Oecologia (2013) 173:1425–1437
DOI 10.1007/s00442-013-2728-2
PLANT-MICROBE-ANIMAL INTERACTIONS - ORIGINAL RESEARCH
Facilitated by nature and agriculture: performance of a specialist
herbivore improves with host‑plant life history evolution,
domestication, and breeding
Amanda M. Dávila‑Flores · Thomas J. DeWitt ·
Julio S. Bernal Received: 9 March 2013 / Accepted: 27 June 2013 / Published online: 19 July 2013
© Springer-Verlag Berlin Heidelberg 2013
Abstract Plant defenses against herbivores are predicted
to change as plant lineages diversify, and with domestication and subsequent selection and breeding in the case of
crop plants. We addressed whether defense against a specialist herbivore declined coincidently with life history evolution, domestication, and breeding within the grass genus
Zea (Poaceae). For this, we assessed performance of corn
leafhopper (Dalbulus maidis) following colonization of
one of four Zea species containing three successive transitions: the evolutionary transition from perennial to annual
life cycle, the agricultural transition from wild annual
grass to primitive crop cultivar, and the agronomic transition from primitive to modern crop cultivar. Performance
of corn leafhopper was measured through seven variables
relevant to development speed, survivorship, fecundity, and
body size. The plants included in our study were perennial
teosinte (Zea diploperennis), Balsas teosinte (Zea mays
parviglumis), a landrace maize (Zea mays mays), and a
hybrid maize. Perennial teosinte is a perennial, iteroparous
species, and is basal in Zea; Balsas teosinte is an annual
species, and the progenitor of maize; the landrace maize is
a primitive, genetically diverse cultivar, and is ancestral to
the hybrid maize; and, the hybrid maize is a highly inbred,
modern cultivar. Performance of corn leafhopper was poorest on perennial teosinte, intermediate on Balsas teosinte
Communicated by Evan H DeLucia.
A. M. Dávila‑Flores · J. S. Bernal (*) Department of Entomology, Texas A&M University,
College Station, TX 77843‑2475, USA
e-mail: juliobernal@tamu.edu
T. J. DeWitt Department of Wildlife and Fisheries Sciences,
Texas A&M University, College Station, TX, USA
and landrace maize, and best on hybrid maize, consistent
with our expectation of declining defense from perennial
teosinte to hybrid maize. Overall, our results indicated that
corn leafhopper performance increased most with the agronomic transition, followed by the life history transition, and
least with the domestication transition.
Keywords Zea mays mays · Zea mays parviglumis ·
Zea diploperennis · Teosinte · Dalbulus maidis
Introduction
Crop plants frequently are poorly defended against herbivore insects compared to their ancestors and wild relatives. For example, Rosenthal and Dirzo (1997) found that
relative injury by a diverse assemblage of folivorous and
stem-boring insects to various taxa of Zea L. (Poaceae)
was predicted by the hypothesis that a gradient of herbivore defense, from strongest to weakest, would be evident
between the “most ancestral” and “most domesticated”
Zea taxa in their study. Their hypothesis followed the
resource allocation hypothesis, which predicts a trade-off
between resource allocation to competing functions, such
as productivity and defense, so that increased allocation
to one function is correlated with decreased allocation to
the other (Herms and Mattson 1992; Mole 1994; Obeso
2002). In particular, Rosenthal and Dirzo (1997) found that
a wild, perennial Zea (Zea diploperennis Iltis, Doebley &
Guzman) suffered the least herbivory, followed by a wild
annual taxon (Zea mays ssp. parviglumis Iltis & Doebley),
a landrace maize (Zea mays ssp. mays L.), and a modern,
high-yielding maize (Zea mays mays), which suffered the
most herbivory. In some cases, differences in the strength
of herbivore defenses between domesticated plants and
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their wild ancestors are due to differences in the quality
and/or quantity of chemical defenses, and are evident as
direct effects on herbivore performance or on recruitment
of natural enemies of herbivores. Thus, Benrey et al. (1998)
found that the herbivores Pieris rapae L. and Zabrotes subfasciatus (Boheman) performed better on cultivated vs.
wild crucifers (Lunaria L., Brassica L.) and beans (Phaseolus L.), respectively. Similarly, Gols et al. (2008) found
that both P. rapae and Mamestra brassicae L. performed
better on cultivated cabbage (Brassica oleracea L.) than
on wild cabbage under controlled, greenhouse conditions.
Several studies focused on Zea revealed significant variation among maize cultivars and teosintes (the wild taxa of
Zea) in the production of herbivore-induced volatiles that
attract the natural enemies of herbivores (Gouinguene et al.
2001; Fritzsche-Hoballah et al. 2002; Degen et al. 2004),
while another found more plant injury in the field and better
performance in the laboratory of the herbivore Spodoptera
frugiperda (J.E. Smith) on a maize landrace compared to
Balsas teosinte (Z. m. parviglumis), the immediate ancestor
of maize (Takahashi et al. 2012). In other cases, domestication seemed to have weakened plant defenses because it
has created a refuge from natural enemies for herbivorous
insects. For example, Chen and Welter (2005, 2007) found
that the harder and larger seeds of domesticated sunflower
(Helianthus annus L.) compared to wild sunflower partially
protected the larvae of Homoeosoma electellum Hulst from
parasitoids, which suffered less parasitism on domesticated
sunflower. Similarly, Wang et al. (2009) found that larvae
of Bactrocera oleae (Rossi) suffered less parasitism on
domesticated olive (Olea europaea L.) than on wild olive
because the larger fruits of the former provided larvae a
structural refuge against parasitism.
Following crop domestication, selection by early farmers and subsequent directed breeding may lead to differences in plant defense levels among crop wild ancestors,
landraces, and modern high-yielding cultivars. High-yielding crop cultivars (e.g., hybrid and other modern varieties)
are the products of systematic breeding efforts emphasizing
high productivity (reproductive and/or vegetative), and typically have narrow, inbred genetic backgrounds. In contrast,
ancestral crop cultivars, such as landraces, are genetically
diverse and have been selected by local environments and
farmers over many generations to satisfy particular dietary,
culinary, and other needs, while maintaining moderate productivity under variable environmental conditions. Thus,
Rosenthal and Dirzo (1997) found differences in insectcaused plant injury levels between landrace maize and
modern, high-yielding maize; and, Rodríguez-Saona et al.
