven et al., 2005). Moreover, small insect herbivores perceive and respond to heterogeneity in plant quality at a finer spatial scale than larger herbivores (Schoonhoven et al., 2005). Also, small insect herbivores are known to avoid feeding on tissues that contain high levels of secondary metabolites, whereas larger insects may be less discriminatory (Schoonhoven et al., 2005). Thus, as with other plant traits, the effect of artificial selection on secondary metabolite concentrations within a particular tissue and its influences on herbivore behavior and performance are strongly determined by insect life history traits, of which body size and feeding site/mode are likely to be highly important. Decreased inducibility

Crop domestication has been shown to either reduce the inducibility of plant defense (Szczepaniec et al., 2013), or leave inducibility unchanged (Ballhorn et al., 2008; Rodriguez-Saona et al., 2011). Induction of plant resistance against insect herbivores is generally activated by two major signaling pathways (Kunkel & Brooks, 2002): the salicylic acid pathway, known to be mostly activated by piercing-sucking insects, and the jasmonic acid/ethylene pathway, generally activated by chewing insect herbivores (Erb et al., 2012; Mithofer & Boland, 2012). Because domestication has frequently reduced plant secondary

compounds (Meyer & Purugganan, 2013; Turcotte et al., 2014), it is highly probable that decreased inducibility has occurred more often than the existing literature may suggest. Plants exhibit, in varying degrees, some baseline resistance or constitutive resistance that protects them against attack by most insect herbivore species (Schoonhoven et al., 2005). In response to herbivory, these resistance traits, both chemical and morphological, often change, usually not only locally at the site where the damage occurred but also systemically in younger tissues (Karban & Baldwin, 1997; Agrawal, 1999). Few studies have directly studied how crop domestication affects inducible plant resistance by comparing the wild progenitor with a domesticated species. It is hypothesized that, if production costs are high, plants should rely on constitutive resistance when herbivore attack is frequent and predictable, whereas plants should rely on inducible resistance when herbivore attack is more unpredictable (Karban & Baldwin, 1997; Kessler & Halitschke, 2009). Indeed, the extent to which plant resistance traits are expressed constitutively or are inducible is plant- and herbivore-species specific, and varies even within plant species (Coleman & Jones, 1991; Ballhorn et al., 2008; Harvey et al., 2011). In rapidly growing crop plants, the allocation of nutrients to both constitutive and inducible resistance traits may be reduced, a pattern that has been found in cabbage, Brassica oleracea L. (Harvey et al., 2011) and in cranberries, Vaccinium macrocarpon Aiton (Rodriguez-Saona et al., 2011). In contrast, Lima bean plants (Phaseolus lunatus L.) exhibiting high inducibility were characterized by low constitutive resistance levels, suggesting a trade-off between constitutive and inducible resistance traits within both wild and domesticated Lima bean plants (Ballhorn et al., 2008). The induction of volatile plant secondary metabolites is often studied in relation to natural enemy attraction (Turlings et al., 1995; Dicke & Baldwin, 2010), primarily in crop plant species (Turlings & Benrey, 1998; Mumm & Dicke, 2010). The production of these HIPVs is plant- and herbivore-species specific, as herbivores of different feeding guilds induce qualitatively and quantitatively different HIPV blends (Arimura et al., 2009; McCormick et al., 2012). Relatively little is known about how plant domestication has altered the quality and quantity of HIPV blends and if these changes influence foraging behavior of insect herbivores and their natural enemies (Gouinguen
e et al., 2001). Natural enemies of insect herbivores can discriminate between plant genotypes that may differ qualitatively and quantitatively in their HIPV blends (McCormick et al., 2012; de Rijk et al., 2013; De Lange et al., 2014). Therefore, it is highly possible that crop domestication can

