![Network related to the negative influence between host oak [genetic diversity (He), secondary metabolites (rutin, caffeic acid, quercetin glucoside, quercitrin, kaempferol glucoside, scopoletin)] and the richness (S) and abundance of canopy gall-inducing wasps and their parasitoids. Nv = normalized value (from 0 to 1), where (1) in the range [0.0-0.22], the influence is very low; (2) in the range [0.22-0.44], the influence is low; (3) in the range [0.44-0.66], there is a medium influence; (4) in the range [0.66-0.88], the influence is high; and (5) in the range [0.88-1], the influence is very high.](https://www.researchgate.net/publication/388136030/figure/fig2/AS:11431281304205608@1737194962382/Network-related-to-the-negative-influence-between-host-oak-genetic-diversity-He_Q320.jpg)
Available via license: CC BY 4.0
Content may be subject to copyright.
Academic Editor: Luc Legal
Received: 19 November 2024
Revised: 13 January 2025
Accepted: 13 January 2025
Published: 17 January 2025
Citation: Castillo-Mendoza, E.;
Valencia-Cuevas, L.; Mussali-Galante,
P.; Ramos-Quintana, F.; Zamilpa, A.;
Serrano-Muñoz, M.; Pujade-Villar, J.;
Tovar-Sánchez, E. White Oaks Genetic
and Chemical Diversity Affect the
Community Structure of Canopy
Insects Belonging to Two Trophic
Levels. Diversity 2025,17, 62.
https://doi.org/10.3390/d17010062
Copyright: © 2025 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license
(https://creativecommons.org/
licenses/by/4.0/).
Article
White Oaks Genetic and Chemical Diversity Affect the
Community Structure of Canopy Insects Belonging to Two
Trophic Levels
Elgar Castillo-Mendoza 1, Leticia Valencia-Cuevas 2, Patricia Mussali-Galante 3, Fernando Ramos-Quintana 1,
Alejandro Zamilpa 4, Miriam Serrano-Muñoz 5, Juli Pujade-Villar 6and Efraín Tovar-Sánchez 1, *
1Centro de Investigación en Biodiversidad y Conservación, Universidad Autónoma del Estado de Morelos,
Cuernavaca 62209, Morelos, Mexico; elgar.castillo@hotmail.com (E.C.-M.);
ramosfernando747@gmail.com (F.R.-Q.)
2Escuela de Estudios Superiores del Jicarero, Universidad Autónoma del Estado de Morelos,
Carretera Galeana-Tequesquitengo s/n, Comunidad El Jicarero, Jojutla 62915, Morelos, Mexico;
leti70477@yahoo.com.mx
3Laboratorio de Investigaciones Ambientales, Centro de Investigación en Biotecnología, Universidad
Autónoma del Estado de Morelos, Cuernavaca 62209, Morelos, Mexico; patricia.mussali@uaem.mx
4Centro de Investigación Biomédica del Sur (CIBIS-IMSS), Xochitepec 62790, Morelos, Mexico;
azamilpa_2000@yahoo.com.mx
5Laboratorio de Sanidad Forestal de PROBOSQUE, Rancho Guadalupe S/N, Conjunto SEDAGRO,
Metepec 52140, Estado de México, Mexico; mirserrano7@gmail.com
6
Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals (Secció invertebrats), Facultat de Biología,
Universitat de Barcelona, 08028 Barcelona, Cataluña, Spain; jpujade@ub.edu
*Correspondence: efrain_tovar@uaem.mx
Abstract: The hybridization phenomenon increases genetic diversity and modifies recom-
binant individuals’ secondary metabolite (SMs) content, affecting the canopy-dependent
community. Hybridization events occur when Quercus rugosa and Q. glabrescens oaks con-
verge in sympatry. Here, we analyzed the effect of the genetic diversity (He) and SMs of Q.
rugosa,Q. glabrescens and hybrids on the community of gall-inducing wasps (Cynipidae)
and their parasitoids on 100 oak canopy trees in two allopatric and two hybrid zones.
Eighteen gall wasp species belonging to six genera and six parasitoid genera contained
in four families were identified. The most representative parasitoid genera belonged to
the Chalcidoidea family. Abundance, infestation levels and richness of gall wasps and
their parasitoids registered the next pattern: Q. rugosa higher than the hybrids, and the
hybrids equal to Q. glabrescens. Oak host genetic diversity was the variable with the highest
influence on the quantitative SMs expression, richness and abundance of gall wasps and
their parasitoids. The influence of SMs on gall wasps and their parasitoids showed the next
pattern: scopoletin > quercitrin > rutin = caffeic acid = quercetin glucoside. Our findings
indicate that genetic diversity may be a key factor influencing the dynamics of tri-trophic
interactions that involve oaks.
Keywords: secondary metabolites; hybridization; white oaks; tri-trophic interactions
1. Introduction
For decades, we have known that variation in plant populations’ structure and ge-
netic diversity leads to changes in their associated arthropod communities. Herbivorous
arthropods can distinguish between different plant species [
1
] and their hybrids [
2
], as
well as between different plant genotypes within a single species [
3
]. Also, genetic varia-
tion in plants affects herbivores and can extend to higher trophic levels among different
Diversity 2025,17, 62 https://doi.org/10.3390/d17010062
Diversity 2025,17, 62 2 of 25
plant species [
4
], among putative plant species and their hybrids [
5
] and among plant
genotypes [
6
]. Consequently, this discrimination between plants can influence arthropod
diversity and community structure [
7
]. Also, some studies have shown that increasing
genetic diversity within interbreeding plant systems (e.g., hybrids and single plant species)
increases arthropod diversity and community structure [
8
,
9
]. Plant genetics play an impor-
tant role in SMs production and plant architecture [
10
–
13
]. These differences impact the
availability, quality and quantity of resources for herbivores, influencing their performance,
population density, community structure and evolutionary patterns [
14
–
16
]. Furthermore,
the effects of plant variation on herbivorous arthropods extends to higher trophic lev-
els, resulting in changes in the composition, abundance and diversity of predators and
parasitoids among different plant species and between parental plant species and their
hybrids [
17
]. However, rarely have chemical traits in plant species been correlated with
plant genetics and arthropod community structure [18,19].
Oaks (Fagaceae: Quercus) are considered the most abundant woody plant group in
the Northern Hemisphere [
20
], with an estimated 500 species worldwide [
21
]. Mexico is
home to 30.3% of oak species and is considered one of the most important diversification
centers of the genus [
22
]. Oaks are important for the ecological functions they perform
(e.g., soil fertilization, nutrient cycling and water balance) [
23
]. Oaks dominate the canopy
of forest ecosystems and have an extensive and complex network of interactions with
other organisms, such as epiphytic plants, mammals, birds, fungi and arthropods [
24
]. In
particular, oak distribution, abundance and species richness have significantly influenced
the distribution and species richness of oak gall wasps [8].
One of the characteristics of the genus Quercus is the high frequency of hybridization
and introgression events between species belonging to the same section [
25
]. Hybridization
is a form of genetic exchange, and several studies on oaks have documented that the
increased genetic diversity of the species involved [
26
,
27
] promotes variation in morpho-
logical, chemical and phenological characteristics, among others [
28
–
30
], with important
consequences at the community structure level [
31
,
32
]. For example, arthropods respond
to certain characteristics of their host plant species, such as biomass, foliar nutritional
quality and SMs, attributes that have a genetic basis [
33
]. These characteristics may influ-
ence the oviposition and feeding preferences of the arthropods associated with oaks and,
consequently, their distribution and abundance [34].
Secondary metabolites are chemical compounds derived from the primary metabolism
but not related to the normal development and/or growth of plants [
35
]. The hybridization
process modifies the metabolic pathways of interacting species, creating differences in
SMs expression (type, concentration and quality) [
36
]. Secondary metabolite expression
in hybrid plants can vary qualitatively and quantitatively [
37
]. Qualitatively, hybrids can
express all or some of the SMs found in parental taxa or even new SMs. Quantitatively, the
concentration of SMs can be higher, intermediate, lower or similar to the concentration in
one or both parental taxa [
38
,
39
]. These compounds are associated with plant survival and
adaptability [40], and in most cases, SMs are involved in defense against herbivory [41].