(2011) found that Lymantria dispar (L.) performed better
on a high-yielding, American cranberry (Vaccinium macrocarpon Aiton) cultivar compared to ancestral cultivars, and
that chemical defenses were reduced in the high-yielding
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Oecologia (2013) 173:1425–1437
cultivar. Other studies showed differences in emission of
volatiles that attract natural enemies and, correspondingly,
in recruitment of natural enemies among maize cultivars,
including maize landraces and modern, high-yielding cultivars (Rasmann et al. 2005; Tamiru et al. 2011).
In addition to effects of directed human selection
through domestication and breeding, natural selection and
evolutionary processes, such as life history evolution, may
affect plant defense against herbivory (Bazzaz et al. 1987).
Presumably, plant life histories reflect adaptations to environments with differing environmental pressures, including herbivore pressures. Thus, perennial species generally
may allocate more resources to their root systems and herbivore defenses because they must survive environmental extremes across growing seasons and are more likely
to suffer injury from herbivores and pathogens over their
lifetime, while annual species generally allocate more to
growth and reproduction because their reproductive opportunities are limited to a single growing season: it pays to
maximize present reproduction when future reproduction
is not an option (Bazzaz et al. 1987). While few studies
have compared the defense strategies of closely related
perennial and annual plant species, some predictions can
be made concerning the strength or nature of defenses
on the bases of life history theory. For example, the plant
apparency hypothesis predicts that apparent plants, such
as perennial species, will invest in broadly effective antiherbivore defenses, including compounds that are effective
against specialists and generalist herbivores, while unapparent plants, such as annual species, will invest in qualitative toxins that are effective against non-adapted specialists
and generalist herbivores (Feeny 1976). Other predictions
can be made on the bases of resource allocation strategies, including at an evolutionary level, because allocation strategies should involve balancing plant reproduction
against survivorship, and the influences of such balancing
on overall fitness. Mutikainen and Walls (1995) directly
compared the defense strategies of closely related annual
and iteroparous perennial plants under variable levels of
resource availability, and hypothesized that perennials
should show stronger induced responses to herbivory than
annual plants, which tend to invest more in reproduction
than defense regardless of the level of available resources.
Other studies found that both defense against and tolerance of herbivory by caterpillars were stronger in perennial teosinte (Zea diploperennis Iltis, Doebley & Guzmán)
compared to annual, Balsas teosinte (Rosenthal and Welter 1995; Rosenthal and Dirzo 1997). Nault and Madden
(1985) compared the performances of insect (Dalbulus
DeLong) specialists on perennial (Tripsacum L. and Zea)
or annual grasses (Zea) and non-specialists (on both Tripsacum and Zea) and found that the specialist’s performance
generally suffered on perennial compared to annual hosts,
Oecologia (2013) 173:1425–1437
independently of the insect’s specialization on perennial or
annual hosts, suggesting that perennial species are better
defended than closely related annual species.
In this study, we compared the performance of a specialist herbivore, corn leafhopper Dalbulus maidis (Delong &
Wolcott) (Hemiptera: Cicadellidae) on a suite of host plants
(Zea spp.) representing three transitions evident in the host
plant genus: first, a life history transition, from perennial to
annual life cycle; second, a domestication transition from
wild annual to domesticated annual, and; third, a breeding transition, from ancestral, landrace cultivar to modern,
hybrid cultivar, derived from the landrace. Our objective
was to determine whether such transitions in the host plant
genus are correlated with differences in plant defenses, as
indicated by the specialist insect’s performance. Plants are
predicted to evolve divergent defense strategies against
specialist and generalist insects (van der Meijden 1996;
Lankau 2007; Ali and Agrawal 2012). For example,
Agrawal et al. (2009b) found that while the content of qualitative defensive compounds (cardenolides) declined with
Asclepias phylogeny, that of quantitative compounds (phenolics) escalated, and suggested that specialist herbivores
promoted a shift in the defensive strategy of Asclepias
away from direct defense and toward increased tolerance
(regrowth ability) (Agrawal and Fishbein 2008; Agrawal
et al. 2009b). Our objective was met through a “forced colonization” approach: corn leafhopper females were forced
to colonize one of five host plant taxa, and their offspring’s
performance was monitored from birth to reproduction on
the newly colonized host. The five host plants considered
in this study were: perennial teosinte (Z. diploperennis);
two “geographic populations” of Balsas teosinte (Z. mays
parviglumis), i.e., maize’s immediate ancestor; and two
maize (Z. mays mays) cultivars, an ancestral landrace and
a derived, modern hybrid. Correspondingly for each transition, viz. life history, domestication, and breeding, we
hypothesized that corn leafhopper performance would be
improved (i.e., plant defense is weaker) on Balsas teosinte
relative to perennial teosinte, on landrace maize relative to
Balsas teosinte, and on hybrid maize relative to landrace
maize. Overall, the study’s results will help us understand
how natural (life history) and artificial (domestication,
breeding) selection acting on plants may influence herbivore performance, microevolution and host-race formation,
and the emergence and evolution of agricultural pests.
Materials and methods
Insect and host plant natural history
Corn leafhopper feeds and reproduces almost exclusively
on members of the grass genus Zea (Nault 1990; Pitre
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1970). Although it is endemic in low- to mid-elevations
(<1,000 m a.s.l.) in subtropical and tropical areas, its distribution ranges from northern Argentina to California and the
USA Gulf states (Heady et al. 1985; Triplehorn and Nault
1985). The genus Dalbulus is believed to have evolved in
western-central Mexico on the all-perennial Tripsacum
and Zea (Nault and DeLong 1980; Dietrich et al. 1998),
and then expanded its host range to the annual Zea species,
including maize (Triplehorn and Nault 1985; Triplehorn
et al. 1990; Dietrich et al. 1998). Unlike most of its congeners, corn leafhopper overwinters as an active, nonreproducing adult (Larsen et al. 1992; Summers et al. 2004;
Moya-Raygoza et al. 2007), and can feed on a variety of
hosts that are known associates of maize and wild Zea, i.e.,
teosintes (Pitre 1970).