10 Chen et al.

inadvertently affect the HIPV blends and the ability of crop plants to recruit natural enemies. There is some evidence that natural enemies can discriminate between wild and domesticated plant genotypes. For example, Cotesia rubecula (Marshall), a specialist braconid parasitoid of Pieris rapae (L.) caterpillars, was more attracted to wild than to cultivated cabbage (B. oleracea), despite their long rearing history on cultivated cabbage (Gols et al., 2011). In contrast, the braconid D. homoeosomae clearly preferred to orient to the domesticated instead of the wild sunflower, although flowers were controlled for size (Chen & Welter, 2003). Similar patterns were found for Stenocorse bruchivora (Crawford), a parasitoid of bruchid beetles: females were more attracted to domesticated than to wild bean seeds (Benrey et al., 1998). Currently it is difficult to detect any directionality of selection in terms of volatile quantity or quality. Even among cabbage cultivars, there is a large amount of variation in HIPV blends, and parasitoids have been shown to be differentially attracted to these plants in the laboratory and the field (Benrey & Denno, 1997; Poelman et al., 2009).

Nutrition Humans have deliberately selected for changes in nutritional content within crops, such as sugar (sugar beet or sugarcane), oil (sunflower, canola), protein (maize, various crops), or mineral content (Evans, 1993). It has also been demonstrated that artificial selection can dramatically alter plant nutritional composition. One of the bestknown cases of artificial selection was conducted to select for protein and oil content in maize, starting in 1896 (Dudley et al., 1974). After 70 generations, protein content reached 215% of the original level, whereas high oil content reached 341% of the original level. Domestication can also alter plant mineral nutrition, even if it is not explicitly targeted by artificial selection (Sotelo et al., 1995; Blair & Izquierdo, 2012). For example, phosphorous levels are higher in bean landraces than in wild genotypes (Beebe et al., 1997), whereas iron and zinc levels are lower in domesticated than in wild beans (Blair & Izquierdo, 2012). Then again, directional selection for the accumulation of some nutrients during domestication may select against the accumulation of other nutrients. Plant quality is a strong determinant of insect herbivore performance, fecundity, and ultimately population growth (Scriber & Slansky, 1981; Awmack & Leather, 2002). Although we focused on traits where artificial selection has been well-documented (e.g., protein, sugar, and oil) (Evans, 1993), it is important to consider that even the shifts in the relative ratios of nutrients and minerals can

influence herbivore performance and fecundity (Awmack & Leather, 2002). Overall, there have not been enough studies to determine the broader patterns of domestication on plant nutrition. There are even fewer studies that have examined the effects of altered plant nutritional content on natural enemies. Increased protein content

Protein is a primary nutrient required for insect growth, but it is generally present in plants at much lower levels than in animals (Price et al., 2011). As the correlation between elemental nitrogen levels and plant protein is quite consistent (Schoonhoven et al., 2005), measuring nitrogen levels in plants is a reasonable proxy for determining plant protein content (Joern et al., 2012). Nitrogen availability is centrally important for herbivores, as increases in nitrogen can significantly improve herbivore performance (Price et al., 2011). In general, crop domestication has increased nitrogen leading to lowered the C:N ratios (Garc
ıa-Palacios et al., 2013). Higher levels of nitrogen tend to improve food quality across all feeding guilds, except for seed predators (Table S2). However, herbivore feeding guilds vary in how consistently they respond positively to increases in nitrogen content (Table S1F). For instance, phloem and sap feeders are particularly dependent on nitrogen availability, as their reproduction and growth are tied to fluctuations in nitrogen levels within a host plant (Weibull, 1987; Awmack & Leather, 2002). Higher levels in plant nitrogen increase performance, fecundity, and ovipositional preference of insect herbivores, especially piercing-sucking, leaf mining, and chewing herbivores (Table S2B). Although chewing herbivores showed a trend of increased performance on plants with higher nitrogen levels, the effect was more variable (Table S1F). The effects of increased nitrogen may differ between sedentary and mobile feeders, as more mobile species are able to move from plant to plant in order to maintain a satisfactory nitrogen intake (Behmer, 2009). The effects of increased nitrogen on parasitoids and predators are most likely to be indirect and tied to the performance of their prey or host (Slansky, 1986). Higher nitrogen levels in plants have been found to translate into increased predator and parasitoid performance (Table S1F). However, when plant nitrogen is increased, natural enemy populations may not be able to increase at the same rate as herbivore populations, thereby limiting their effectiveness in regulating herbivore populations (de Sassi et al., 2012). Overall, we would expect that increased nitrogen levels in plants would result in higher rates of herbivory and better herbivore and natural enemy performance.

