15TH INTERNAT IONAL SYMPOS IUM ON INSECT-PLANTRELAT IONSH IPS

Complex tritrophic interactions in response to cropdomestication: predictions from the wildYolanda H. Chen1*, Rieta Gols2, Chase A. Stratton1, Kristian A. Brevik1 & Betty Benrey31Department of Plant and Soil Sciences, University of Vermont, Burlington, Vermont, USA, 2Laboratory of Entomology,

Wageningen University, 6708 PBWageningen, The Netherlands, and 3Institute of Biology, Laboratory of Evolutionary

Entomology, Universit�e de Neuchatel, Neuchatel, Switzerland

Accepted: 25March 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 prefer-

ences for higher nutritional content and larger plant structures. In contrast, the general effect of low-

ered plant secondary metabolites did not always influence herbivores consistently. Given that crop

domestication appears to be a transformative process that fundamentally alters insect–plant interac-tions, we believe that a more detailed understanding of the community-wide effects of crop domesti-

cation 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

pest control activities. Crop domestication is far from

unidirectional; different human cultures have applied con-

sistent and divergent selection pressures (Brush et al.,

1995; Smartt & Simmonds, 1995; Brush & Perales, 2007).

As a result, crop varieties can display extraordinary pheno-

typic 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 & Ben-

rey, 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

*Correspondence: Yolanda Chen, Department of Plant and Soil

Sciences, University of Vermont, 63 Carrigan Drive, Burlington,

VT 05405, USA. E-mail: yolanda.chen@uvm.edu

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

DOI: 10.1111/eea.12344

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 inter-

actions. Our approach involved examining insect interac-

tions on both wild and cultivated plants to determine

whether there were insect patterns associated with a direc-

tional 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 deliber-

ately targeted by domestication, such as selection for larger

plant structures (Schwanitz, 1966; Evans, 1993) or reduc-

tions 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 & Sim-

monds, 1995), reduction in branching and tillering (Evans,

1993; Rosenthal &Welter, 1995; Doust, 2007; Chen & Ber-

nal, 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 (Rodriguez-

Saona 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 herbi-

vore 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 thewild 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 bydomestication 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 nega-

tively 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 (nu-

trients 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 ene-

mies 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 indi-

rect and of varying strength.

Crop domestication can dramatically alter morphologi-

cal, secondary chemistry, and nutritional plant traits,

which are, by design, phenotypes that are not found in nat-

ure. Although insect herbivores would never encounter

such extreme phenotypes in the wild, herbivore responses

2 Chen et al.

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 domesticatedmaize

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.

Crop domestication: predictions from the wild 3

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 per-

formance (Thompson& Pellmyr, 1991; Vet &Dicke, 1992;

Chen & Welter, 2003; Kennedy, 2003). Factors that influ-

ence long-distance searching and orientation of insect her-

bivores 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 nat-

ural enemies for food and host/prey location (Vet &Dicke,

1992; Bruce et al., 2005; Dicke & Baldwin, 2010). Domes-

tication 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 her-

bivore-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 distri-

bution 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 devel-

opmental 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 tol-

erate plant variation and still be able to capture prey effec-

tively. 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 ene-

mies 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 vola-

tile 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 herbi-

vores 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 forag-

ing behavior and, consequently, their response to herbi-

vore 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 locat-

ing and capturing prey (Gingras et al., 2002; Chen &

Welter, 2003; Reynolds & Cuddington, 2012). Some para-

sitoids 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 domesti-

cation selects for architecturally simpler plants that spa-

tially aggregate herbivore species, parasitoids that attack a

single herbivore at a time could be less effective in control-

ling herbivore populations. Therefore, due to the variabil-

ity in life history characteristics, natural enemy species

may vary in their response to bottom-up changes in herbi-

vore 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 den-

sity, 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: chew-

ing, boring, leaf mining, piercing/sucking, galling, seed

predators (non-seed) natural enemy predators, and para-

sitoids. We attempted to identify as many studies as possi-

ble within each subcategory (plant trait*herbivore guild)in order to identify specific examples of how each insect

4 Chen et al.

guild responded to the plant traits. We found that some

plant trait/insect guild categories were more represented

than others; therefore, we allocated more effort toward

searching for more examples in the plant trait/insect guild

categories that were less represented.