Studies of the genus Quercus have reported that hybridization induces variation in the
qualitative and quantitative expression of SMs [
42
,
43
]. In general, the most frequently reported
SMs in oak leaves are flavonoids, terpenoids, tannins and aliphatic
compounds [43,44]
, which
can act as insect attractants, feeding inhibitors, regulators of the respiratory chain (terpenoids–
tannins), cytotoxins and regulators of larval development (flavonoids). These compounds are
associated with generalist and some specialist herbivores [45].
The endophagous, gall-inducing wasps belonging to the Cynipidae family (Hy-
menoptera: Cynipidae: Cynipini Tribe) associated with the genus Quercus are considered
one of the most specialized groups of herbivorous insects [
46
]. It has been proposed that
Diversity 2025,17, 62 3 of 25
cynipids can detect small physiological, chemical or phenological changes in their host
oaks, which allow them to “select” oviposition and/or feeding sites [
47
,
48
]. The galls
induced by cynipids form a tri-trophic system with great ecological activity [
49
], harboring
a closely associated community of guest organisms and parasitoids, particularly from the
Chalcidoidea family [
48
]. The parasitoids associated with cynipids are specific to them;
it has been reported that their communities may be affected by the genetic attributes or
chemical defense mechanisms of plants [
9
,
50
]. Therefore, oaks and their associated gall
insects and parasitoids represent an excellent system to study the effect of the genetic and
chemical variations that result from hybridization events on cynipid communities and their
associated parasitoids.
The identification of hybrid individuals is crucial in studies related to hybridization.
Hence, different markers have traditionally been employed, emphasizing genetic and chemical
markers (SMs) [
43
,
51
–
53
]. Given that DNA-based markers depend on genotypic data, they are
viewed as the most effective markers for identifying hybrids, highlighting Simple Sequence
Repeats (SSRs; [
33
]), which can effectively differentiate the heterozygous condition and are
clearly favored over dominant markers. Regarding SMs and due to their oligogenic control,
they have a much more predictable inheritance compared to morphological traits, which are
generally influenced by polygenic control and the emergence of transgressive characters [
54
].
Consequently, several researchers have utilized SMs alongside genetic markers to detect
hybrid individuals within natural populations. Finally, hybrids’ SMs play a crucial role,
possibly contributing to the success of hybrid populations by expressing unique combinations
of SMs that enhance their defense against herbivores [54].
A previous study reported genetic (microsatellite) and chemical (flavonoid) evidence of
hybridization in a white oak complex formed by Q. glabrescens and Q. rugosa [43]. The authors
detected specific chemical markers for each parental species and a complementary pattern of the
qualitative expression in hybrids, that is, the presence of flavonoids from the parental species.
The aim of this study was to evaluate the effect of the genetic diversity and SMs of a
Q. glabrescens
×
Q. rugosa complex on their associated community structure of gall-inducing
wasps and parasitoids. The following questions were posed: (1) Do hybridization events
between Q. glabrescens and Q. rugosa promote quantitative differences in the pattern of
flavonoid and coumarin expression in their hybrids? (2) Is there a relationship between
the genetic diversity and SMs variation in the Q. glabrescens
×
Q. rugosa complex and the
associated community of gall-inducing insects (Cynipidae) (3) What is the level of influence
of genetic diversity and SMs on the community of gall-inducing wasps? (4) Do the genetic
and chemical attributes of the host oak affect the community of parasitoids associated with
gall-inducing wasps?
2. Materials and Methods
2.1. Study Species
Quercus glabrescens Benth. and Q. rugosa Née are abundant species in the four study
sites. Q. glabrescens includes large trees of up to 20 m in height, with a trunk diameter of
1 m. Q. rugosa includes large trees of up to 25 m in height, with a trunk diameter of 1 m.
Both species show a wide geographical distribution in Mexican mountains and canopy
dominance [
43
]. In a previous study, Castillo-Mendoza and collaborators [
43
] documented
hybridization between both Quercus species in sympatric zones.
2.2. Study Sites and Population Sampling
The oak trees sampled in the present study correspond to the populations previously
identified morphologically and genetically by Castillo-Mendoza et al. [
43
]. Specifically, we
used the two sympatric sites between Q. glabrescens and Q. rugosa and the allopatric popula-
Diversity 2025,17, 62 4 of 25
tions of these species. In total, 100 individuals belonging to four populations (two allopatric
[20 trees/site, one for each parental species] and two sympatric sites
[30 trees/site])
were
analyzed (Table 1). We selected this sample size considering that previous studies have
used similar sample sizes and found significant and robust results [
8
,
9
,
18
]. To minimize
the influence of environmental and spatial variables on gall-inducing wasps and their
parasitoid communities, all study sites shared the following characteristics: geological
history (all localities belonged to the central part of Mexico, originating during the Pliocene–
Quaternary [
55
]), weather (sub-humid temperate [
56
]), altitude (between 2318 and 2667 m),
vegetation type (mature oak) and soil type (volcanic origin: histosol [
57
]). Also, all sampled
individuals were mature trees without apparent damage by other herbivores.
Table 1. Locality name, state, altitude, geographic coordinates and sample size for the collecting sites
of Q. glabrescens ×Q. rugosa in Central Mexico.
Location N State Altitude
(m)
Coordinates
(N–W) Taxa
Allopatric stand
Tlaxco 20 Tlaxcala 2588 19◦41′44.7′′–98◦4′49.1′ ′ Q. glabrescens
Coajomulco 20 Morelos 2667 19◦2′3.5′′ –99◦11′54.1′′ Q. rugosa
Sympatric stand
Huitzilac 30 Morelos 2318 19◦1′57′′ –99◦16′34′′ Q. glabrescens,Q. rugosa, hybrid
Omitlán de Juárez 30 Hidalgo 2522 20◦9′57′′ –98◦39′16′′ Q. glabrescens,Q. rugosa, hybrid
2.3. Molecular Data
In a previous study, we found that molecular markers (microsatellites, SSRs)
supported the hybridization hypothesis between Q. rugosa and Q. glabrescens [
43
].
The genetic diversity analyses were performed with eight nuclear SSR primers: ss-
rQpZAG110 [
58
], ssrQpZAG11, ssrQrZag56 [
59
], Quru-GA-0A01, Quru-GA0E09, Quru-
GA-0C11, Quru-GA-1C08 and Quru-GA-1F07 [
60
]. All these nSSRs showed polymor-
phisms among the individual trees of the Q. glabrescens
×
Q. rugosa complex. For more
technical details, see Castillo-Mendoza et al. [43].
2.4. Chemical Data
In an earlier study, we identified nine flavonoids and one coumarin of the
Q. glabrescens
×
Q. rugosa complex [
43
]. In total, 48 individuals [Q. glabrescens
(n= 18), Q. rugosa (n= 18), hybrids (n= 12)] were quantitatively analyzed using the
same extracts obtained by Castillo-Mendoza et al. [
43
]. Column chromatography was
employed to purify the extracts, and we obtained 10 mg of pure compound per popula-
tion. Due to their high heritability and specificity, flavonoids have been the most studied
compounds [
13
] and are used as chemical markers to diagnose plant hybridization [
30
].
HPLC was employed to determine flavonoid concentrations through calibration curves,
which are generated by known commercial standards for each compound (the caffeic acid,
kaempferol glucoside, quercetin, quercitrin, rutin and scopoletin present in Q. rugosa, hybrids,
and Q. glabrescens ([see Appendix A] [Sigma-Aldrich Chemical Co., St. Louis, MO, EUA]).
Chemical separation was carried out in a reversed-phase column supelcosil (rp-18, 25 cm,
4 um) under a gradient TFA/acetonitrile (flow = 0–9 mil/min; vol. 10
µ
L, wavelength
350 nm
).
Afterward, the area of each known standard was determined, and a graph correlating to the
area of the peak, with its mass, was created. Finally, the SMs concentration was calculated as
the mean ±standard error (µg/mL−1) on a dry weight (DW) basis.