The grass genus Zea includes five species: Zea diploperennis (perennial teosinte), Zea perennis (Hitcht.) Reeves
& Manglesdorf, Zea luxurians (Durieu & Asch.) Bird,
Zea nicaraguensis Iltis & Benz, and Zea mays. The last
species is further divided into four subspecies: Zea mays
huehuetenangensis (Iltis & Doebley) Doebley, Zea mays
mexicana (Schrader) Iltis, Zea mays parviglumis (Balsas
teosinte), and Zea mays mays (maize) (Buckler and Stevens 2005). Maize is the only domesticated taxon in the
genus Zea, and it is the most widely distributed and cultivated host taxa considered in this study. Studies have
shown that maize was domesticated in western-southern
Mexico from Balsas teosinte, from where it subsequently
spread throughout the Americas and worldwide (Matsuoka
et al. 2002; Fukunaga et al. 2005; Vigouroux et al. 2008;
Heerwaarden et al. 2011). Both Balsas teosinte and perennial teosinte occur in central, western Mexico, the first at
low- to mid-elevations (ca. 480–1,360 m a.s.l.), and the second at mid- to high-elevation (ca. 1,350–2,250 m a.s.l.) in a
small mountain range (Benz et al. 1990; Sánchez-González
et al. 1998; Buckler and Stevens 2005). In this study, we
compared the performance of corn leafhopper on perennial
teosinte, Balsas teosinte, a landrace maize cultivar and a
hybrid maize cultivar.
Three transitions relevant to plant defense against herbivores are evident in Zea: life history, domestication,
and breeding. The hypotheses that those transitions influenced the strength of herbivore defenses in Zea can be
rigorously tested with corn leafhopper because of its close
affinity with Zea. Specialist herbivores, such as corn leafhopper, are predicted to be susceptible to novel defenses
encountered in novel, potential hosts, but well adapted for
coping with their host plant’s defenses (Ali and Agrawal
2012). Thus, corn leafhopper’s performance would differ on perennial teosinte, Balsas teosinte, landrace maize,
and hybrid maize if differences in their herbivore defenses
approximate the differences prevalent among novel host
plants.
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Experimental insects and host plants
All corn leafhoppers used in this study were obtained from
a colony initiated with individuals collected from maize
fields in the vicinity of El Grullo (Jalisco state, Mexico;
19°48′N, 104°13′W) in the summer of 2008. The colony
was kept in a plastic frame mesh cage (BugDorm-44545F;
Megaview Science, Taichung, Taiwan) on seedlings of a
Mexican landrace of maize (Elotes Occidentales), usually
in their four- to six-leaf stage, in a room with a photoperiod
of 12:12 h (light:dark; L:D) and a temperature of 24–28 °C.
Five different host plants were grown from seed in a
greenhouse: perennial teosinte (Z. diploperennis), Balsas
teosinte 1 (Z. mays parviglumis), Balsas teosinte 2, landrace maize (Z. mays mays), and hybrid maize (Z. mays
mays). Seed of perennial teosinte was collected in the
location of Corralitos (19°36′48.78″N, 104°18′23.49″W),
within the Sierra de Manantlán Biosphere Reserve
(Jalisco state, Mexico) (UNESCO 2011). Balsas teosinte
1 and Balsas teosinte 2 were collected in San Lorenzo
(Ejutla, Jalisco, Mexico; 19°56′60″N, 103°59′0″W) and
El Cuyotomate (Ejutla, Jalisco, Mexico; 19°58′10.39″N,
104°4′3.00″W), respectively. Seed of Tuxpeño landrace
maize were obtained from USDA NPGS (GRIN accession PI 511649), and seed of hybrid maize was purchased
from a commercial seed provider (variety NB2; Híbridos
NOVASEM, Zapopan, Jalisco, Mexico). The hybrid maize
was plausibly derived from Tuxpeño germplasm because
both are subtropical, white dent maizes, and Tuxpeño is the
most widely adapted Mexican maize landrace and is used
extensively for breeding of subtropical maizes (SánchezGonzález 2011; Wen et al. 2012).
All plant seedlings were grown on BACCTO Premium
Potting soil (85–15–10) (Michigan Peat, Houston, TX),
without fertilizer. The perennial and Balsas teosinte 1 and 2
plants were grown from seeds that were germinated in Petri
dishes after they were removed from their fruit cases with
the aid of nail clippers. Seedlings were used in the experiment when they were in the V3–V5 stage (i.e., from three
to five collared leaves).
Experiment
Young (1–5 days old ± 1.5 days) corn leafhopper females
were obtained by creating cohorts by placing a potted
maize seedling (Elotes Occidentales landrace) inside the
colony cage for 3 days so that females from the colony
would oviposit on the seedling. The seedling was removed
from the colony cage, all adult and immature corn leafhoppers were removed, and the seedling was held in a separate cage, free of corn leafhoppers. Corn leafhoppers were
allowed to emerge, develop to adult stage, and mate. Adult
females were then removed with the aid of an aspirator for
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Oecologia (2013) 173:1425–1437
use in the experiment. This process was repeated weekly to
ensure a constant supply of corn leafhopper females of a
known age. To promote oviposition during the experiment,
corn leafhopper females used in each trial were isolated,
without access to host plant substrate, in 50-ml centrifuge
tubes (with a fine-mesh window on the cap) containing a
moist paper towel for 24 h immediately prior to initiating a
replicate trial.