8 Chen et al.

lepidopteran herbivores, whereas it had more variable effects on fitness correlates, such as herbivore survival, body mass, or development time (Table S2A). Plant secondary metabolites tended to have a negative effect on the performance of generalist herbivores but not on specialists (Table S2A), probably because (many) specialized herbivores that are well-adapted to the host are able to sequester phytochemicals from their host plant. Within groups of phytochemicals (e.g., glucosinolates, alkaloids, iridoid glycosides), the effects of secondary compounds on herbivores tend to be compound specific (Barbosa et al., 1991; Bodnaryk, 1997; Cheng et al., 2013). Moreover, the compounds that confer resistance against specialist herbivores are different from those that confer resistance against generalist herbivores (Gols et al., 2008). Although secondary metabolite concentrations have been inversely correlated with herbivore performance in

laboratory experiments, this relationship is not always observed under field conditions. For instance, a laboratory study on preference and performance of a specialist herbivore (Tyria jacobaeae L.) of ragwort (Jacobaea vulgaris Gaertn. = Senecio jacobaea L.) found no correlation with pyrrolizidine alkaloid (PA) concentration, but herbivore damage levels in the field were correlated with specific PA concentrations (Macel et al., 2002; Macel & Klinkhamer, 2010). Similarly, results from a meta-analysis that examined the relative importance of different plant traits as predictors for herbivore resistance (Carmona et al., 2011), did not find a strong association between concentrations of plant secondary metabolites and herbivore susceptibility. Overall, we found that the impact of phytochemicals on insect performance tends to be more pronounced for generalist than for specialist herbivores (Table S2A) and this may explain the overall neutral effect in Table 1.

Table 1 Summary of herbivore guild responses to traits commonly selected upon during domestication based on Tables S1 and S2. The physical plant traits describe a directionality of selection. The directional effect is denoted positive or negative, when there was a significant effect in the same direction for at least one of the measured response variables. Each number represents the number of studies that found this particular trend: ↑, an increase; ↓, decrease; Ø, no change; ↕, variable response in insect activity. The columns ‘↑ Response proportion’ denote the proportion of the total studies that responded positively to the variation associated with domestication. If more than 2/3 of the studies for a guild showed a positive response, the cells are shaded and the value for the overall response is given in bold font

He rbi vore s Traits

Physical

Chemical

Enlargement Leaves, shoots, plant organs height, stem /structures thickness Flowers, fruits, seeds, seed heads Simplification of architecture Reduced trichome densities Reduced tissue toughness Increased phenological uniformity Reduced levels of secondary metabolites Nitrogen, Increased protein, nutrition amino acids Sugars

Chewing

Borers

Leafminers

↑1, Ø 1

↑2, ↕ 1 ↑3

Piercing / Galling sucking ↑1, Ø 1

Natural e ne mi e s Seed ↑Response Parasitoid Predator ↑Response predator/ proportion proportion frugivore