By measuring the peak areas, the calibration curves were linear (r
2
> 0.998), in the
concentration range of 12.5 to 200 ng. Six control standards containing 12.5, 25, 50, 100
Diversity 2025,17, 62 5 of 25
and 200
µ
g/mL
−1
in triplicate were used (10
µ
L injection each) to ensure accuracy and
precision, where RSD (%) values were within 2% of the actual concentrations (Table 2). This
confirmed the precision and validation of the method. The method has the advantage of
using a simple gradient elution in the reverse phase without adding buffers.
Table 2. Regression analysis, limits of detection and limits of quantification for the six analytes of
the assay.
Secondary Metabolite Detection Limits (nm) Regression
Equation r2Linear Range
(µg/mL−1)
LOD
(
µ
g/mL
−1
)
LOQ
(
µ
g/mL
−1
)
quercetin-3-O-rutinoside (rutin) 312 Y= 17,931 X−99,324
0.9996
12.5–200 12.33 37.38
quercetin-3-O-glucoside (quercetin) 312 Y= 22,019 X−219,819
0.9955
12.5–200 10.78 32.67
caffeic acid 312 Y= 24,759 X−91,894
0.9991
12.5–200 4.10 12.45
scopoletin 330 Y= 25,131 X+ 66,600
0.9991
12.5–200 8.85 17.74
kaempferol-3-O-glucoside
(kaempferol glucoside) 312 Y= 11,149 X+ 17,786
0.9980
12.5–200 7.91 23.99
quercetin-3-O-rhamnoside (quercitrin)
312 Y= 7837 X+ 4622
0.9996
12.5–200 4.49 13.61
Y= the peak area in UV chromatograms monitored at 312 nm, X= compound concentration injected,
r2= determination coefficient, LOD = limits of detection, LOQ = limits of quantification.
For this study, we identified two new metabolites using the same chemical
methodology and individuals employed previously by Castillo-Mendoza et al. [
43
]
(Table 2; Appendix A). Also, we determined the concentration of four SMs [caffeic acid,
quercetin-3-O-glucoside (=quercetin), quercetin-3-O-rutinoside (=rutin), quercetin-
3-O-rhamnoside (=quercitrin)] identified previously by Castillo-Mendoza et al. [
43
]
and two new SMs characterized in the present study [(kaempferol-3-O-glucoside
(=kaempferol glucoside) and scopoletin]. Finally, flavonols 1-5 and the alkyl coumarate
were not quantitatively analyzed, because it was not possible to determine their spe-
cific identification (see Table 2in Castillo-Mendoza et al. [
43
]). From now, we will use
the simple nomenclature for each compound (Appendix A).
Also, for statistical analysis, the values below the detection limit of the HPLC were
assigned as half of this limit [61].
2.5. Canopy Gall-Inducing Wasp Communities and Associated Parasitoids
The gall-inducing wasp and parasitoid community structure associated with Q. rugosa
(n= 40) and Q. glabrescens (n= 40), including their hybrids (n= 20), was analyzed in
the same 100 individuals as in Castillo-Mendoza et al. [
43
]. We selected oak individuals
between 10.0 and 13.4 m (mean
±
standard error) (Q. rugosa: 10.59
±
0.11, Q. glabrescens:
11.58
±
0.13, hybrid: 10.89
±
0.09) in height and with 10.2–13.2 m
2
(Q. rugosa: 14.95
±
0.35,
Q. glabrescens: 13.02
±
0.37, hybrid: 11.83
±
0.65) of crown cover. Oak gall-inducing wasps
and parasitoid were sampled in April and December 2016. The infestation by gall-inducing
wasps associated with each host tree was estimated using four randomly selected branches
and 200 leaves (50 leaves per branch) in the middle part of the canopy. For each insect
species, an average infestation value was estimated (number of galls/200 leaves
×
100) over
the four branches. Galls collected in each host tree were separated into the morphospecies
level, placed in previously vouchered plastic containers and transported to the labora-
tory where the insects emerged. Wasps were identified to the finest possible taxonomic
level [62–74], and their parasitoids were identified at the genus level [75–78].
2.6. Statistical Analysis
2.6.1. Genetic Diversity of Host Plant
To estimate the influence of the Q. rugosa,Q. glabrescens and hybrids’ genetic diversity
on SMs, canopy gall-inducing insects and their parasitoids, the expected heterozygosis
(He: the probability that two alleles taken at random from the population are different) was
Diversity 2025,17, 62 6 of 25
used to analyze the genetic diversity at the population level. The genetic analyses were
performed with the same eight nSSR primers reported by Castillo-Mendoza et al. [43]. He
was used because it is frequently employed to evaluate the influence of population genetic
diversity on the community structure [
8
,
9
,
79
]. The software used for the mean expected
heterozygosity (He) was Popgene v. 1.31 [
80
]. Thereafter, a Kruskal–Wallis analysis of
variance was conducted to determine significant differences in genetic diversity values
among populations [81].
2.6.2. Community Structure of Canopy Gall-Inducing Insects and Associated Parasitoids
An analysis of variance (ANOVA) was conducted ([Model III (orthogonal)] [
81
]) to
determine the effect of oak host taxa (Q. rugosa,Q. glabrescens, and hybrid: independent
variable) on species richness, abundance and infestation percentage of gall-inducing insects
and their associated parasitoids (dependent variables). Also, the Shannon–Wiener diversity
index (H’) was estimated to characterize species diversity in a community; subsequently,
the index (H’) was compared between pairs of taxa with a randomization test (delta,
δ
);
this test re-samples 10,000 times from a distribution of species abundances produced by
a summation of the two samples [
82
]. In order to satisfy parametric test assumptions,
percentage data were corrected as X= arcsin (%)½, and discontinuous data were trans-
formed as
X= (X) ½ + 0.5
[
81
]. A Tukey test was carried out to determine differences in
mean infestation (%), abundance and species richness between hybrid oaks and parental
species [
81
]. The software used for statistical analysis was STATISTICA 8.0 [
83
] and Species
Diversity and Richness version 3.03 [84].
2.7. Influence of Host Taxa, Genetic Diversity and Secondary Metabolites on Canopy Gall-Inducing
Insects and Associated Parasitoids
We used a multiple regression approach to examine whether the host taxa (Q. rugosa,
Q. glabrescens and hybrid) genetic diversity levels (He) and SMs (caffeic acid, quercetin
glucoside, rutin, quercitrin, scopoletin and kaempferol glucoside) influence the canopy
gall-inducing wasps and associated parasitoids. This analysis was helpful to determine the
relative contribution from each factor on the abundance and species richness variation of
gall-inducing wasps and their parasitoids. We used a standard least squares model with
a partial (type III sums of squares) error structure and genetic diversity and SMs as our
factors. We excluded variables with a non-significant correlation coefficient (p> 0.05) to
improve the analysis. Considering that He is a variable that contributed to SMs expression,
we were interested in determining whether the host He can predict the SMs. Therefore, we
used simple linear regressions.
The Shannon-Wiener diversity index (H’) vs. species richness (S) (r= 0.830, p< 0.01),
galls abundance vs. galls infestation levels (r= 0.957, p< 0.001) and parasitoids abundance
vs. parasitoids infestation levels (r= 0.597, p< 0.001) variables were correlated. To assess
the relationship between He and SMs, regression analyses were conducted only with Sand
the abundance of gall-inducing insects and their parasitoids variables. The software used
for statistical analysis was STATISTICA 8.0 [83].
We also built networks comprising pathways that facilitate the measurement of the
negative and positive influence of genetic diversity and SMs on the richness and abundance
of the gall inductor wasps and their parasitoids. We used the linear regression method to
quantify the causal relationship between dependent and independent variables. Specifically,
we used the slope value of the interpolated straight line derived from the linear regression
method to quantify the relationship trend either in an upward or a downward direction.