For each replicate trial, individual corn leafhopper
females (hereafter “F0 females”) were forced to colonize one of five host plant seedlings: perennial teosinte
(n = 8 females), Balsas teosinte 1 (n = 8), Balsas teosinte 2 (n = 7), landrace maize (n = 10), or hybrid maize
(n = 7). Forced colonization consisted of caging an individual F0 female for 48 h on a leaf (youngest leaf after the
whorl leaf) of a seedling. Cages consisted of two frames
(13 × 8 × 1 cm) cut from 10 mm-thick Cellfoam 88 (Midwest Products, IN) lined with a soft-foam gasket between
the frames (internal dimensions 11 × 6 × 1.5 cm), which
sandwiched the leaf and contained the corn leafhopper
female. After 48 h, each F0 female and cage were removed,
and the pot holding each seedling was fitted with a plastic cage to enclose the seedling and incubated (25 ± 2 °C,
~70 relative humidity, 14:10-h L:D dark cycle) until a
generation of new (F1) adults emerged. Seedlings were
examined daily during incubation to record the following
performance variables: (1) F0 fecundity (=mean number
of eggs laid by F0 females in 48 h); (2) F0 egg survival
(=proportion eggs hatching based on F0 fecundity); (3)
F0 egg development time (=mean days from oviposition
to appearance of each 1st-instar nymph); (4) F1 nymph
development time (=mean days between appearances of
F1 1st-instar nymphs and adults); (5) F1 nymph survival
(=proportion of 1st-instar nymphs surviving to adulthood,
i.e., F1 adults); (6) F1 female mass (=weight of adult F1
females); (7) F1 male mass (=weight of adult F1 males);
and (8) F1 fecundity (=mean eggs laid by F1 females in
48 h on the host on which they developed). Leaves were
excised from seedlings exposed to F0 females in order to
measure F0 fecundity and estimate F0 egg survival. This
was done by staining the leaves (and eggs within) following an optimized McBride technique (Backus et al. 1988),
then counting the number of F0 eggs laid in each plant,
while noting the number of eggs that showed evidence of
hatching. Once F0 females were removed, each seedling
was examined daily to record the number of (F1) 1st–instar
nymphs emerging daily (indicating F0 egg development
time), and the number of F1 adults emerging daily (indicating F1 nymph development time); the number of F1 adults
in relation to 1st–instar nymphs was used to estimate F1
nymph survival. When emergence of F1 adults ceased, they
were grouped by gender, and all males and a subsample of
females were sacrificed by freezing then dried to constant
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weight (3 days at 80 °C) to measure their mass; the remaining females were individually caged on a new plant of the
same host on which they had developed (i.e., the host that
their female parent was forced to colonize), and allowed to
oviposit for 48 h in order to assess F1 fecundity, after leaf
staining, as described above.
tested whether F1 fecundity changed relative to F1 fecundity via a one-sample t-test on the differences between F1
and corresponding F0 fecundity values (=mean F1 fecundity − F0 fecundity, per replicate) under the hypothesis that
the difference was nil.
Statistical analysis
Results
We applied multivariate ANOVA (MANOVA) (x = host
plants; y = performance variables, except F0 fecundity
which was used as a weight) to address whether the performance of corn leafhopper varied among the five host plants,
followed by planned, a priori contrasts (with Sidak’s multiple comparisons correction) (Abdi and Williams 2010) to
evaluate whether corn leafhopper overall performance was
affected by transitions in Zea: (1) life history, i.e., perennial
teosinte vs. Balsas teosinte 1 and 2; (2) domestication, i.e.,
Balsas teosinte 1 and 2 vs. landrace maize; and (3) breeding, i.e., landrace maize vs. hybrid maize. Additionally, we
generated variable maps to visualize how each performance
variable contributed to differentiation between two host
plants within each a priori contrast (Numerical Dynamics
2013). The x-axis of the variable maps indicates the average performance ratio between two host plants, while the
y-axis indicates −log(ratio); performance variables that
increase with a given transition are positioned in the upperright panel, while those that decrease are positioned in the
lower-left panel, and each variable’s contribution to differentiation is indicated by its distance from the origin.
Univariate, fully randomized ANOVA was applied to
each of the performance variables indicated above, except
F1 fecundity. For F1 fecundity, we used univariate analysis
of covariance (ANCOVA) with F0 eggs as a covariable to
guard against ovipositional preference for maize (the host
plant used to maintain the corn leafhopper laboratory colony) in the F1 females, although a prior study showed that
(F0) females did not show an ovipositional preference for
any of the host plants when they were denied a choice of
host plant (Bellota-Villafuerte 2012). When warranted by
a significant ANOVA or ANCOVA (P < 0.05), we applied
planned, a priori contrasts (with Sidak’s correction; Abdi
and Williams 2010) to evaluate whether individual performance variables were affected by transitions in Zea (1) life
history, (2) domestication, and (3) breeding, as described
above.