↑6 , Ø 1, ↓1

↑10, ↕ 2, ↓1, Ø 1 ↑1,↓2

↑1

↑1

0.72

↑2, Ø 1, ↓3

0.33

0.71

↑1, Ø 1, ↓3

0.20

0.60

↑3, Ø 2

↑3

0.86

↑12, ↕1, ↑2, ↓1 ↑2, ↓1 ↑7, ↓2, ↓1 , Ø 3 Ø1

↑3, Ø 1

0.70

↑7, Ø 1

↑3, ↓4, Ø1

0.63

↑3, Ø 1

↑1, ↕ 1, ↑1 Ø1

↑1, ↓1

0.71

↑3

↑1

1.00

↑1, ↓1

↑2,↓1, Ø2

0.60

↓1

↑1, Ø 2

0.50

↑13, ↕1, ↑1 ↓1 , Ø 2

0.78

↓1

↑3, ↓1

↑1

↑1,Ø 1

↑15, ↕2, ↓7 , Ø 3

↑2

↑1, Ø 1 ↑5, ↓4 , Ø3

↑9, ↕1, Ø1

↑4, ↕1, ↑3, ↕1, ↑9, Ø2 Ø1 Ø3

↑5, ↓1

↓1

0.70

↑2

↑1

Ø1

↓1, Ø1

0.40

Ø1

↑1, Ø2

12 Chen et al.

studies are needed to resolve the strength of this relationship. Given that domestication can alter the density and physical distribution of herbivores, how are natural enemies predicted to respond? Parasitoid foraging success varies depending upon life history characteristics, age, feeding status, and responses to variation in herbivore densities within a patch (Godfray, 1994). Also, patch-leaving decisions tend to be species and guild specific (Godfray, 1994; Papaj et al., 1994). Parasitoids that attack concealed hosts tend to leave a patch after foraging for a fixed time, independent of local host density (Weis et al., 1989; Romstock-Volkl, 1990). However, other parasitoids initially disperse after attacking one host, but will then show an affinity to a particular patch by returning to it (Nealis, 1986). Therefore, herbivore and natural enemy responses to crop domestication may be highly dependent upon individual life history.

6

7

8

Potential outcomes On the basis of the evidence reviewed in this study, we outline potential outcomes on herbivore and natural enemy responses to single plant traits targeted by plant domestication. Our goal is to make generalizations on the potential consequences of crop domestication on the associated insects and to highlight those areas for which more research is needed. For each of these outcomes, we indicate whether there is available supporting evidence (SE), contrasting evidence (CE), or insufficient evidence (IE) to draw conclusions. We only present a representative subset of these potential outcomes for the various plant traits presented in previous sections. 1 An increase in the size of the plant structure or organ used by herbivores will result in increased abundance and performance of herbivores, and herbivores may benefit from an adverse effect on natural enemy accessibility (SE). 2 Seed predators, fruit burrowers, gall feeders, and in general herbivores that feed on internal and protected plant structures will be mostly affected by the size and accessibility (e.g., stem toughness, seed coat thickness) of this structure (IE). 3 A reduction in physical defenses (e.g., trichomes and latex) in crop plants will positively affect both herbivores and natural enemies (SE). 4 An increase in the nutrient content of crop plants or plant structures will result in increased herbivore and natural enemy performance (SE). 5 Plant traits will indirectly affect natural enemies via the changes in the density and quality of the herbivorous host or prey. Increased densities of herbivores due to

9

10

enlargement of organs/structure and their performance due to decreased toxicity will increase the availability of hosts/prey quality to support parasitoid development (CE). On the other hand, increased herbivore performance on crop plants due to higher nutrient content may negatively affect natural enemies due to faster herbivore development and increased ability to encapsulate parasitoid eggs (‘slow growth-high mortality’ hypothesis) (CE). For all of the above outcomes, we would expect that: the performance of herbivores and natural enemies that are associated with the tissues targeted by domestication will be altered more than the performance of herbivores and natural enemies associated with tissues that are not targeted by domestication (IE). Altered plant traits in crop plants will differentially affect generalist and specialist herbivores. For example, generalist herbivores will benefit from a reduction in plant secondary metabolites than specialists, which are adapted to the plant’s chemical defenses (CE). Selection on plant traits will differentially affect generalists and specialist parasitoids. For example, plant volatiles may have been reduced in crop plants rendering them less attractive or harder to find for generalists than for specialist parasitoids (CE). The previous potential outcomes mostly refer to single plant traits. Correlated plant traits will most likely have non-additive but interactive effects on herbivores and natural enemies (IE). For example, an increase in seed size may be accompanied by a decrease in the thickness of the seed coat. Seed predators and their parasitoids may improve their performance on these seeds because of the greater ease in chewing through or ovipositing through a thinner seed coat. Therefore, increased herbivore and natural enemy performance may result from greater access to seed resources due to the thinner seed coat rather than greater overall resources from an increased seed size.