We used values between 0
◦
and 90
◦
, which are easier to interpret. We selected a sigmoid
function to model the behavior of the relationships, defining five zones that represent the
influence of the independent variable X on the dependent variable Y, which are described
Diversity 2025,17, 62 7 of 25
as follows: (1) in the range [0
◦
, 20
◦
], the influence of X on Y is very low; (2) in the range
the influence is low; (3) in the range [40
◦
, 60
◦
], there is a medium influence; (4) in the range
[60
◦
, 80
◦
], the influence is high; (5) in the range [80
◦
, 90
◦
], the influence is very high. It is
important to mention that the sigmoid function is also applicable to the case of negative
influences. For practical reasons, we transform the quantitative relationships between the
dependent and independent variables expressed by normalized values (Nv) between 0 to 1
into qualitative values represented by five zones through the sigmoid function depicted in
Figure 4. These five zones are described as follows: Zone 1 (range [0, 0.22]), the influence of
X in Y is very low; Zone 2 (range [0.22, 0.44]), the influence of X in Y is low; Zone 3 (range
[0.44, 0.66]), the influence of X in Y is medium; Zone 4 (range [0.66, 0.88]), the influence of
X in Y is high; Zone 5 (range [0.88, 1]), the influence of X in Y is very high. For more details,
see Appendix C).
3. Results
3.1. Genetic Diversity of the Three Oak Taxa Hosting Gall-Inducing Insects
Genetic analysis of the Q. rugosa
×
Q. glabrescens complex, using eight nuclear mi-
crosatellites, showed that He presented the following pattern: hybrid (0.669) > Q. rugosa
(0.637) > Q. glabrescens (0.447). The Kruskal–Wallis analysis of variance revealed signifi-
cant differences among these values, while the Tukey test showed that the highest values,
found in the hybrid taxa, differed statistically from both parental species (Table 3). These
genetic differences between host plants can lead to changes in morphological, phenological
or chemical attributes that constitute the range of resources and conditions that can be
exploited by arthropods.
Table 3. Mean (
±
standard deviation) of genetic diversity (He) and concentration of secondary
metabolites (SMs) per taxa (Quercus glabrescens,Q. rugosa and hybrid). Kruskal–Wallis results to
determine the effect of oak taxa on genetic diversity and concentration of SMs (rutin, quercetin, caffeic
acid, scopoletin, kaempferol glucoside, quercitrin).
Taxa
Genetic
Diversity Rutin Caffeic Acid Quercetin Quercitrin Kaempferol
Glucoside Scopoletin
(He) (H2, 48) (H2, 48 ) (H2, 48) (H2, 48) (H2, 48 ) (H2, 48)
Detection limit
(mg/g) 3.701 1.232 3.234 1.348 2.374 1.455
Q. rugosa 0.637 a 4.90 ±0.20 a 3.59 ±0.35 a 5.78 ±0.23 a 16.46 ±1.53 a 10.65 ±2.00 ab 8.25 ±0.96 a
Q. glabrescens 0.447 b 3.37 ±0.40 b 2.75 ±0.35 ab 3.55 ±0.03 b 6.64 ±0.39 b 5.95 ±0.51 b 2.62 ±0.16 b
Hybrid 0.699 c 0.0 c 1.87 ±0.44 b 4.17 ±0.12 c 2.44 ±0.09 c 8.47 ±0.29 a 1.49 ±0.24 c
Kruskal–Wallis 73.794 *** 28.852 *** 6.411 * 37.880 *** 38.470 *** 7.639 * 34.455 ***
Different letters show significant differences between taxa: p< 0.05. * = p< 0.05, *** = < 0.001.
3.2. Qualitative and Quantitative Variation of Secondary Metabolites
A total of six compounds have been identified for this white oak complex, all of
which were present in the three taxa analyzed (Table 3). These six compounds were
quantitatively characterized (mg/g extract) at the taxa level in the present study. It was
found that the concentrations of all the analyzed compounds were significantly different
between Q. rugosa and Q. glabrescens, and that Q. rugosa had the highest concentrations
of all the metabolites. The most important compounds, in terms of concentration, found
in Q. rugosa were quercetrin, kaempferol and scopoletin. In the case of Q. glabrescens, the
most important were quercetrin and kaempferol (Table 3). The concentration of caffeic
acid found in the hybrid taxa was different from that found in Q. rugosa but not from the
concentration found in Q. glabrescens; in the case of kaempferol, an inverse pattern was
found. With respect to quercetin, its concentration was between the concentrations found
in both parental species. The concentrations of quercetrin and scopoletin were below those
Diversity 2025,17, 62 8 of 25
found in both parental species. It is worth noting that the most important metabolites, in
terms of concentration, found in the hybrid taxa were kaempferol and quercetrin, in that
order. The results suggest that (a) the taxa has an effect on the quantitative expression
of the secondary metabolites under study and (b) it is possible to identify three patterns
of inheritance in the quantitative expression of the hybrid taxa: a dominant inheritance
pattern with respect to caffeic acid and kaempferol, since their concentrations were similar
to those found in some of the parental species; an intermediate inheritance pattern with
respect to quercetrin expression; and a subexpression pattern with respect to quercetrin
and scopoletin. Quantitative chemical changes in the host plants of the Q. glabrescens
×
Q.
rugosa complex can impact herbivorous insects either directly by causing antifeedant or
toxic effects upon ingestion or indirectly by attracting their natural enemies. These changes
may alter insect herbivory patterns and consequently impact the distribution, abundance
and diversity of arthropods.
3.3. Composition of the Community of Gall-Inducing Insects and Their Parasitoids
The canopy arthropod community associated with the Q. rugosa
×
Q. glabrescens
complex was characterized based on the analysis of 1082 galls belonging to 25 gall wasp
(Cynipidae) species. Twenty-two species were recorded in Q. rugosa; fifteen in hybrids; and
ten in Q. glabrescens; all species were grouped into 10 genera (Table 4, Figure 1).
Table 4. List of gall-inducing wasp species and their parasitoids associated with the Quercus rugosa
×
Q. glabrescens complex in Central Mexico. P is equal to the presence of the species.
Superfamily Family Genus Species Host Taxa
Q. rugosa Q. glabrescens Hybrid
Gall wasps
Cynipoidea Cynipidae Andricus A. sphaericus P P
A. nievesaldreyi P P
A. nr georgei P P
A. nr parmula P
A. nr sanchezi P P
A. sp1 P P P
A.nr P
Atrusca A.pictor P P P
A. grupo bulboides P P P
A. sp1 P P P
A. sp2 P P P
A. sp3 P P P
Cynips C. sp1 P P
C. sp2 P
C. sp3 P
C. sp4 P P
Disholcaspis D. sp1 P P
D. sp2 P
Dros D. perlentum P
Druon D. rasfiaum P
Estriatoandricus
E. georgei P P
E. fornesanus P
Ferum F. vitrium P
Kinseyella K. quercusobtusata P
Neuroterus N. sp1 P P P
Parasitoids
Chalcidoidea Eulophidae Baryscapus Baryscapus sp. P
Galeopsomia Galeopsomia sp. P P P
Eurytomidae Sycophila Sycophila sp. P
Eurytoma Eurytoma sp. P P
Ormyridae Ormyrus Ormyrus sp. P P
Torymidae Torymus Torymus sp. P P P
Diversity 2025,17, 62 9 of 25
Diversity 2025, 17, x FOR PEER REVIEW 10 of 26
Figure 1. Cont.
Diversity 2025,17, 62 10 of 25
Diversity 2025, 17, x FOR PEER REVIEW 11 of 26
Figure 1. Gall-inducing wasps found in Q. glabrescens × Q. rugosa complex.
3.4. Effect of Genetic Diversity and the Expression of Secondary Metabolites on the Communities
of Gall-Inducing Insects and Parasitoids
The results show that Q. rugosa had the highest values in all the community parame-
ters analyzed, and these values differed statistically from those reported for Q. glabrescens
and the hybrid taxa (Table 5). In contrast, there were no significant differences in any of
the parameters evaluated between the laer two taxa. Thus, the results of this study sug-
gest the following: (a) an effect of the host taxa on the parameters that characterize the
community of gall-inducing insects and parasitoids; (b) a dominant inheritance paern
with respect to the susceptibility of the hybrid taxa to the arthropods associated with its
canopy, as this susceptibility did not differ from that found in the parental species Q. gla-
brescens. Our results suggest that the gall-inducing insect community associated with hy-
brids is similar in structure and diversity to the parental species Q. glabrescens.
Figure 1. Gall-inducing wasps found in Q. glabrescens ×Q. rugosa complex.