We used mean F1 and corresponding F0 female fecundity on each of the host plants to assess whether colonization of the different hosts affected the (48 h) fecundity
of (F1) females relative to that of the corresponding (F0)
female parent. Based on the mean F1 and F0 female fecundity values we calculated relative fecundity of F1 to F0
females (=mean F1 fecundity/F0 female fecundity), and
One-way MANOVA confirmed a significant multivariate
main effect of host plant on corn leafhopper performance
(Wilks’ λ = 0.068, P < 0.0001) (Fig. 1), and a priori contrast comparisons showed that corn leafhopper performance
improved with the transitions in life history (P = 0.004,
F7, 29 = 3.94), domestication (P = 0.013, F7, 29 = 3.15),
and breeding (P = 0.001, F7, 29 = 5.03). The major axis
of differences in corn leafhopper performance on the five
host plants discriminated performance according to host
plant life history, while the horizontal axis discriminated
according to domestication and breeding status. Variable maps showed that performance variables associated
with F1 individuals (F1 nymph development time, nymph
survival, female mass, male mass, and fecundity) contributed most to the effects of the three transitions that were
evaluated. Thus, F1 fecundity, F1 female mass, and F1 male
mass contributed most to the effect of life history transition
(Fig. 2a), F1 nymph survival contributed most to the effect
of domestication transition (Fig. 2b), and F1 female mass
and F1 male mass contributed most to the effect of breeding
Fig. 1 Multivariate ANOVA centroid plot of corn leafhopper (Dalbulus maidis) performance variables on five Zea host plants. The plot
shows the centroids (multivariate least squares means) on the first
two canonical variables for each host plant. The first canonical axis
is the vertical axis, while the second canonical axis is the horizontal axis. Biplot rays radiating from origin (overall mean) show directions of performance responses in canonical space; ellipses show the
95 % confidence region for the centroid of each host plant. From
left to right, performance variable biplot rays are adult male size, F1
fecundity, nymph-adult development time, nymph-adult survivorship,
and adult female size; host plants are perennial teosinte (Zea diploperennis; Perennial), Balsas teosinte (Zea mays parviglumis; Balsas
1, Balsas 2), and maize (Zea mays mays; Landrace, Hybrid). A piori
contrasts (P ≤ 0.017) indicated that corn leafhopper performance was
positively affected by transitions in Zea from perennial to annual life
cycle (perennial teosinte vs. Balsas teosintes 1 and 2), from wild to
domesticated taxon (Balsas 1 and 2 vs. landrace maize), and from
genetically diverse to genetically narrow agricultural cultivar (landrace maize vs. hybrid maize)
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-5.3
Oecologia (2013) 173:1425–1437
F1 eggs
A
Male size
-Log(P)
Egg development
Female size
Up-regulation
Egg survival
Nymph survival
-5.3
-1.4
Down-regulation
Nymph development
B
Nymph survival
-Log(P)
Egg survival
Female size
Up-regulation
Male size
Nymph development
F1 eggs
Egg development
-1.4
-2.3
Down-regulation
Female size
C
Male size
-Log(P)
Nymph survival
F1 eggs
Egg development
Up-regulation
Nymph development
Egg survival
-2.3
Down-regulation
Fig. 2 Variable maps showing that a F1 female fecundity (F1 eggs),
adult female (Female size) and male sizes (Male size), and nymph
to adult development time (Nymph development) are the performance variables that most contribute to differentiation (indicated by
distance from origin) between corn leafhopper’s (Dalbulus maidis)
performance on perennial teosinte (Z. diploperennis) and Balsas teosinte (Z. mays parviglumis); b nymph survival to adult (Nymph survival) is the variable that most contributes to differentiation between
performance on Balsas teosinte and landrace maize (Z. mays mays),
and c adult female size is the variable that most contributes to differentiation between performance on landrace maize and hybrid maize.
Dotted ellipses contain individual performance variables not found
to differ between host plant pairs in each plot (P > 0.017, a priori
contrasts; see text)
transition (Fig. 2c). Similarly, univariate ANOVA (details
below) confirmed that all performance variables associated
with F1 individuals (nymph development time, nymph survival, female and male mass, and fecundity), but none with
F0 individuals (fecundity, egg survival, egg development
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time) significantly affected overall corn leafhopper performance. Taken altogether, MANOVA suggested that corn
leafhopper performance was best on hybrid maize, poorest
on perennial teosinte, and intermediate on Balsas teosintes
1 and 2 and landrace maize (Fig. 1).
The (univariate) ANOVA results indicated that corn leafhopper F0 fecundity, F0 egg survival, and F0 egg development time were not affected by the host plant colonized
by the parental female (all F4, 35 ≤ 1.0, P ≥ 0.4). Thus,
across the five host plants, corn leafhopper F0 fecundity was 29.5 ± 10.5 eggs (mean ± SD), F0 egg survival
was 73.2 ± 6.3 %, and F0 egg development time was
8.3 ± 0.7 days.
In contrast to F0 fecundity, survival, and egg development time, the nymph development time, nymph survival, female and male masses, and fecundity of F1 corn
leafhoppers were affected by the host plant colonized
by the parental female (Fig. 3a–e). The F1 nymph to
adult development time (P = 0.001) (Fig. 3a), survivorship of nymphs (P = 0.006) (Fig. 3b), mass of females
(P < 0.0001) and males (P < 0.0001) (Fig. 3c, d), and
fecundity of F1 females (P < 0.0003) (Fig. 3e) were
all affected by the host plant that was colonized by the
female parent. Of the three relevant transitions, the life
history transition affected the most corn leafhopper performance variables (Fig. 4). Thus, nymph to adult development time was longer (P = 0.0005) (Fig. 4a), female
and male adult mass higher (P ≤ 0.0001) (Fig. 4b, d),
and fecundity greater (P = 0.0001) (Fig. 4c) on (annual)
Balsas teosinte compared to perennial teosinte. The effect
of the domestication transition was evident in the higher
nymph to adult survivorship on landrace maize compared
to Balsas teosinte (P = 0.016) (Fig. 5), while the effect
of the breeding transition was evident in the greater mass
of adult females on hybrid maize compared to landrace
maize (P = 0.0003) (Fig. 6).
For each host plant, the fecundity of F1 females seemed
to suffer relative to that of their (F0) female parent’s fecundity, from a low of ~10 % decrease in females whose
parents colonized Balsas teosinte 1 to a high of ~89 %
decrease in females whose parents colonized perennial teosinte (Table 1). However, only the fecundity loss of females
whose parents colonized perennial teosinte was statistically
significant (P < 0.01).