Discussion The form and function of plant traits are commonly considered to have evolved under natural selection and, in turn, plant traits can ultimately shape an entire community of interacting species (Thompson, 2002, 2005; Whitham et al., 2003). Wild progenitors of crop plants host a whole array of insect herbivores and natural enemies (Charlet, 1999; Michaud, 2011; Chen et al., 2013), which have adapted to the plant morphological and chemical traits of wild ancestors prior to domestication. During artificial selection of crop plants, traits such as fruit,

Crop domestication: predictions from the wild 13

flowers, seed heads, and stems have been selected to be larger because they directly contribute to increases in yield. However, under artificial selection for taste and yield, traits that contribute to plant morphology and defense against herbivores may have also been altered. Studies that have quantified rates of herbivory within a community context have found that there are three major groups of traits that most strongly affect herbivory: physiological (Johnson et al., 2009; Kurokawa et al., 2010), morphological (Loranger et al., 2012; Robinson et al., 2012), and phenological (Johnson & Agrawal, 2005; Loranger et al., 2012). Using a meta-analysis correlating plant traits with insect herbivory across species, Carmona et al. (2011) found that gross morphological traits, such as the extent of branching and plant size, are correlated with herbivory, as well as physical traits associated with resistance, such as trichomes or latex. However, the meta-analysis by Carmona et al. (2011) found that the extent to which these traits influence herbivores is dependent upon herbivore life history. In contrast to the Carmona et al. (2011) study, Loranger et al. (2012) found that leaf nitrogen levels and lignin concentration most strongly predicted herbivory levels. Increasingly, plant chemistry does not appear to be the major determinant of herbivory documented in natural communities (Carmona et al., 2011; Loranger et al., 2012). Our findings here also partially support this idea. Nevertheless, there is still ample evidence that changes in plant chemistry associated with domestication can alter herbivore abundance and performance (Harvey & Gols, 2011; Chen et al., 2015). One possibility for this apparent discrepancy is that studies such as Carmona et al. (2011) examined plant susceptibility to herbivores as the key dependent value using a correlational approach, rather than directly examining herbivore performance, as in the studies reviewed by Chen et al. (2015). Generalist and specialist herbivores vary in their response to plant secondary compounds, as plant chemicals may either stimulate or inhibit herbivores (Schoonhoven et al., 2005; Ali & Agrawal, 2012). Turcotte et al. (2012) found that domestication (in a study using 29 independent domestication events) can increase the survival or performance of generalist herbivores. Although we did not explicitly account for whether insects were considered specialists or generalists within our review, we predict that declines in secondary metabolites would benefit generalists more than specialists, because specialists have specific enzymatic machinery to detoxify specific plant defenses (Ratzka et al., 2002). Given that many plant traits selected by crop domestication also happen to favor insect herbivore activity, is it then unavoidable that all insect herbivores associated with the wild ancestor would become insect pests? Although the

findings of this review may suggest that all herbivores have the potential to become pests, we recognize that variation in environmental factors and life histories may complicate this relationship in the field (Chen et al., 2015). The best available evidence on the incidence of insect pests comes from crops grown within their region of origin, near their wild relatives. Within crop fields that are sympatric with their wild progenitors, relatively few herbivores actually reach outbreak levels, suggesting that most herbivores tend to be well controlled by their natural enemies (Chen et al., 2015). There are many factors that suggest that the effect of domestication on insect–plant interactions may be more complicated than the direct relationships described in Tables 1, S1, and S2. First, most of the studies included in this review examined only the responses of a single feeding guild rather than an entire assemblage. Interactions between herbivores within an assemblage can range from closely interacting to casually interacting, so domestication may affect herbivores directly and indirectly via interactive effects on the herbivore assemblage. Second, some selected traits are more tightly correlated with other plant traits, such as the relationship between overall size and the size of individual structures (Carmona et al., 2011). For plant traits that are strongly correlated with other plant traits, there may be more widespread effects across an entire plant or herbivore assemblage (Wise & Rausher, 2013). On the other hand, plant traits that are not well correlated with each other may result in more specific effects on only a subset of herbivores. Finally, although we know that natural enemy responses can be highly variable based upon life history variation, we do not have a strong sense as to how strongly plastic parasitoid foraging behavior can be. Our findings raise an important question for sustainable agriculture: How can we maximize food production and at the same time select for resistance to insect pests? Crop domestication activities are still ongoing around the world (Casas et al., 2007; Blanckaert et al., 2011; Bost, 2013), and there are many breeding efforts to counter the losses in natural resistance traits or traits incurred during domestication (Degenhardt et al., 2009; Tamiru et al., 2011; Blair & Izquierdo, 2012; Bleeker et al., 2012). We believe that crop domestication is a transformative process that fundamentally alters interactions between plants, herbivores, and their natural enemies. Given that selection for the growth forms favored by humans appear to enhance herbivory, how do we simultaneously select for resistance and traits valued by humans? Although we believe that reviews such as this are an appropriate place to start, evidence for some of these potential outcomes is still limited and several remain highly speculative. In order to determine the extent to