The most representative genera in terms of the species were Andricus (n= 12)
>Atrusca =Cynips (n= 4) > Estriatoandricus (n= 2), Ferum (n= 1) = Kinseyella (n= 1)
=Neuroterus (n= 1). In terms of abundance, the wasp species with the greatest number
of individuals were Disholcaspis sp3 (386), Neuroterus sp1 (339) and Andricus georgei (177).
Inquiline wasps of the genus Synergus emerged from 2.5% of all the collected galls; these
wasps were not included in the analysis. Furthermore, parasitic insects were present in
24.3% of all the collected galls. At the family level, Eulophidae and Eurytomidae were
the most representative, with two genera of parasitoids each. For their part, Ormyridae
and Torymidae only registered one genera of parasitoids each (Table 4).
Diversity 2025,17, 62 11 of 25
3.4. Effect of Genetic Diversity and the Expression of Secondary Metabolites on the Communities of
Gall-Inducing Insects and Parasitoids
The results show that Q. rugosa had the highest values in all the community parameters
analyzed, and these values differed statistically from those reported for Q. glabrescens and
the hybrid taxa (Table 5). In contrast, there were no significant differences in any of the
parameters evaluated between the latter two taxa. Thus, the results of this study suggest the
following: (a) an effect of the host taxa on the parameters that characterize the community
of gall-inducing insects and parasitoids; (b) a dominant inheritance pattern with respect to
the susceptibility of the hybrid taxa to the arthropods associated with its canopy, as this
susceptibility did not differ from that found in the parental species Q. glabrescens. Our
results suggest that the gall-inducing insect community associated with hybrids is similar
in structure and diversity to the parental species Q. glabrescens.
Table 5. ANOVA results to determine the effect of oak taxa (Quercus rugosa,Q. glabrescens and
hybrid) on abundance, infestation percentage, species richness (mean
±
standard deviation) and
Shannon–Wiener diversity index (H’) of canopy gall-inducing wasps and their parasitoids.
Abundance
Infestation (%)
Richness Diversity (H’)
Gall wasps
Q. rugosa 31.85 ±4.44 a 15.95 ±2.22 a 6.30 ±0.51 a 2.492 A
Q. glabrescens 12.35 ±2.20 b 6.17 ±1.10 b 1.90 ±0.39 b 0.821 B
Hybrid 5.35 ±1.35 b 2.67 ±0.67 b 2.25 ±0.39 b 2.429 A
Anova (F2,97) 14.979 *** 15.717 *** 29.644 ***
Parasitoids
Q. rugosa 6.50 ±1.15 a 23.16 ±3.49 a 1.42 ±0.14 a 0.620 AB
Q. glabrescens 0.70 ±0.27 b 9.46 ±3.88 b 0.25 ±0.07 b 0.905 A
Hybrid 0.75 ±0.42 b 11.38 ±5.80 b 0.25 ±0.09 b 0.362 B
Anova (F2,97) 41.359 *** 6.282 * 89.138 ***
Different small letters show significant differences at p< 0.05 (Tukey’s honestly significant differences test);
different capital letters show significant differences at p< 0.05 ([82]δtest). * = p< 0.05, *** = < 0.001.
The results of the network analysis show that the He of the Q. glabrescens
×
Q. rugosa
complex had a significant effect on the quantitative expression of four of the six SMs
analyzed. Quercetin glucoside, kaempferol glucoside and scopoletin were positively
influenced (Figure 2), whereas caffeic acid was negatively influenced (Figure 3).
Furthermore, it was found that He had a positive and significant effect on the abun-
dance and richness of gall-inducing insects and parasitoids. However, according to the
normalized values (Nvs), the magnitude of the influence of the oak host genetic diversity
has the following pattern: abundance and richness of gall insects > abundance and richness
of parasitoid insects > SMs (Figure 2). Even so, five out of six SMs analyzed (83.33%) had
an influence on some of the parameters of the gall insects community. It was found that
scopoletin, quercetin glucoside and caffeic acid had a significant and positive influence on
the abundance of these insects. Similarly, rutin and quercetin glucoside positively affected
the richness of gall-inducing species. In contrast, quercitrin and rutin had a negative
influence on the abundance of gall insects (Figures 2and 3). It is worth noting that, in
terms of normalized values (Nvs), the influence of the SMs showed the following pattern:
abundance > gall insect richness, regardless of direction. Finally, it was found that only
33.33% (two out of six) of the SMs analyzed had an influence on the parameters that charac-
terize the parasitoid insect community. It was found that quercitrin had a positive influence
on the abundance and richness of parasitoids, while scopoletin negatively affected both
parameters (Figures 2and 3).
Diversity 2025,17, 62 12 of 25
Diversity 2025, 17, x FOR PEER REVIEW 12 of 26
Table 5. ANOVA results to determine the effect of oak taxa (Quercus rugosa, Q. glabrescens and hy-
brid) on abundance, infestation percentage, species richness (mean ± standard deviation) and Shan-
non–Wiener diversity index (H’) of canopy gall-inducing wasps and their parasitoids.
Abundance Infestation (%) Richness Diversity (H’)
Gall wasps
Q. rugosa 31.85 ± 4.44 a 15.95 ± 2.22 a 6.30 ± 0.51 a 2.492 A
Q. glabrescens 12.35 ± 2.20 b 6.17 ± 1.10 b 1.90 ± 0.39 b 0.821 B
Hybrid 5.35 ± 1.35 b 2.67 ± 0.67 b 2.25 ± 0.39 b 2.429 A
Anova (F
2,97
) 14.979 *** 15.717 *** 29.644 ***
Parasitoids
Q. rugosa 6.50 ± 1.15 a 23.16 ± 3.49 a 1.42 ± 0.14 a 0.620 AB
Q. glabrescens 0.70 ± 0.27 b 9.46 ± 3.88 b 0.25 ± 0.07 b 0.905 A
Hybrid 0.75 ± 0.42 b 11.38 ± 5.80 b 0.25 ± 0.09 b 0.362 B
Anova (F
2,97
) 41.359 *** 6.282 * 89.138 ***
Different small leers show significant differences at p < 0.05 (Tukey’s honestly significant differ-
ences test); different capital leers show significant differences at p < 0.05 ([82] δ test). * = p < 0.05, ***
= < 0.001.
The results of the network analysis show that the He of the Q. glabrescens × Q. rugosa
complex had a significant effect on the quantitative expression of four of the six SMs ana-
lyzed. Quercetin glucoside, kaempferol glucoside and scopoletin were positively influ-
enced (Figure 2), whereas caffeic acid was negatively influenced (Figure 3).
Figure 2. Network related to the positive influence between host oak [genetic diversity (He), sec-
ondary metabolites (rutin, caffeic acid, quercetin glucoside, quercitrin, kaempferol glucoside, sco-
poletin)] and the richness (S) and abundance of canopy gall-inducing wasps and their parasitoids.
Nv = normalized value (from 0 to 1), where (1) in the range [0.0–0.22], the influence is very low; (2)
in the range [0.22–0.44], the influence is low; (3) in the range [0.44–0.66], there is a medium influence;
Figure 2. Network related to the positive influence between host oak [genetic diversity (He), sec-
ondary metabolites (rutin, caffeic acid, quercetin glucoside, quercitrin, kaempferol glucoside, scopo-
letin)] and the richness (S) and abundance of canopy gall-inducing wasps and their parasitoids.
Nv = normalized value (from 0 to 1), where (1) in the range [0.0–0.22], the influence is very low; (2) in
the range [0.22–0.44], the influence is low; (3) in the range [0.44–0.66], there is a medium influence;
(4) in the range [0.66–0.88], the influence is high; and (5) in the range [0.88–1], the influence is
very high.
The network results show that the range of normalized values [0.66–0.88] is of
interest (Figure 4). This is the case for the following relationships depicted in the network
related to positive influences, all of them converging in the abundance of gall-inducing
wasps: (a) quercetin glucoside
→
abundance of gall-inducing wasps = 0.726, (b) scopoletin
→
abundance of gall-inducing wasps = 0.888, (c) caffeic acid
→
abundance of gall-inducing
wasps = 0.651 (this value is very close to the high-influence zone), (d) He
→
abundance of
gall-inducing insects = 0.644 (this value is very close to the high-influence zone) (Figure 2).
Derived from these relationships, we can conclude that three SMs contribute importantly
to the abundance of gall-inducing wasps. This condition gives special importance to the
role of SMs in the abundance of gall-inducing wasps.