We used general search terms within Web of Science

(*plant trait and variation and insect or herbi* or parasite*or natural enemy or predator or tritrophic), coupled with

separate searches for each of the following morphological

plant traits (leaf size, stem and diameter or variation and

stem length, seed size, flower size, fruit size, seed head size,

flowering uniformity or flowering synchronization,

reduced branching or architectural complexity or number

of branches, trichome density or trichome number, bract

size or length and glume size or length, and tissue tough-

ness) (Table S1). We also combined the general search

terms for tritrophic interactions with search terms on

plant quality (chemical defense or resistance or secondary

metabolites, inducibility, protein concentration or con-

tent, oil concentration or content, and sugar concentration

or content). For the phenology section, we included: phe-

nology, cultivar, nature, budding, crop, agriculture, insect,

herbivore, natural enemy, damage, and cultivar, synch*,and unif*.Due to the broad scope of the study and our mission to

examine all of the relationships within our orthogonal

grid, we chose to perform a qualitative systematic review.

We decided against doing a meta-analysis because the

effort alone would overwhelm our review team and there

was unlikely to be enough data to evenly populate all of

the cells of our grid. Given that 50–500 studies are typicallyused to test a single relationship within a meta-analysis

(Barton & Koricheva, 2010; Chaplin-Kramer et al., 2011;

Letourneau et al., 2011), our grid of 14 plant traits and

eight herbivore feeding guilds or 112 relationships would

quickly become too unwieldy to perform a meta-analysis

on each relationship. During the search process, we

exhaustively searched for at least 20 studies to populate

each plant trait/feeding guild relationship (Table S2).

However, many of plant trait/feeding guild relationships

have not been well studied, so many of the cells fell short

of our goal of 20 studies per relationship.

Our objective was to describe trends that we found in

the literature, knowing full well that the responses of indi-

vidual species can be highly stochastic and that there could

be gaps in the literature. We only summarized the trends

of a particular plant trait/feeding guild relationship if there

were at least three studies in the cell and if the majority of

the studies showed the same direction in the response. We

found that the majority of the reviewed studies tended to

only focus on herbivores that were associated with a single

trait or subset of traits, rather than on the entire insect

assemblage associated with a single plant species

(Table S1).We found that all of the studies examined only

within-population insect responses, examining a single

geographic location or the responses of a single insect pop-

ulation. The only studies that examined herbivore

responses to manipulated plant traits were the studies on

crop plants that involved several insect varieties. We did

not find any studies that examined whether variation in

plant traits resulted in correlated changes across diverse

feeding guilds. This is important because the activity of

key herbivores and their response to plant selection could

cause interactive effects in dictating resource availability

for other herbivores (Tscharntke, 1999). Therefore, inter-

active effects between plants and herbivores can lead to

more complex species interactions than the direct interac-

tions described in Table S1 (but see Stephens et al., 2013).

Physical traits

Enlargement of plant structures

One of the most obvious phenotypic differences between

wild and domesticated plants is the size of the harvested

organs (Evans, 1993). However, increase in the size of tar-

geted organs may be correlated with changes in the size of

other organs (Schwanitz, 1966; Evans, 1993). We exam-

ined the literature to review insect herbivore response to

increases in leaf size, fruit size, seed size, and stem diame-

ter. Many of the studies that matched our criteria also

tested the plant vigor hypothesis (Price, 1991), which pre-

dicts that female herbivores should oviposit on vigorous,

or rapidly growing plants, or plant structures. Within this

hypothetical framework, larger plant structures are consid-

ered to be more vigorous and of higher quality, as they

have attained higher overall growth than average-sized

plants within the population. Across all the major herbivo-

rous insect orders, Cornelissen et al. (2008) found in a

meta-review that herbivores are more abundant on larger

or more vigorously growing plants, but herbivore survival

does not appear to be dependent upon plant vigor. Among

herbivore feeding guilds, sap-sucking, leaf-mining, and

gall-forming insects are the most responsive to variation in

plant vigor (Cornelissen et al., 2008).