14 Chen et al.

which these outcomes can be generalized, we need more experimental studies focusing on different domestication events, which will likely generate useful knowledge that can be utilized in biological control and plant breeding programs. Unlocking these patterns and matching them with insects that are adapted to particular niches on wild progenitors will provide insight as to how domestication affects pest control. Ultimately, crop domestication has been the process responsible for producing the food crops that feed the world. A more careful analysis of the community-wide effects of domestication is needed to determine to what extent artificial selection has compromised our ability to achieve natural pest control on different crops and develop truly sustainable agroecosystems.

Acknowledgements We thank Thomas Degen for assisting with the design of the figure. This study was supported by funds from the Vermont Agricultural Experiment Station and a grant no. 31003A-127364 from the Swiss National Science Fund.

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Supporting Information Additional Supporting Information may be found in the online version of this article: Table S1. Effects of changes in plant physical traits on the behavior and/or performance of insect herbivores and their natural enemies. Studies are included that measure the effects of these traits in wild or cultivated systems denoted by wild or cult (when known) in the first column. Insect herbivores are classified according to feeding guilds. Natural enemies are classified as predators or parasitoids; the latter group is further categorized according to life history traits such as host stage attacked (when given) and endo- or ectoparasitism. We further indicated (when known) whether the insects were generalists (G) (polyphagous for herbivores, attacking species in more than one genus for natural enemies) or specialists (S) (mono- or oligophagous for herbivores, attacking species in one genus for natural enemies) and whether studies were conducted in the field studying natural colonization or whether they were conducted in the laboratory or greenhouse (= lab).

The studied traits are (A) enlargement of plant organs/ structures, (B) simplified architecture, (C) reduced trichome densities, (D) reduced tissue toughness, and (E) increased phenological uniformity. Results are presented with arrows when statistically significant. Symbol clarification: ↑, increased; ↓, decreased; ↕, variable response; Ø, no effect, DT, development time; NE, natural enemy. Attack can refer to likelihood or rate of attack. Table S2. Effects of changes in plant chemical traits on the behavior and/or performance of insect herbivores and their natural enemies. Studies are included that measure the effects of these traits in wild or cultivated systems denoted by wild or cult (when known) in the first column. Insect herbivores are classified according to feeding guilds. Natural enemies are classified as predators or parasitoids; the latter group is further categorized according to life history traits such as host stage attacked (when given) and endo- or ectoparasitism. We further indicated (when known) whether the insects were generalists (G) (polyphagous for herbivores, attacking species in more than one genus for natural enemies) or specialists (S) (mono- or oligophagous for herbivores, attacking species in one genus for natural enemies) and whether studies were conducted in the field studying natural colonization or whether they were conducted in the laboratory or greenhouse (= lab). The studied traits are (A) reduced levels of secondary chemistry and (B) increased nutrition. Results are presented with arrows when statistically significant. Symbol clarification: ↑, increased; ↓, decreased; ↕, variable response; Ø, no effect; DT, development time; NE, natural enemy. Attack can refer to likelihood or rate of attack.