Discussion
The results of this study showed that performance of the
specialist herbivore corn leafhopper was influenced by
three transitions in its host plant genus: life history, domestication, and breeding. Our overall hypothesis was that
corn leafhopper performance would be best on host plants
1431
25
20
15
10
5
0
0.4
Male adult mass (mg)
A
P = 0.001, F = 5.98, df = 4, 35
Nymph-adult survivorship
30
1.0
P = 0.006, F = 4.41, df = 4, 31
B
P < 0.0001, F = 10.49, df = 4, 34
D
0.8
0.6
0.4
0.2
0.0
P < 0.0001, F = 10.49, df = 4, 34
0.4
C
Male adult mass (mg)
Nymph-adult development time (days)
Oecologia (2013) 173:1425–1437
0.3
0.2
0.1
0.0
0.3
0.2
0.1
0.0
35 P = 0.0003, F = 7.32, df = 4, 29
(F0 eggs, P = 0.023, F = 5.74, df = 1, 29)
30
E
ren
Pe
l
nia
s 1 sas 2 drace
l
lsa
Ba
Ba
Lan
brid
Hy
Eggs laid
25
20
15
10
5
0
l
n ia
ren
Pe
s
lsa
Ba
1
ls
Ba
2
ce
as
dr a
Lan
brid
Hy
Fig. 3 Means (±SE) of individual performance variables of corn
leafhopper (D. maidis) on five Zea host plants, perennial teosinte
(Z. diploperennis; Perennial), Balsas teosinte (Z. mays parviglumis;
Balsas 1, Balsas 2), and maize (Z. mays mays; Landrace, Hybrid):
nymph to adult development time (days) (a), survival (proportion)
(b), adult size (mass in mg) of males (c) and females (d), and fecundity of F1 females (eggs laid during 48-h period) (e). ANOVA statis-
tics are inset, except in e where analysis of covariance parameters are
shown. The general trend is for corn leafhopper survivorship to adult,
adult size, and fecundity to increase from perennial teosinte to hybrid
maize, and development time to adult to decrease. The fecundity of
F0 females, egg eclosion rate, and egg to nymph development time
did not vary among the host plants (P ≥ 0.43; see text), so are not
shown
artificially selected for high productivity over herbivore
defenses, such as the maizes, and poorest on hosts naturally
selected for herbivore defense as a means of maximizing
productivity, such as the teosintes. Thus, corn leafhopper
performance was expected to be better on Balsas teosinte
than on perennial teosinte, on landrace maize than on Balsas teosinte, and on hybrid maize than on landrace maize.
The estimated F-values for each transition, which under
equality in df are indicative of effect size, suggested that
the corn leafhopper performance improved the most with
the breeding transition (F7,29 = 5.03), followed by the life
history (F7,29 = 3.94) and domestication (F7,29 = 3.15)
transitions.
The effects of Zea life history transition, from a perennial to an annual life cycle, on corn leafhopper performance
were evaluated by contrasting perennial teosinte with the
annual Balsas teosinte. Performance was better on Balsas
teosinte compared to perennial teosinte, consistent with
our prediction. Furthermore, while multivariate analyses
showed that corn leafhopper performance was influenced
by all three transitions, subsequent univariate analyses
showed that more performance variables were affected by
13
Oecologia (2013) 173:1425–1437
25
A
B
24
0.4
23
22
21
P = 0.0005,
t = 3.82, df = 21
P = 0.0001,
t = 4.50, df = 18
0.5
C
D
30
25
20
0.4
15
P < 0.0001,
t = 4.74, df = 20
10
0.3
P = 0.0001,
t = 4.50, df = 17
5
0
Perennial
Annual
Fig. 4 Corn leafhopper (D. maidis) performance improved with
the transition in its host plant’s life cycle from perennial to annual
largely because its development time to adult was shortened (a),
while the adult sizes of females (b) and males (c) and the fecundity
Perennial
Annual
of F1 females (d) increased on Balsas teosinte (Z. mays parviglumis;
Annual) compared to perennial teosinte (Z. diploperennis; Perennial).
Inset statistics correspond to a priori contrasts. See Fig. 1 for comparison of overall performances on those host plants
0.70
0.9
0.8
0.7
P = 0.016,
t = 2.54, df = 19
0.6
Female adult mass (mg)
1.0
Nymph-adult survivorship
0.3
0.2
20
0.2
0.65
0.60
0.55
0.50
Wild
Domesticated
Fig. 5 Corn leafhopper (D. maidis) performance improved with the
transition in domestication from wild annual host (Z. mays parviglumis) to a domesticated annual host (Z. mays mays) largely because
the survivorship to adult increased between the wild annual (Wild)
and domesticated annual (Domesticated). Inset statistics correspond
to a priori contrast. See Fig. 1 for comparison of overall performances
on these host plants
the life history transition compared to the other transitions.
Perennial and annual plants are expected to have different metabolic resource allocation strategies, particularly in
that annual species may be selected to maximize present
reproduction, thus partially sacrificing defense, because
future reproduction is foregone (Bazzaz et al. 1987). Perennial teosinte is an iteroparous, rhizomatous grass that
P = 0.0003,
t = 4.12, df = 14
0.45
0.40
0.5
13
0.5
Eggs laid
Male adult mass (mg)
26
Female adult mass (mg)
Nymph-adult development (days)
1432
Landrace
Hybrid
Fig. 6 Corn leafhopper (D. maidis) performance improved with the
transition in maize (Z. mays mays) from genetically diverse landrace
to genetically narrow hybrid largely because the adult size of females
increased between the landrace (Landrace) and hybrid (Hybrid)
maize. Inset statistics correspond to a priori contrast. See Fig. 1 for
comparison of overall performances on these host plants
propagates clonally (Masarovicova et al. 2000; SánchezVelásquez et al. 2001). Balsas teosinte is an annual grass
that completes its entire life cycle within a single growing season, having only one opportunity to reproduce,
and allocating more of its resources to reproduction, via
seed, compared to perennial teosinte (Rosenthal and Dirzo
1997; Mondragón-Pichardo and Vibrams 2005). The different resource-allocation strategies corresponding to the
1433
Oecologia (2013) 173:1425–1437
Table 1 The fecundity of Dalbulus maidis females (F1) relative to the fecundity of their female parents (F0) was influenced by the Zea host that
was colonized by the parent (critical P per Bonferroni correction is 0.01)
Ratio offspring to parent fecundity
P (F0 fecundity − F1 fecundity = 0)
Perennial teosintea
2.8/26.1
0.11
<0.01 (t = −5.08, df = 7)
Balsas teosinte 1b
26.6/29.5
0.90
0.73 (t = −0.36, df = 7)
Balsas teosinte 2b
20.7/26.1
0.79
0.34 (t = −1.04, df = 6)
Landrace maize
17.8/33.5
0.53
0.05 (t = −2.33, df = 9)
Hybrid maizec
25.0/31.0
0.81
0.23 (t = −1.34, df = 6)
c
Fecundity was measured as the number of eggs laid per female over a 48-h period
a
Zea diploperennis
b
Zea mays parviglumis
c
Zea mays mays
two life histories should affect how the plants interact with
their environments, including insect herbivores. Consistent
with the expectation of differing metabolic resource allocation strategies between perennial and annual plants, a
prior study showed that in the field perennial teosinte grew
slower and produced fewer seeds than Balsas teosinte, but
suffered similar to less injury by non-specialized stemboring and folivorous insects (Rosenthal and Dirzo 1997).