Table S1 presents the results categorized by variation in

plant traits and insect feeding guild. For studies that exam-

ined herbivore responses to enlargement of vegetative and

reproductive structures, organ enlargement increased

insect densities, bearing in mind that galling insects and

seed predators/frugivores were overrepresented

(Table S1). Freitas et al. (1999) found, from examining

herbivory patterns of 76 lepidopteran species, that larger

leaves were more likely to be attacked. But for galling

insects, the relationship between leaf size and galling insect

Crop domestication: predictions from the wild 5

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 influ-

enced 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 Pha-

neta 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 germina-

tion 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 domestica-

tion process are: dormancy, seed set and size, color, tough-

ness, time tomaturity, and dispersal (Evans, 1993).

Plant stem diameter typically increases during domesti-

cation due to a reduction in overall branching and reallo-

cation 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 aggre-

gation of the herbivores that attack those structures. Both

the density and accessibility of hosts can influence the for-

aging behavior and efficacy of natural enemies. The

enlargement of plant structures can impact natural ene-

mies 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). Like-

wise, increased size of the sunflower head is associated with

a decrease in the amount of time a parasitoid, Doli-

chogenidea homoeosomae (Muesebeck), spent foraging for

its lepidopteran host, where many were protected within a

refuge (Chen & Welter, 2003). Moreover, D. homoeoso-

mae 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 architec-

turally complex support a more diverse herbivore assem-

blages (Askew, 1980). For example, Araujo et al. (2006)

found that an increase in plant architectural structure pos-

itively 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 herbi-

vores. 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, result-

ing 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 domestica-

tion process (Bellota et al., 2013), but the trend of reduced

6 Chen et al.

trichome density is not consistent across crops (Turcotte

et al., 2014). Similarly, changes in trichome length and

density are inconsistent during domestication and selec-

tive breeding, with some cultivars showing a decrease in

trichomes (Kanno, 1996), and others an increase, espe-

cially when trichomes are selected for as a resistance trait

(Talekar & Lin, 1994). With few exceptions, reduced tri-

chomes are positively correlated with an increase in herbi-

vore 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) tri-

chomes 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 compromis-

ing 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 domestica-

tion (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 simul-

taneously 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 synchro-

nization 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 unifor-

mity and the maturation of targeted structures synchro-

nized with herbivore activity, the herbivore impact on

plant fitness will likely increase (Table S1). For instance,

English-Loeb & Karban (1992) found that a higher pro-

portion 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 lit-erature, 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 neu-