Diversity 2025,17, 62 13 of 25
Diversity 2025, 17, x FOR PEER REVIEW 13 of 26
(4) in the range [0.66–0.88], the influence is high; and (5) in the range [0.88–1], the influence is very
high.
Figure 3. Network related to the negative influence between host oak [genetic diversity (He), sec-
ondary metabolites (rutin, caffeic acid, quercetin glucoside, quercitrin, kaempferol glucoside, sco-
poletin)] and the richness (S) and abundance of canopy gall-inducing wasps and their parasitoids.
Nv = normalized value (from 0 to 1), where (1) in the range [0.0–0.22], the influence is very low; (2)
in the range [0.22–0.44], the influence is low; (3) in the range [0.44–0.66], there is a medium influence;
(4) in the range [0.66–0.88], the influence is high; and (5) in the range [0.88–1], the influence is very
high.
Furthermore, it was found that He had a positive and significant effect on the abun-
dance and richness of gall-inducing insects and parasitoids. However, according to the
normalized values (Nvs), the magnitude of the influence of the oak host genetic diversity
has the following paern: abundance and richness of gall insects > abundance and rich-
ness of parasitoid insects > SMs (Figure 2). Even so, five out of six SMs analyzed (83.33%)
had an influence on some of the parameters of the gall insects community. It was found
that scopoletin, quercetin glucoside and caffeic acid had a significant and positive influ-
ence on the abundance of these insects. Similarly, rutin and quercetin glucoside positively
affected the richness of gall-inducing species. In contrast, quercitrin and rutin had a neg-
ative influence on the abundance of gall insects (Figures 2 and 3). It is worth noting that,
in terms of normalized values (Nvs), the influence of the SMs showed the following pat-
tern: abundance > gall insect richness, regardless of direction. Finally, it was found that
only 33.33% (two out of six) of the SMs analyzed had an influence on the parameters that
characterize the parasitoid insect community. It was found that quercitrin had a positive
influence on the abundance and richness of parasitoids, while scopoletin negatively af-
fected both parameters (Figures 2 and 3).
The network results show that the range of normalized values [0.66–0.88] is of inter-
est (Figure 4). This is the case for the following relationships depicted in the network re-
lated to positive influences, all of them converging in the abundance of gall-inducing
Figure 3. Network related to the negative influence between host oak [genetic diversity (He), sec-
ondary metabolites (rutin, caffeic acid, quercetin glucoside, quercitrin, kaempferol glucoside, scopo-
letin)] and the richness (S) and abundance of canopy gall-inducing wasps and their parasitoids.
Nv = normalized value (from 0 to 1), where (1) in the range [0.0–0.22], the influence is very low; (2) in
the range [0.22–0.44], the influence is low; (3) in the range [0.44–0.66], there is a medium influence;
(4) in the range [0.66–0.88], the influence is high; and (5) in the range [0.88–1], the influence is
very high.
In the case of the network of negative influences, the influence of SMs scopoletin
on the richness and abundance of gall parasitoids is noteworthy. The value of Nv in
these relationships is located in the zone of high influence. The negative influence of the
quercitrin metabolite in the abundance of gall-inducing wasps is specially highlighted,
because the value of the Nv is very close to the zone of very high influence (Figure 3).
These findings suggest that the variation in SMs concentrations in the host plants of the
Q. glabrescens
×
Q. rugosa complex is influenced by genetic factors, and that plant chemistry
serves as an intermediary connecting plant genes to the herbivore community and its
associated parasitoids.
Diversity 2025,17, 62 14 of 25
Diversity 2025, 17, x FOR PEER REVIEW 14 of 26
wasps: (a) quercetin glucoside → abundance of gall-inducing wasps = 0.726, (b) scopoletin
→ abundance of gall-inducing wasps = 0.888, (c) caffeic acid → abundance of gall-induc-
ing wasps = 0.651 (this value is very close to the high-influence zone), (d) He → abundance
of gall-inducing insects = 0.644 (this value is very close to the high-influence zone) (Figure
2). Derived from these relationships, we can conclude that three SMs contribute im-
portantly to the abundance of gall-inducing wasps. This condition gives special im-
portance to the role of SMs in the abundance of gall-inducing wasps.
Figure 4. Function that models the behavior of the relationships depicted in the network related to
the influences. The X axis shows the normalized values (Nvs) between 0 and 1. The sigmoid function
models the behavior of the relationships through qualitative values, which are easier to interpret.
We define five zones that represent the influence of the independent variable X on the dependent
variable Y, which are (1) in the range [0–0.22], the influence of X on Y is very low; (2) in the range
[0.22–0.44], the influence is low; (3) in the range [0.44–0.66], there is a medium influence; (4) in the
range [0.66–0.88], the influence is high; and (5) in the range [0.88–1], the influence is very high. See
Appendix C for more details.
In the case of the network of negative influences, the influence of SMs scopoletin on
the richness and abundance of gall parasitoids is noteworthy. The value of Nv in these
relationships is located in the zone of high influence. The negative influence of the quer-
citrin metabolite in the abundance of gall-inducing wasps is specially highlighted, because
the value of the Nv is very close to the zone of very high influence (Figure 3). These find-
ings suggest that the variation in SMs concentrations in the host plants of the Q. glabrescens
× Q. rugosa complex is influenced by genetic factors, and that plant chemistry serves as an
intermediary connecting plant genes to the herbivore community and its associated para-
sitoids.
4. Discussion
Figure 4. Function that models the behavior of the relationships depicted in the network related
to the influences. The Xaxis shows the normalized values (Nvs) between 0 and 1. The sigmoid
function models the behavior of the relationships through qualitative values, which are easier to
interpret. We define five zones that represent the influence of the independent variable Xon the
dependent variable Y, which are (1) in the range [0–0.22], the influence of Xon Yis very low; (2) in
the range [0.22–0.44], the influence is low; (3) in the range [0.44–0.66], there is a medium influence;
(4) in the range [0.66–0.88], the influence is high; and (5) in the range [0.88–1], the influence is very high.
See Appendix Cfor more details.
4. Discussion
The present study analyzed simultaneously the impact of genetic diversity (He,
modified by hybridization events) and the expression (quantitatively) of six foliar SMs
(flavonoid and coumarin) on the arthropod communities of two trophic levels associated
with a white oak canopy complex: gall–inducing wasps (herbivores) and their associated
parasitoids (predators).
4.1. Genetic Diversity and Secondary Metabolite Expression
Recent studies have reported that the He of some oak taxa oscillates between
0.25 and 0.88 [
26
,
85
–
87
]. In the present work, we found that Q. rugosa,Q. glabrescens
and their hybrids presented He values of 0.43, 0.47 and 0.69, respectively, data that are
in accordance with previous reports. Moreover, our results showed that the hybrid taxa
presented the highest He values in comparison with both parental taxa. This result is
consistent with other reports for oak populations where hybrids have been detected [
26
,
88
].
It has been suggested that hybrid taxa constitute new genetic variants that result from the
pool genetic combination of their parental taxa, a condition that is expressed in a higher
level of genetic diversity [26].
In general, it has been reported that the expression of SMs in plants, including
oak species, has an important genetic component [
29
,
89
]; we analyzed flavonoid and
coumarin expression, considering the existing information about their expression and
inheritability [90]
that suggests that both parameters are strongly determined by genetic
Diversity 2025,17, 62 15 of 25
factors [
13
,
91
–
93
]. In this context, Klaper et al. [
94
] found that at least seven phenolic
compounds have a high probability of being inheritable in Q. laevis. Specifically, the authors
reported that the expression of these compounds in this oak species is the result of an
additive genetic variability pattern.