Compared to our results, the results of Rosenthal and
Dirzo (1997) less clearly implied stronger plant defenses
in perennial teosinte compared to Balsas teosinte. However, they used injury by non-specialist insects as a proxy
for plant defense, so their results may reflect partial adaptation to both host plants in the insects, and did not separate defense from tolerance responses in the host plants.
Moreover, the results of an earlier study implied weaker
indirect defense (lower induced-volatile production)
against a generalist herbivore in perennial teosinte than in
Balsas teosinte (Gouinguene et al. 2001). The dissimilarity of plant defense responses among these studies may
reflect differential responses to specialist vs. generalist herbivores among plants, and trade-offs between corresponding defense strategies, such as between direct and indirect
defenses and herbivory tolerance (e.g., regrowth ability)
(van der Meijden 1996; Lankau 2007; Agrawal and Fisbein Agrawal and Fisbein 2008). For example, Agrawal and
Fishbein (2008) found that direct defense against specialist herbivores (measured as cardenolide content) declined,
while tolerance (regrowth ability) escalated with phylogeny in Asclepias, so that the basal species of the genus presented stronger direct defense and lower regrowth ability
compared to distal species.
The effects of the domestication transition on corn leafhopper performance were evaluated by comparing between
Balsas teosinte and Tuxpeño landrace maize. Our results
showed a significant effect of the domestication transition on overall performance, though further analyses
showed that only nymph to adult survivorship improved
significantly with the transition. Based on the resource
allocation hypothesis, compared to Balsas teosinte, landrace maize should allocate less of its metabolic resources
to herbivore defense because it allocates more resources
to productivity. Moreover, domestication and subsequent
improvement of maize, and crops generally, implied
selection for greater productivity and increased reliance
on human cultivation, including reliance for overcoming
biotic and abiotic stressors, such as herbivores, pathogens,
and drought. Thus, landrace maize was shown to produce
more biomass and suffer less herbivore injury than Balsas
teosinte in a prior study (Rosenthal and Dirzo 1997). However, similar to our results that same study showed weak to
nonexistent differences in insect injury, though the injury
measured was by non-specialist insects, as noted above.
The slight performance difference we found may reflect a
strong similarity in plant defenses between maize and its
progenitor Balsas teosinte. Although morphological, phenological and other differences are very marked between
the two host plants, maize retains very high levels of its
progenitor’s genetic diversity, and shows low genetic differentiation from it, compared to other crops, and the two
taxa easily cross-fertilize and form fully fertile F1 hybrids
in the field (Doebley 2004; Buckler and Stevens 2005; Vigouroux et al. 2005; Heerwaarden et al. 2011; Hufford et al.
2012). Moreover, a recent study found evidence of recovery
of genetic diversity in landraces following domestication
(Hufford et al. 2012). Thus, the plant defenses of Balsas
teosinte and landrace maize may be very similar, and their
defense against a specialist herbivore such as corn leafhopper may be a complex trait, i.e., dependent on multiple
traits or processes, each with a small effect on individual
performance variables, and consequently each with low statistical significance, as suggested by the univariate ANOVA
results. This is consistent with the expectation that broad
defenses (e.g., digestibility reducers, physical defenses)
are directed against specialist herbivores, and specific
defenses (e.g., toxins) against generalists. Additionally,
13
1434
the negative effect on nymph to adult survivorship indicates that defenses are acting on corn leafhopper’s nymphal
stage, including physical defenses, such as leaf toughness.
A recent study suggested that Balsas teosinte may be more
resistant to mouthpart penetration than landrace maize
(Bellota-Villafuerte 2012), which may affect food uptake in
nymphs and their development into adults.
We evaluated the effects of the breeding transition on
corn leafhopper performance by contrasting the landrace
maize against the hybrid maize. Our results were consistent with the prediction that corn leafhopper would perform
better on hybrid maize than on landrace maize. Differences
in genetic variability of the two maize cultivars may have
strongly mediated the relatively large effect of the breeding
transition. While maize landraces generally contain much
of the genetic diversity of Balsas teosinte, and Tuxpeño is
among the most genetically diverse of Mexican landraces,
commercial maize hybrids are among the least genetically
diverse Mexican maize cultivars (Sánchez-González 2011;
Hufford et al. 2012). Additionally, modern maize breeding has focused largely on increased productivity, particularly seed yield and quality (Whitt et al. 2002; Buckler and
Stevens 2005; Hufford et al. 2007; Tian et al. 2009), which
may have resulted in weaker herbivore defenses per the
resource allocation hypothesis (Herms and Mattson 1992;
Mole 1994; Obeso 2002). However, our results also showed
that the difference in overall performance was mediated
largely by a single performance variable, adult female size,
which increased significantly with the transition from landrace to hybrid maize. This result reinforces our suggestion (above) that maize defense against corn leafhopper is
a complex trait, depending on a variety of defenses, each
with a small effect on the insect’s performance. Crop breeding for greater productivity has been shown to affect herbivore performance, or crop performance vis-à-vis herbivory,
in other studies. For example, one study found greater
insect [Callosobruchus maculatus (F.)] oviposition and
survivorship and lower germination rate of insect-infested
seeds in groundnut (Vigna subterranea L. Verdc.) breeding
lines compared to landraces (Magagula and Maina 2012).