tral effects on ovipositional preferences of specialist

Crop domestication: predictions from the wild 7

lepidopteran herbivores, whereas it had more variable

effects on fitness correlates, such as herbivore survival,

body mass, or development time (Table S2A). Plant sec-

ondary metabolites tended to have a negative effect on the

performance of generalist herbivores but not on specialists

(Table S2A), probably because (many) specialized herbi-

vores 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 com-

pounds on herbivores tend to be compound specific (Bar-

bosa 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 herbi-

vore (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 exam-

ined 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 susceptibil-

ity. 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

Chewing Borers Leaf-miners

Piercing / sucking

Galling Seed predator/ frugivore

↑Response proportion

Parasitoid Predator ↑Response proportion

Leaves, shoots, plant height, stem thickness

↑1, Ø 1 ↑2, ↕ 1 ↑3 ↑1, Ø 1 ↑6 , Ø 1, ↓1

0.72 ↑2, Ø 1, ↓3

0.33

Flowers, fruits, seeds, seed heads

↑10, ↕ 2, ↓1, Ø 1

0.71 ↑1, Ø 1, ↓3

0.20

Simplification of architecture

↑1,↓2 ↑1 ↑1 0.60 ↑3, Ø 2 ↑3 0.86

Reduced trichome densities

↑12, ↕1, ↓1 , Ø 3

↑2, ↓1 ↑2, ↓1 ↑7, ↓2, Ø 1

↑3, Ø 1 0.70 ↑7, Ø 1 ↑3, ↓4, Ø 1

0.63

Reduced tissue toughness

↑3, Ø 1 ↑1 ↑1, ↕ 1, Ø 1

↑1 ↑1, ↓1 0.71 ↑3 ↑1 1.00

Increased phenological uniformity

↑3, ↓1 ↑1,Ø 1 ↑1, ↓1 ↑2 ↑2,↓1, Ø 2

0.60 ↓1

Reduced levels of secondary metabolites

↑15, ↕2, ↓7 , Ø 3

↑1, Ø 1 ↑5, ↓4 , Ø 3

↑1, Ø 2 0.50 ↑13, ↕1, ↓1 , Ø 2

↑1 0.78

Nitrogen, protein, amino acids

↑9, ↕1, Ø1

↑4, ↕1, Ø1

↑3, ↕1, Ø3

↑9, Ø2 ↑5, ↓1 ↓1 0.70 ↓1

Sugars ↑2 ↑1 Ø1 ↑1, Ø2 Ø1 ↓1, Ø1 0.40

seimenelarutaNserovibreH

Traits

Chemical

Physical

Increased nutrition

Enlargement organs /structures

8 Chen et al.

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 direc-

tion (Table S2A). Few studies have reported effects of

reduced phytochemical concentrations on predator per-

formance. Herbivores that are well adapted to their host

plant and sequester phytochemicals from them can experi-

ence increased predation if a reduction in secondary

metabolites causes them to become less deterrent to gener-

alist 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 spe-

cial organs (glandular trichomes) or cells to prevent phyto-

toxicity. 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 cir-

cumvent plant resistance traits (Dussourd et al., 1993;

Inbar et al., 1995; Walling, 2008). Food plant specializa-

tion 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 herbi-

vores perceive and respond to heterogeneity in plant qual-

ity 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 perfor-

mance 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; Rodri-

guez-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 bymost insect herbivore species (Schoonho-

ven 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 domestica-

tion affects inducible plant resistance by comparing the

wild progenitor with a domesticated species. It is hypothe-

sized that, if production costs are high, plants should rely

on constitutive resistance when herbivore attack is fre-

quent and predictable, whereas plants should rely on

inducible resistance when herbivore attack is more unpre-

dictable (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 (Tur-

lings 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 feed-

ing guilds induce qualitatively and quantitatively different

HIPV blends (Arimura et al., 2009; McCormick et al.,

2012). Relatively little is known about how plant domesti-

cation 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 discrimi-

nate 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

Crop domestication: predictions from the wild 9

inadvertently affect theHIPV blends and the ability of crop

plants to recruit natural enemies.

There is some evidence that natural enemies can dis-

criminate 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 culti-

vated cabbage (Gols et al., 2011). In contrast, the braconid

D. homoeosomae clearly preferred to orient to the domesti-

cated instead of the wild sunflower, although flowers were

controlled for size (Chen &Welter, 2003). Similar patterns

were found for Stenocorse bruchivora (Crawford), a para-

sitoid 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 varia-

tion 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 nutri-

tional content within crops, such as sugar (sugar beet or

sugarcane), oil (sunflower, canola), protein (maize, vari-

ous crops), or mineral content (Evans, 1993). It has also

been demonstrated that artificial selection can dramati-

cally alter plant nutritional composition. One of the best-

known 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 con-

tent 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 deter-

mining 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 domesti-

cation 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 nitro-

gen 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 prefer-

ence of insect herbivores, especially piercing-sucking, leaf

mining, and chewing herbivores (Table S2B). Although

chewing herbivores showed a trend of increased perfor-

mance on plants with higher nitrogen levels, the effect was

more variable (Table S1F). The effects of increased nitro-

gen 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 per-

formance 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.