In a previous study, Castillo-Mendoza et al. [
43
] documented the presence of nine
SMs (eight phenolic compounds and one coumarin) in the Q. glabrescens
×
Q. rugosa com-
plex. Following the same methodology, it was possible to identify two more compounds,
kaempferol glucoside (phenolic compound) and scopoletin (coumarin). The quantitative
analysis of the caffeic acid, quercetin glucoside, rutin and quercitrin (characterized by
Castillo-Mendoza et al. [
43
]) and both compounds identified in the present work revealed
that hybridization between Q. glabrescens and Q. rugosa affects the quantitative expression
of the SMs analyzed. Particularly, it was found that the hybrid taxa show three patterns
of SMs expression: dominant, intermediate and subexpression. This finding is in accor-
dance with the scientific literature, where the first two patterns are the most common in
plants [
38
,
39
]. Also, Rehill et al. [
95
], using the previously mentioned methodology, found
that the heritability of phenolic compounds is controlled by dominant genes, although the
development strategies differ between hybrid and parental taxa.
The subexpression pattern found for quercitrin and scopoletin can be explained as
follows: (a) the low concentration of these compounds on foliar tissue, that makes it
undetectable (optimal defense theory [
96
]); (b) hybridization may modify the metabolic
route that drives to its quantitative expression [
97
]; and (c) point mutations in biosynthetic
genes because of interspecific gene flow. Finally, Cheynier et al. [
98
] mentioned that
phenolic compound expression is produced mainly through changes in the transcription
rate of biosynthetic genes. Such factors are highly sensitive to changes in their components.
Hence, if hybridization processes alter any of the basic components of the metabolic route,
this change may in turn repress the expression of the final product, such as in the case of
rutin in our study.
4.2. Characterization of Gall-Inducing Insect Community and Their Parasitoids
In the present study, we documented the highest species richness of gall-inducing in-
sects associated with Q. rugosa and the lowest species richness associated with Q. glabrescens.
This pattern may be explained by their contrasting geographic range distribution in Mexico.
For example, Q. rugosa is distributed along 27 Mexican states [
99
], suggesting the environ-
mental heterogeneity in which this species distributes itself, resulting in its high phenotypic
plasticity. It has been documented that a higher phenotypic plasticity of oak host canopies
may result in more resources and conditions, creating a higher number of microhabitats
for gall-inducing wasps [
33
]. Moreover, in accordance with the international oak society,
Q. rugosa participates in hybridization events with at least five other white oak species not
including Q. glabrescens. These events may contribute to a wider range of resources and
conditions that Q. rugosa is offering to its canopy insects. On the contrary, Q. glabrescens
is distributed along nine Mexican states and at altitudes higher than 2500 m; therefore,
this may limit gall-inducing wasp establishment, due to a reduction in their colonization
areas. Moreover, due to the environmental and geographical conditions in which this
oak species distributes itself, its associated insects should have particular characteristics
that allows them to establish themselves [
100
]. Pascual-Alvarado et al. [
101
] did not find
galls associated with Q. glabrescens. Finally, a pattern of dominant heritage was docu-
mented for the hybrid taxa because the analyzed parameters for both gall-inducing insects
and their parasitoids did not differ from the parameters reported for the parental species
Q. glabrescens. This result agrees with reports where this genetic pattern is the most common
found in plants [38,39].
Diversity 2025,17, 62 16 of 25
Another result is that we found six parasitoid genera (grouped in four families)
associated with 18 gall species. For example, Serrano-Muñoz [
102
] reported the presence
of nine parasitoid genera associated with six gall wasp genera (in 17 oak species). Also,
Valencia-Cuevas et al. [
9
] registered the presence of 10 genera associated with 18 gall species
(in Q. castanea). It has been suggested that three key factors influence parasitoid community
structure: (1) spatiotemporal niche traits define the distribution of hosts in space (oak taxon
galled, location of the gall on the oak) and time (season and duration of development) that
determine the likelihood of recognition by parasitoids; (2) resource traits define the quality
of the host resource per gall (number of hosts per gall, host size) potentially available to
parasitoids; and (3) gall morphology traits capture variation in the structure of the gall
tissues parasitoids must penetrate to access the host resources, acting as direct defenses
against particular natural enemies [
103
]. These groups of traits affect parasitoid success
in host detection (spatiotemporal niche) and host exploitation (resource, morphology),
respectively [
104
]. Also, these results highlight the need for more sampling. Specifically, in
this work we found a positive and significant relationship between gall-inducing insects
and parasitoid richness, a fact that suggests that this variation in parasitoid species richness
may be directly related to the resources that gall species offer (the number of hosts per gall,
host size), as mentioned. In the future, it would be useful to test these hypotheses.
In this study, we found three parasitoid genera (Torymus,Ormyrus and Eurytoma), in
addition to Sycophila, which has also been reported in red oaks [
9
,
105
], a fact that may
suggest that these insects may be generalists, independently of if they establish on red or
white oaks. In the case of Baryscapus and Galeopsomyia, they were found only established
on white oaks [105], supposing a certain degree of specificity.
4.3. Effect of Genetic and Chemical Diversity on Gall-Inducing Insect Community and
Their Parasitoids
The network analysis showed the magnitude and direction of the relationships be-
tween genetic diversity (He), SMs (flavonoids) and the gall-inducing insect community
and their parasitoids (abundance and richness) associated with the Q. glabrescens
×
Q.
rugosa complex. Specifically, we found that He had a positive effect on tree SMs: quercetin
glucoside, kaempferol glucoside, scopoletin. In contrast, a negative influence was found on
caffeic acid. These results are in agreement with studies that report that the expression and
heritability of these SMs in plants are strongly determined by genetic factors [
91
–
93
]. In the
case of caffeic acid, this compound is a precursor of different flavonoids and coumarins (the
Shikimic acid pathway [
105
,
106
]), and it is not a final product of this route. Hence, we can
suggest that the decrease in caffeic acid concentration (negative influence), along with the
increase in the genetic diversity levels of the analyzed taxa, may be because this compound
is being used as a precursor for quercetin glucoside, scopoletin and kaempferol glucoside
production, a fact that could also explain the increase in these compounds (positive influ-
ence) as genetic diversity increases. Also, we found that He had a positive and significant
effect on the abundance and richness of gall-inducing insects. Similar results have been
registered in phytophagous insect communities associated with different plant species (e.g.,
poplars [
16
]; eucalyptus [
107
]; willows [
108
]; and oaks [
79
]). For example, Valencia-Cuevas
et al. [
9
] found that the genetic diversity of the oak host species Q. castanea had a positive
and significant influence on richness and endophagous insect density (Cynipidae). An
increase in host plant genetic diversity can enhance their architectural complexity and
nutritional quality [
109
], which subsequently favors a greater abundance of herbivorous
insects [
110
] due to an increase in resources and conditions that they can employ [
8
]. Addi-
tionally, higher genetic diversity can alter the arthropod community structure by affecting
the host plant’s resistance or susceptibility to herbivores, as well as the herbivores’ ability
to recognize the host plant as a suitable host [
111
]. Moreover, it has been reported that
Diversity 2025,17, 62 17 of 25
primary productivity increases as genetic diversity also increases, so a higher number of
individuals and arthropod species can be supported by plants with higher levels of genetic
diversity [112].
Additionally, we found that the positive effect of oak host genetic diversity scaled up
to the next trophic level: the richness and abundance of insects and parasitoids. It has been
proposed that direct effects that have a genetic basis in plants also influence the next trophic
level [
32
]. Under this scenario, we expected that richness and gall insect abundance would
be influenced directly by the genetic traits of the host plant, but also those genetic traits
would have an influence on the parasitoid insect community. This last hypothesis was
supported by our results, since the network analysis evidenced that the host taxa He had a
positive and significant influence on two parameters of the parasitoid insect community.
These last results are in accordance with Bailey et al. [
113
], Johnson [
114
] and Valencia-
Cuevas et al. [
9
], who suggest that genetic variation in plants may be a determinant factor
that regulates herbivore population dynamics and interactions between plants, herbivores
and parasitoids.
Although host genetic diversity had a positive and significant influence on herbivores
and their parasitoid community, in agreement with the Nv values, the host genetic diversity
influence pattern found in our study is as follows: abundance and richness of gall-inducing
insects > abundance and richness of parasitoid insects. This pattern may be explained
because herbivores obtain resources directly from their host plants [
115
]. So, genetic and
chemical changes in host plants will have direct consequences and a greater magnitude
of influence on their associated herbivores than on parasitoid communities. Also, we
found that the abundance and richness of parasitoid insects were affected positively. This
last result is in accordance with Koricheva and Hayes [
116
], who evidenced through a
meta-analysis the positive effects of the genetic diversity levels of the host plant on predator
and parasitoid arthropods.