Rodríguez-Saona et al. (2011) found that the performance
of L. dispar was better on a high-yielding, American cranberry cultivar compared to ancestral cultivars, and that
defensive chemistry was reduced in the high-yielding cultivar, as noted above. Similarly, other studies showed differences in defensive chemistry among maize cultivars,
including maize landraces and modern, high-yielding cultivars (Rasmann et al. 2005; Tamiru et al. 2011). To date,
no study has tested corn leafhopper performance on a range
of maize cultivars, though performance differences were
suggested in a study that showed differences in the insect’s
abundance between fields consisting of different maize
genotypes (Power 1988).
13
Oecologia (2013) 173:1425–1437
The fecundity of F1 offspring (F1 fecundity) suffered
significantly only for forced colonization of perennial
teosinte. This result is consistent with observations indicating that plant defenses are generally stronger in wild
crop relatives compared to the corresponding crop species. However, this result is also consistent with observations indicating that corn leafhopper comprises at least two
subpopulations, one associated with perennial teosinte and
another with maize (and Balsas teosinte) (Medina et al.
2012; Dávila-Flores 2012). In this study, we forced females
of the “maize subpopulation” to colonize perennial teosinte
and found that within a single generation their (F1) female
offspring suffered a ca. 90 % fecundity loss, and produced
~3 % of the eggs that were produced overall by F1 females
on the annual Zea (Balsas teosintes and maizes). This loss
of fecundity could be a mechanism, i.e., immigrant inviability, maintaining in part the existence of two corn leafhopper subpopulations associated with different hosts.
Overall, the corn leafhopper performance variables associated with the (F0) founding generation (F0 fecundity, egg
development time, egg survival) were not affected by the
transitions nor by the host plants. This is consistent with
the results of Bellota-Villafuerte (2012) where, in a nochoice context, females equally oviposited on specimens
of the same set of host plants evaluated in this study. In
contrast, other studies have shown defensive responses
targeting herbivore eggs, including strong ovicidal effects,
through production of defensive metabolites, in rice (Oryza
sativa L.) cultivars resistant to a non-specialist leafhopper
(Sogatella furcifera Horvath) (Seino et al. 1996; Suzuki
et al. 1996; Hilker and Meiners 2011). This suggests that
defense against corn leafhopper involved antibiosis of
nymphs and perhaps adults, and that antixenosis (repellency or non-preference) targeting adults and any defenses
targeting eggs are either not relevant or are weak.
Physical defenses such as pubescence and leaf toughness can affect herbivore performance (Jindal and Dhaliwal 2011; Bellota-Villafuerte 2012). For example, BellotaVillafuerte (2012) assessed whether two putative physical
defenses, leaf pubescence and toughness, and corn leafhopper host preference were affected by life history, domestication, and breeding transitions in Zea, as evaluated in
this study. His results for leaf toughness and host preference, but not pubescence, were consistent with the pattern
of stronger defenses in wild vs. domesticated Zea found in
this study. Thus, the differences in corn leafhopper performance we found in this study may be due in part to differences in leaf toughness among the host plants.
Overall, our findings agreed with those of previous studies suggesting that plant defenses are stronger in perennial than annual plants, in crop ancestors than crops, and
in landraces than modern varieties (e.g., Rosenthal and
Dirzo 1997; Benrey et al. 1998; Rodríguez-Saona et al.
Oecologia (2013) 173:1425–1437
2011; Szczepaniec et al. 2012; Takahashi et al. 2012). A
prior study with a similar set of host plants clearly showed
that plant productivity increases from perennial Zea to
hybrid maize, and that plant injury by non-specialist (oligophagous) herbivores is positively correlated with plant
productivity (Rosenthal and Dirzo 1997). In parallel, our
findings are consistent also with a phylogenetic decline of
direct defenses directed at corn leafhopper, a specialist herbivore (Agrawal and Fishbein 2008; Agrawal et al. 2009a,
b), though: (1) we did not address whether there is a corresponding escalation in other defensive strategies (e.g.,
tolerance); and (2) human selection and breeding in the
landrace and hybrid maizes may override any phylogenetic
trends. So, in general, weaker herbivore defense appears to
be correlated with greater productivity in Zea, a trend that
overlaps with the phylogeny of Zea, from basal, wild perennial taxa, to wild annuals, to a recent domesticated taxon,
which spans from landrace to modern, hybrid cultivars.
However, several questions remain unanswered concerning plant defenses against corn leafhopper and the apparent trade-off between productivity and defense in Zea. For
example, in this study we did not elucidate the identity nor
nature of plant defenses against corn leafhopper, whether
physical or chemical, nor whether and how strongly nutritional differences among the host plants may have affected
corn leafhopper’s performance. Additionally, a direct test of
the defense-productivity trade-off is desirable, particularly
under common garden conditions, and in both “natural”
and agricultural environments, because the former environment may favor the teosintes, while the latter environment may favor the maizes. Finally, future studies should
examine whether our results are independent of population
genetic structuring in corn leafhopper in light of the known
existence of corn leafhopper subpopulations specializing
on perennial teosinte or maize (Medina et al. 2012).
Acknowledgments We are grateful to Dr Ramón Cuevas and Francisco Santana Michel (both at Universidad de Guadalajara, Autlán
campus, Mexico) for facilitating collection of perennial and Balsas
teosinte seed, respectively, Dr Mark Millard (USDA NPGS, Ames,
IA) for providing Tuxpeño landrace seed, and Dr Raul Medina (Texas
A&M University, College Station) for critical review of an early version of the manuscript. This project was supported in part by National
Science Foundation (NSF-DEB 0818240) and Hatch (TEX07234)
funds to J. S. B, and CONACyT-TAMU Visiting Student Researcher
Program funds to A. M. D.-F.
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