10 Chen et al.

Increased sugar content

Some crops such as maize, sugar beet, and sugarcane, have

been targeted by domestication for higher sugar content

(Jackson, 2005; Basnayake et al., 2012; Bian et al., 2014).

We did not find enough studies per guild to see a clear

relationship between higher sugar content and insect

performance (Tables S2B and 1). However, unnaturally

high sugar content could negatively affect herbivores, as

the relationship between sugar content and herbivore

abundance may be curvilinear. For example, Palevsky

et al. (2005) describe an upper threshold of sugar content

in dates, beyond which populations of the spider mite

Oligonychus afrasiaticus (McGregor) decline. The only

negative association between sugar content and insect per-

formance was in a frugivorous tephritid fly, Bactrocera

cucurbitae (Coquillett), where increased sugar in the bitter

gourd decreased larval density (Dhillon et al., 2005).

Summary of evidence

We examined the literature on insect–plant interactions todetermine how insect herbivores and natural enemies

responded to directional changes in plant traits targeted by

domestication. We collected data with the intention of

developing the most evenly distributed dataset; however,

we found that some plant trait and insect guild relation-

ships were better studied than others. Although there was

uneven coverage in the literature, we attempted to detect

some broader trends (Table 1). We only considered a rela-

tionship as displaying a detectable trend if: (1) there were

at least three independent studies examining the relation-

ship, (2) >65% of the studies within the grid cell showed

the same directionality for the relationship, and (3) pat-

terns within individual herbivore guilds were not contra-

dictory. The shaded cells within Table 1 highlight the

herbivore guilds that responded to the examined plant

traits. Overall, we found that herbivores were studied >39more often than natural enemies (77.1 vs. 22.9% of stud-

ies), and parasitoids were more frequently studied than

predators (Table 1).

Herbivores clearly benefit from directional selection on

the traits that characterize the domestication syndrome,

but the effects on natural enemies were less consistent or

not well documented (Table 1). Among the nine plant

traits that we examined, there was a positive relationship

between six of the plant traits and herbivore performance

or behavior (Table 1). Variation in physical traits clearly

influenced patterns of herbivory more strongly than

changes in secondary metabolites. Out of the nine cate-

gories of physical traits, five strongly benefited herbivores,

and an additional two categories showed a moderate

benefit to herbivores. The physical traits that appeared to

be strongly associated with increased herbivory were

enlargement of (both vegetative and reproductive) plant

structures, reduction in trichomes, and decreased tissue

toughness. We found that physical plant traits frequently

influenced the likelihood that herbivores would oviposit,

survive, and damagemore plant tissue (Table S1).

Although domestication has frequently resulted in a

reduction in secondary metabolites (Meyer et al., 2012),

the relationship between decreases in constitutive sec-

ondary metabolites and herbivory was not consistent in

this dataset (Table S2A). However, many insect pests and

their natural enemies show improved performance on

crop plants with decreased secondary metabolites com-

pared to their wild progenitors (Chen et al., 2015). Never-

theless, to conclusively determine that a decrease in

secondary metabolites leads to a consistent positive effect

on insect performance, many more studies are needed.

These studies need to be performed in a wide range of nat-

ural and agro-ecosystems, including herbivores and natu-

ral enemies from different feeding guilds that display

varying degrees of specialization. For instance, generalist

and specialist herbivores may respond differently to a

domestication gradient (Ali & Agrawal, 2012). In addition,

herbivorous species likely vary in how phenotypically plas-

tic they behave in response to novel ecological variation.

Changes in plant quality were more implicated in affect-

ing herbivore growth and development. We did not detect

consistent herbivore responses to secondary metabolites.