In this study, we detected quantitative chemical changes in the host plants of the
Q. glabrescens
×
Q. rugosa complex. This condition can impact herbivorous insects either di-
rectly by causing antifeedant or toxic effects upon ingestion or indirectly by attracting their
natural enemies [
117
]. These changes may alter insect herbivory patterns and consequently
impact the distribution, abundance and diversity of these arthropods and their associated
parasitoids. An influence analysis also showed the magnitude and direction of the SMs
effect on arthropods associated with the Q. glabrescens
×
Q. rugosa complex. In terms of nor-
malized values (Nvs), SMs influence registered the next pattern: abundance and richness
of gall-inducing insects > abundance and richness of parasitoid insects, independently of
the direction. This pattern may be explained when considering that herbivores have a more
direct influence on their host plant attributes, such as SMs, in comparison to parasitoid
insects that depend more on their direct resources, which are these herbivores. This is also
supported by the fact that 83.33% of the SMs analyzed had an influence on gall-inducing
insects and only 33.33% affected parasitoid insects. Stahl and co-workers [
118
] documented
that the interaction of herbivore–plant is highly dependent on mechanisms that are related
to SMs, specifically in toxification–detoxification mechanisms. Parasitoids can be attracted
by the emission of volatile compounds that enable them to detect potential prey, a fact that
could indirectly regulate the success of herbivore attacks in some species [
119
,
120
]. We do
not know that other cues are at play in this system; however, in the literature it has been
reported that in addition to olfactory stimulus, parasitoid searching and host location is
influenced by other external stimuli such as visual ones (e.g., shoots containing developing
galls or free of galls but with expanded leaves), tactile one (vibrational sounding) and even
cues of CO
2
(that signal locations of actively respiring gall larvae/pupae) [
121
,
122
]. Also,
our analysis showed that caffeic acid, scopoletin and quercetin glucoside had a positive and
Diversity 2025,17, 62 18 of 25
significant influence on gall insect abundance. In general, it is known that caffeic acid may
favor scopoletin expression [
123
], which has antifungal and antibacterial properties [
124
].
For example, scopoletin is a phenolic coumarin that can be isolated from various plant
species [
125
], and it has been proposed as an important phytoalexin against pathogens [
124
].
For wild tobacco (Nicotiana attenuata), it has been documented that scopoletin possessed
antifungal activity against the necrotrophic fungus Alternaria alternata,
in vitro
and
in vivo
conditions [
126
]. In this context, it has been reported that for cynipids the fungal mortality
is ecologically significant, and the host flavonoids (as tannins) may serve a defensive func-
tion, helping to reduce the levels of fungal infestation, as reported for the cynipid gall wasp
Dryocosmus dubiosus associated with Q. agrifolia and Q. wislizenii [
127
]. So, this metabolite
may increase the resistance to fungi attacks, enabling gall wasps to complete their life cycle;
however, to probe this hypothesis, it would be necessary to carry out studies to know
whether the gall insects feeding on these oaks containing these compounds. For the case of
quercetin glucoside, it has been reported that this is a metabolite that can be a feeding stim-
ulant for herbivore insects [
128
]. This response was observed in the larvae of the silkworm
Bombyx mori fed with the foliar tissue of its host the mulberry tree,
Morus alba [129]
, and in
the Western corn root worm Diabrotica virgifera, which feeds on the pollen of the sunflower
Helianthus annuus L. [130].
Quercitrin also had a positive and statistically significant effect on richness and para-
sitoid abundance. Possibly, the expression of this particular SM may be part of the indirect
defense of the plant, resulting in the attraction of different parasitoid species and/or
predators [131,132].
So, an increase in the concentration of this SM may help oak host species to reduce
the virulence of gall wasps, favoring the abundance and diversity of parasitoid insects.
Similarly, rutin and quercetin glucoside positively affected gall species richness. In contrast,
quercitrin and rutin had a negative influence on gall-inducing insect abundance. In this
sense, it is important to mention the biological properties of these compounds; it has
been reported that rutin and quercetin glucoside had a positive impact on the richness of
gall-inducing insects, probably because they act as feeding cues or stimulants influencing
insect feeding behavior, favoring more species on the host plant [
133
]. In contrast, rutin
and quercitin had a negative influence on gall wasp abundance, perhaps because these
SMs affect the growth, survival and development of herbivores, being lethal at high
concentrations [134,135].
On the other hand, caffeic acid has an influence on the feeding, growth and sur-
vival rates of generalist insects and on the reproductive structures of fungi and bacteria
(bacteriostatic or bactericidal effects) [
136
–
138
]. The last mentioned effects may have a
negative impact on secondary fauna (mites, spiders and different predators) and on gall
decomposition rates, enabling the development of more diverse communities with a higher
abundance, in comparison to those that do not express this particular SM.
Finally, scopoletin had a negative impact on richness and on parasitoid abundance.
Diverse studies have documented that this SM reduces female fecundity and longevity [
107
],
a fact that suggests that the negative effects have an impact only on parasitoids, and
as documented earlier, scopoletin impacts positively on gall wasp abundance, possibly
because of the elimination of their natural predators. However, more experiments are
needed to increase our knowledge about how insects not only perceive these metabolites,
but also how they utilize them. This would help us understand more completely the role
they play in plant–insect interactions.
Diversity 2025,17, 62 19 of 25
5. Conclusions
The results obtained in the present study show that all the aims of the present study
were addressed. Specifically, that an increase in oak host genetic diversity as a result of
hybridization events influences the expression of SMs with high heritability rates, as well
as having negative effects on the herbivore and parasitoid communities of host plants.
These findings demonstrate the importance that genetic and secondary chemical diversity
has on the plant–herbivore–parasitoid interactions. Hence, the loss of the genetic diversity
levels of host plants may result in a loss of arthropod species along trophic levels, a fact that
comprises the ecosystem function. Moreover, hybridization events between Q. glabrescens
and Q. rugosa promoted quantitative differences in the pattern of SM expression in their
hybrids. Regarding the construction of networks related to these positive and negative
influences, they allowed the building of influence pathways to facilitate the analysis of the
influence of genetic diversity and host plant SMs on the richness and abundance of gall
inductors and their parasitoids.
Author Contributions: Conceptualization, E.T.-S.; methodology, E.C.-M. and A.Z.; validation, E.T.-S.;
formal analysis, E.T.-S. and F.R.-Q.; investigation, E.C.-M. and L.V.-C.; resources, E.T.-S. and P.M.-G.;
data curation, E.C.-M., J.P.-V. and M.S.-M.; writing—original draft preparation, E.C.-M.; writing—
review and editing, E.T.-S., L.V.-C. and P.M.-G.; supervision, E.T.-S. All authors have read and agreed
to the published version of the manuscript.
Funding: This work was supported by CONAHCyT, Mexico (Grants 440788) under the pro-
gram “Programa de Becas Posdoctorales” through a postdoctoral fellowship granted to Elgar
Castillo Mendoza.
Institutional Review Board Statement: Not applicable.
Data Availability Statement: The data that support the findings of this study are available from the
corresponding author upon reasonable request.
Acknowledgments: To CONAHCyT for a postdoctoral grant to E.C.-M. (440788). Zamilpa Alejandro
thanks the IMSS foundation. We also thank Gabriel Flores, Joel Castañeda and Claudia Cerezo for lab
and field assistance.
Conflicts of Interest: The authors declare no conflicts of interest.
Appendix A
UV spectra, chemical structure and chromatogram of phenolic compounds: quercetin-
3-O-rutinoside (= rutin) (1), caffeic acid (2), quercetin-3-O-glucoside (= quercetin)
(3), kaempferol-3-O-glucoside (= kaempferol glucoside) (4), quercetin-3-O-rhamnoside
(= quercitrin) (5) and scopoletin (6) present in Q. rugosa, hybrids and Q. glabrescens.
Appendix B
Retention time in minutes of the phenolic compounds characterized in three oak taxa
and the corresponding commercial reference (Sigma-Aldrich).
Appendix C
Conceptual development of the model. The way of quantifying the causal relationship
between two variables
Diversity 2025,17, 62 20 of 25
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