Most of the studies investigated the effects of secondary

plant chemistry on insects in the laboratory, so no clear

predictions can be made on how reduced levels of sec-

ondary metabolites affect behavior and performance of

both herbivores and their natural enemies under field con-

ditions. For nutritional traits, we found a very consistent

and strong increase in herbivore abundance in response to

increased protein content (Table S2), suggesting that her-

bivores closely mirror human preferences in nutritional

content. We did not find sufficient evidence to evaluate

herbivore responses to increased sugar content. We also

did not find any studies examining natural enemy

responses to the higher herbivore levels as a result of

increased nutritional quality of the food plants.

Due to the paucity of studies, it is still difficult to pre-

dict how selection on domestication traits may influence

natural enemies (Table S2). The two consequences that

were best supported were that structure enlargement

reduced parasitism and a decreased trichome density

improved parasitoid foraging efficiency. Decreased tissue

toughness and decreased inducibility of resistance also

appear to improve parasitoid activity, but again, more

Crop domestication: predictions from the wild 11

studies are needed to resolve the strength of this

relationship.

Given that domestication can alter the density and phys-

ical 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; Rom-

stock-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.

Potential outcomes

On the basis of the evidence reviewed in this study, we out-

line potential outcomes on herbivore and natural enemy

responses to single plant traits targeted by plant domesti-

cation. Our goal is to make generalizations on the poten-

tial 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), con-

trasting evidence (CE), or insufficient evidence (IE) to

draw conclusions. We only present a representative subset

of these potential outcomes for the various plant traits pre-

sented 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 acces-

sibility (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 herbi-

vores 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

enlargement of organs/structure and their perfor-

mance due to decreased toxicity will increase the avail-

ability of hosts/prey quality to support parasitoid

development (CE).

6 On the other hand, increased herbivore performance

on crop plants due to higher nutrient content may

negatively affect natural enemies due to faster herbi-

vore development and increased ability to encapsulate

parasitoid eggs (‘slow growth-highmortality’ hypothe-

sis) (CE).

7 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 domes-

tication will be altered more than the performance of

herbivores and natural enemies associated with tissues

that are not targeted by domestication (IE).

8 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).

9 Selection on plant traits will differentially affect gener-

alists and specialist parasitoids. For example, plant

volatiles may have been reduced in crop plants render-

ing them less attractive or harder to find for generalists

than for specialist parasitoids (CE).

10 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 her-

bivore 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 commu-

nity 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,

12 Chen et al.

flowers, seed heads, and stems have been selected to be lar-

ger 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 resis-

tance, such as trichomes or latex. However, the meta-anal-

ysis 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 spe-

cialist herbivores vary in their response to plant secondary

compounds, as plant chemicals may either stimulate or

inhibit herbivores (Schoonhoven et al., 2005; Ali & Agra-

wal, 2012). Turcotte et al. (2012) found that domestica-

tion (in a study using 29 independent domestication

events) can increase the survival or performance of gener-

alist 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 special-

ists, because specialists have specific enzymatic machinery

to detoxify specific plant defenses (Ratzka et al., 2002).

Given that many plant traits selected by crop domestica-

tion 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 nat-

ural 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 domes-

tication (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 funda-

mentally alters interactions between plants, herbivores,

and their natural enemies. Given that selection for the

growth forms favored by humans appear to enhance her-

bivory, 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

Crop domestication: predictions from the wild 13

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. Amore careful analysis of the commu-

nity-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 his-

tory traits such as host stage attacked (when given) and

endo- or ectoparasitism. We further indicated (when

known) whether the insects were generalists (G) (polypha-

gous for herbivores, attacking species in more than one

genus for natural enemies) or specialists (S) (mono- or oli-

gophagous 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 tri-

chome densities, (D) reduced tissue toughness, and (E)

increased phenological uniformity. Results are presented

with arrows when statistically significant. Symbol clarifica-

tion: ↑, increased; ↓, decreased; ↕, variable response; Ø, noeffect, 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 his-

tory traits such as host stage attacked (when given) and

endo- or ectoparasitism. We further indicated (when

known) whether the insects were generalists (G) (polypha-

gous for herbivores, attacking species in more than one

genus for natural enemies) or specialists (S) (mono- or oli-

gophagous 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 pre-

sented 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.

20 Chen et al.